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Hydrometallurgy 202 (2021) 105603 Contents lists available at ScienceDirect HYDRO Hydrometallurgy MET ELSEVIER evier.com/locate/hydromet Electrochemical investigation of microbially and galvanically leached chalcopyrite C. Tanne, A. Schippers Federal Institute forGeosciences and NaturalResources (BGR),ResourceGeochemistry,Stilleweg 2,D-30655,Germany ARTICLEINFO ABSTRACT Keywords: The effect of the galvanic interaction between anodic chalcopyrite and cathodic pyrite was investigated by long- Galvanic corrosion term electrochemical measurements of the galvanic coupling current and verified by chemical leaching and Chalcopyrite bioleaching. For the first time galvanic corrosion measurements (in the absence and in the presence of micro- Pyrite Bioleaching organisms) over days are reported. Combined microbial and galvanic leaching of chalcopyrite showed increased Cu recovery in the presence of pyrite. Corrosion resulted in mineral dissolution depending on multiple param- Electrochemistry eters (like metal corrosion). However, maximal chalcopyrite dissolution via bioleaching occurred in the presence of a large cathodic pyrite surface. Highest copper recovery was observed in case of high rest potential differences between galvanically coupled minerals (pyrite coupled with copper concentrate). A comparison of electro- chemical data of this study with scientific literature revealed a wide range of rest potential data for a single metal sulfide. Fundamental research on galvanic interaction of mixed mineral systems need to focus on unified experimental parameters to allow a comparison. 1. Introduction approaches have become one of the major recent trends in bio- hydrometallurgy (Kaksonen et al., 2020). One of these approaches are Biomining, i.e. applied bioleaching or biooxidation, is performed as electrobioreactors, which raised increasing interest in the last three biohydrometallurgical processing of ores to recover valuable metals decades (Tanne and Schippers, 2019a). Such reactors are based on an such as Au, Co, Cu, Ni, U and Zn. The leaching is caused by redox re- externally forced shift of the electrochemical conditions within the actions at the liquid-solid interface, which results in the dissolution of reactor. However, a shift of the redox conditions on the mineral surface metal sulfides in the ore. The underlying mechanism can be described as can also occur spontaneously. This can be accomplished by galvanic a corrosion process. Thereby, microbial cells maintain the acidic and interactions between two or more minerals of different electrochemical oxidative environment, which promotes metal sulfide dissolution. The nature. This naturally occurring phenomenon was frequently investi- electron transfer between the attached microbial cells and the surface of gated in biohydrometallurgical research (Tanne and Schippers, 2019a). the mineral is mediated by the Fe3+ /Fe2+ redox couple. Such redox re- The driving force of the redox reactions is the difference between the lations can be monitored by potential or current measurements using minerals’ rest potentials in an electrolyte. By their rest potential dif- electrochemical techniques or influenced bye electrochemical ference, two connected minerals can be distinguished in a cathodically applications. protected and an anodically sacrificed mineral (Donati and Sand, 2007). The use of advanced electrochemical techniques is widely researched Provided that an electric and electrolytic contact is established between and applied in bioscience as bioelectrochemistry (Arduini et al., 2017; these two minerals, the anodic mineral is preferentially dissolved during Harnisch and Holtmann, 2019), in material science for corrosion leaching. Thus, conductive metal sulfides can be sorted by their rest investigation (Figueira, 2017; Payne et al., 2017) as well as in metal- potential under defined redox conditions similar to the galvanic series of lurgy for melting and deposition of metals (Popov et al., 2002). Conse- metals (Fig. 1). quently, an intersection of these disciplines, namely Metal sulfides such as sphalerite and chalcocite, which are very biohydrometallurgy, is well suited to implement electrochemical ap- susceptible to dissolution (susceptible to corrosion) - also referred to as proaches for the optimization of metal recovery. Thus, electrochemical "active" in corrosion electrochemistry - are ranked below the mineral * Corresponding author. E-mail address: Axel.Schippers@bgr.de (A. Schippers). https://doi.org/10.1016/j.hydromet.2021.105603 Received 24 January 2021; Received in revised form 31 March 2021; Accepted 3 April 2021 Available online 14 April 2021 0304-386X/? 2021 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http:/ org/licenses/by/4.0/) C. Tanne and A. Schippers Hydrometallurgy 202(2021) 105603 less susceptible to corrosion (more noble) 2. Material and methods 2.1.Material Metals A chalcopyrite sample consisted of hand selected pieces from an abandoned mine in Bad Grund (Cpy BG, Harz Mountains, Germany). A Platinum Pyrite (FeS2) second chalcopyrite sample originated from Quebec, Noranda Mines, Gold Canada (Cpy Que). The pyrite sample (P) consisted of cm-sized cubic Chalcopyrite (CuFeS2) Silver crystals from Navajun (Spain). Several pieces of each mineral sulfide Covellite (CuS) were used to produce mineral electrodes. Other pieces were ground and Titanium sieved for analyses and leaching experiments. Inductively coupled Copper Chalkocite (Cu2S) plasma - optical emission spectrometry (ICP-OES) was used to deter- mine the chemical elemental composition of each mineral sample after Tin Bornite (CusFeS4) dissolution in aqua regia. Additionally, silicon was determined by so- Lead dium peroxide fusion with subsequent inductively coupled plasma - Pentlandite (Fe,Ni)gS8 mass spectrometry (ICP-MS) and total sulfur was analyzed using a LECO Gusseisen Pyrrhotite (FeS to Fe1oS11) CS 230 carbon-sulfur analyzer. The chemical composition of the mineral Cast iron samples is given in Table 1. The main minerals chalcopyrite and pyrite Galena (PbS) were confirmed according to X-ray diffraction analysis (Supplementary Zinc Material Fig. S1-S3). Magnesium Sphalerite (ZnS) A copper concentrate was obtained from black shale ore deposits (KGHM, Poland). The concentrate had a particle size of <90 μm and consisted of pyrite and the copper sulfides chalcopyrite, bornite, chal- cocite and covellite in different quantities, and had the following elemental composition: 13.3 wt% Cu, 9.4 wt% Fe, 16.5 wt% S, 0.064 wt % Ag, 1.1 wt% total inorganic carbon and 9.1% total organic carbon more susceptible to corrosion (less noble,"active") (Hedrich et al., 2018). The sulfide mineral samples used for leaching experiments had these specific surface areas analyzed by Bru- Fig. 1. Schematic classification of some metals and mineral sulfides, which can nauer-Emmett-Teller (BET) measurement: Cpy BG 0.3 m?/g, pyrite (P) be used for a rough indication of cathodic and anodic electrode behavior in a 0.2 m²/g, copper concentrate 5.2 m2/g. Quartz (purity ≥99.8%) was galvanic cell. Environmental conditions are not considered here. purchased from Sigma-Aldrich (Germany). All powdered samples were sieved to obtain the 63 to 125 μm fraction for leaching experiments. sulfides pyrite and chalcopyrite which are less easily dissolvable. This has been done in the same manner for “more active" metals such as magnesium, aluminum and zinc which are ranked below more inert 2.2. Microbial culturing and leaching procedure metals such as gold or platinum. This compilation of data enables a Leaching experiments were performed aerobically at 42 °C in 100 ml rough prediction of galvanically assisted leaching behavior (Berry et al., shake flasks at 180 rpm with 50 ml basal salt medium containing 66 mg 1978; Mehta and Murr, 1982, 1983). The sequence in the galvanic series Na2SO4, 450 mg (NH4)2SO4, 50 mg KCl, 500 mg MgSO4 · 7 H2O, 50 mg depends on material properties and environmental conditions (such as temperature, pH value and solution redox potential).
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The galvanic behavior of mixed mineral systems and their role dur- Table 1 ing oxidative bioleaching have been thoroughly studied (Donati and Sand, 2007; Tanne and Schippers, 2019a), and the occurrence of Element Content [%] galvanic interactions between different minerals and their influence Chalcopyrite BG Chalcopyrite Que Pyrite during bioleaching processes are stated in several studies including Cu 31.2 27.8 Not detected bioleaching of chalcopyrite (e.g. Khoshkhoo et al., 2014; Zhao et al., S 31.1 36.5 53.6 2015; Liu et al., 2018; Saavedra et al., 2018). However, detailed elec- Fe 27.4 29.2 42.8 trochemical data are missing, e.g. the resting potential is frequently used 5 Not detected Not detected without confirming measurements and time-resolved measurements of Zn 0.73 2.85 <0.14 galvanic current are rare and often short (hours instead of days). How- A1 0.3 0.39 0.26 Pb 0.25 <0.2 <0.23 ever, leaching processes commonly run over days or even months. Mn 0.2 <0.2 <0.23 Therefore, this study focusses on spontaneous electrochemical effects K 0.06 <0.2 <0.23 during (bio)leaching of mineral sulfides. One of the most frequently Mg 0.06 <0.39 <0.46 described galvanically assisted bioleaching systems concerns the pro- Na 0.03 <0.2 <0.23 As 0.01 0.75 <0.29 cessing of cathodic pyrite in the presence of anodic “sacrificed” chal- Ni 0.01 <0.08 <0.09 copyrite (or secondary copper sulfides). Considering this case, this study Cd 0.01 0.05 0.05 provides more detailed time-resolved electrochemical data in the pres- Ag 0.004 0.06 0.03 ence and in the absence of leaching microorganisms. This study aims to Ba 0.004 <0.01 <0.01 Be 0.002 <0.01 <0.01 investigate the actually measurable parameters of galvanic interaction. Co 0.002 <0.08 <0.09 Furthermore, it is considered whether galvanic effects are also evident in Cr 0.002 <0.04 <0.05 the leaching results and whether other factors influence the controlled Mo 0.001 <0.1 <0.11 simultaneous leaching of various minerals. For this purpose, chalcopy- Sr 0.001 <0.001 <0.002 rite from different sources was investigated covering different electro- Ca <0.26 <0.39 <0.46 chemical activities of this most important mineral for copper recovery. Bi <0.01 0.23 0.23 T1 <0.01 <0.2 <0.23 Li <0.01 <0.01 <0.01 V <0.004 <0.14 <0.16 C. Tanne and A. Schippers Hydrometallurgy 202 (2021) 105603 KH2PO4 and 14 mg Ca(NO3)2 · 4 H2O per liter. For bioleaching an diameter) and the top was covered with conductive silver lacquer to acidophilic, moderately thermophilic mixed culture of iron- and sulfur- increase the electrical contact area. This rod was combined with a plastic oxidizing bacteria was used comprising Sulfobacillus (Sb.) thermosulfi- tube (5 mm inner diameter). This combination formed the basic working dooxidans, Sb. acidophilus, Sb. benefaciens, Leptospirillum ferriphilum and electrode with a cavity in the front, which was identical for all working Acidithiobacillus caldus. The mixed leaching culture was adapted to 5 g electrodes. Current densities were calculated for the circular 5 mm chalcopyrite in 50 ml medium (10% pulp density) by several transfers of diameter surface (electrode surface of 0.196 cm2). the active culture based on previous results in our laboratory (Hedrich Unprocessed mineral samples and leaching residues were used to et al., 2016, 2018). This pulp density was used in all leaching experi- produce the carbon paste electrodes and electrochemically investigated ments, too. For the variation of the anodic and cathodic surface areas in as described in our previous study (Tanne and Schippers, 2019b). the galvanic leaching experiments different amounts of chalcopyrite BG Briefly, carbon paste material was prepared from 1 g of synthetic and pyrite were mixed. The composition of the 5 g leaching substrate graphite powder (7-11 μm, Alfa Aesar, Germany) and 860 mg paraffin varied. Samples were mixed and termed as shown in Table 2. oil (Fluka Analytical, Germany) which were formed into a carbon paste. Adjustment of pH was performed by adding sterile filtered 0.5 M Per single working electrode 216 mg of carbon paste were gently mixed H2SO4. Bioleaching assays were inoculated by the addition of 2.5 ml with 116 mg of sample. freshly grown mixed culture to 50 ml medium (5% inoculum, Tanne and Tafel plots were obtained by potentiodynamic polarization via Schippers, 2019a, 2019b). The inoculum had a cell concentration of scanning from an initial potential of -75 mV vs. open circuit potential to 2.5x108 ± 3.3x107 cell/ml. Abiotic leaching was performed in the same a final potential of +75 mV vs. open circuit potential with a scan rate of way as bioleaching, but without inoculation. Biotic and abiotic leaching 0.5 mV/s. Cyclic voltammetric measurements were initiated at the open experiments ran for 8 to 17 days. circuit potential and in the direction of positive potentials. Scans were Samples of the leaching solution were regularly taken, diluted (1:10) performed between -500 and 700 mV vs. Ag/AgCl/3 M NaCl with a in 0.64% nitric acid and analyzed via ICP-OES to determine the scan rate of 20 mV/s. Voltammetric and potentiodynamic measurements extracted Cu by measuring the Cu concentration in solution during the were performed in iron free microbial medium to prevent the electro- leaching process. To determine the ferrous and ferric iron concentration chemical investigation from overlaying signals of iron ions (redox sig- a photometrical ferrozine-based assay was used (Lovley and Phillips, nals and strongly shifted solution redox potential). 1987). The pH and solution redox potential were measured using a Pt The driving force of the galvanic effect, which triggers galvanically electrode vs. Ag/AgCl (filled with saturated KCl). Leaching residues catalyzed corrosion, results from the electrochemical potential differ- were dried at 105 °C for 12 h and were then stored under nitrogen at- ence between the two electrically and electrolytically connected con- mosphere in a desiccator for electrochemical analyses. ductors. The rest potential (also open circuit potential) is the electrochemical potential of an electrode (relative to a reference elec- trode) which is time-dependently measured without the application of 2.3. Electrochemical analyses an external voltage and without a net current flowing (hence frequently All electrochemical measurements including potentiodynamic po- termed zero-current potential, too). The rest potential is strongly influ- enced by the electrolyte conditions and, therefore, is variable over time. larization, cyclic voltammetry as well as measurements of open circuit In the case of an electrode-electrolyte system coming close to a steady potential and galvanic currents were performed by the use of the state the measured potential signal becomes stationary. This special case potentiostat Interference 10oo (Gamry Instruments, USA). Electro- at which anodic and cathodic reaction rates are equal is called corrosion chemical analysis of unprocessed samples and leached residues were potential. In the context of galvanically assisted (bio)leaching this po- conducted using a three-electrode-system in a conventional electro- chemical cell within a faradaic cage. The cell was a 20 ml glass vial with tential is reported as rest potential, too. Rest potential measurement and the measurement of galvanic coupling currents were done by the use of a Teflon cap to fix the three electrodes. The counter electrode was a massive mineral electrodes (chalcopyrite from Bad Grund or from coiled platinum wire and the reference electrode was an Ag/AgCl elec- trode (filled with 3 M NaCl as inner electrolyte). Unless otherwise noted, Quebec, Pyrite from Navajun, Supplementary Material Fig. S4) in iron- free 1 M H2SO4 or in microbial growth medium (as electrolyte) with all electrochemical potentials are related to this reference electrode (+209 mV vs. SHE and - 35 mV vs. SCE). If not stated otherwise 15 ml of 25 mM ferric iron, respectively.
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Rest potential measurements were performed in the absence of microorganisms by the measurement of the the microbial growth medium were used as electrolyte during electro- open circuit potential until the steady state signal remained stable over chemical measurements which were performed under aerobic condi- hours. The galvanic corrosion current experiments were conducted in tions at 42 °C. the absence and in the presence of the microbial leaching consortium. A copper wire was incorporated within an epoxy resin rod (5 mm The electrochemical application for this measurement was performed by using the potentiostat in ZRA (zero resistance ammeter) mode (Sup- Table 2 plementary Material Fig. S5). This technique connects the examined Labels of used mineral sample mixtures for galvanic leaching experiments. materials as if they were directly connected with a wire. Simultaneously, Sample label Chalcopyrite [%] Pyrite [%] the current flow was measured. It is a typical test for contact corrosion to C4P0 100 0 measure the galvanic coupling current between two dissimilar C3P1 75 25 electrodes. C2P2 50 50 The mineral samples had a height of 5 mm and a diameter of 5 mm. COP4 100 。 With exception of the circular top and bottom, these cylindrical mineral pieces were coated with epoxy resin, too. The samples were loaded into Sample label Chalcopyrite [%] Quartz [%] the cavity of a base working electrode. A small piece of mineral-free C4Q0 100 0 carbon paste was put between the silver lacquer surface and the min- C3Q1 75 25 eral sample to optimize the electrical contact, to avoid capillary C2Q2 50 50 migration into the upper working electrode rod and to avoid the COQ4 0 100 migration of silver ions into the mineral sample. Only during galvanic current measurements, the electrolyte was stirred to obtain conditions Sample label Copper concentrate [%] Pyrite [%] close to the aerobic leaching process. For galvanic current measure- K4P0 100 0 ments in the presence of microorganisms 10 ml of pre-culture were K2P2 50 50 centrifuged and washed with microbial growth medium (electrolyte). C. Tanne and A. Schippers Hydrometallurgy 202 (2021) 105603 Centrifugation and washing were performed twice. Finally, the cells E vS. SHE [mV] were diluted in the measurement solution. 700r Pyrite Chalcopyrite 3. Results and discussion 600- Covellite 3.1. Rest potentials of metal sulfides Chalcocite 500l Pentlandite Rest potentials measured in this study as well as reported rest po- Galena tentials of various metal sulfides are summarized in Table 3. In addition, Fig. 2 shows the potential range and their overlap graphically. Table 3 400F Bornite clarifies that mineral sulfides can be classified roughly according to rest Pyrrhotite potential values. Nevertheless, there is a wide range of reported rest 300F Table 3 Sphalerite Rest potentials of different mineral sulfides at various electrolyte conditions as 200F measured in this study and as reported in different other studies. Mineral sulfide Electrolyte T Literature Rest 100F (massive [°C] potential vs. electrode) SHE [mV] Pyrite (FeS2) 0.9 K Jyothi et al., 691a 0F inoculated 1989 1 M H2SO4 20°℃ this study 660b (Navajun) 0.5 M H2SO4, -100F Chmielewski 643b oxygen free and Kaleta, 2011 1 M H2SO4 25 Mehta and Murr, 630 -200F 1983 1 M HCIO4 25 Mehta and Murr, 620 1983 0.9K Jyothi et al. 541a -300- uninoculated 1989 640b Fig. 2. Graphical representation of reported rest potential ranges of metal Chalcopyrite 1 M H2SO4 20 this study (Bad (CuFeS2) Grund) sulfides vs. SHE. 0.9 K Jyothi et al., 551a inoculated 1989 potential values of a single type of mineral sulfide. This is due to the lack 0.5 M H2SO4, Chmielewski 539b of defined standard conditions for the applied rest potential measure- oxygen free and Kaleta, 2011 ment. In detail, the reason can be found in the variation of the testing 1 M HCIO4 25 Mehta and Murr, 530 1983 procedure (like composition and properties of the used electrolyte) and 1 M H2SO4 20 520 in the differences of the mineral chemistry. The latter point includes the 1983 heterogeneity of the mineral sulfides themselves. This relates in partic- 9 K pH 2.5 Natarajan and 491a ular to their surface chemistry, which is largely determined by the Iwasaki, 1983 0.9 K Jyothi et al., 406a mineral composition, impurities, their electronic structure and probably uninoculated 1989 the type and spread of “"passivation" states (O'Connor and Eksteen, 1 M H2SO4 20 this study 285b 2020). In contrast, the conditions of the electrolyte can be easily (Quebec) controlled but are rarely uniform in the reports. Its properties, such as Covellite (CuS) 0.5 M H2SO4, Chmielewski 499b composition, concentration, pH value, temperature and the presence of oxygen free and Kaleta, 2011 1 M HCIO4 25 Mehta and Murr, 420 redox-active species or biocatalysts influence the redox properties of the 1983 electrolyte. These redox conditions must be strictly defined in the Chalcocite (Cu2S) 1 M H2SO4 20 Mehta and Murr, 440 electrochemical comparison of electrode materials. However, since no 1983 standards are defined for uniform conditions during the measurement of 0.5 M H2SO4, Chmielewski 360b and Kaleta, 2011 mineral sulfide rest potentials, a wide range of data is reported in oxygen free Bornite 0.5 M H2SO4, Chmielewski 404b various publications. (CusFeS4) oxygen free and Kaleta, 2011 The position of mineral sulfides in this series is regularly used in the Pentlandite (Fe, 9 K pH 2.6 Natarajan and 341-421a (bio)hydrometallurgical literature as a sufficient fact for the postulation Ni)gSs Iwasaki, 1983 Natarajan and 351-361a of galvanically enhanced dissolution. However, the heterogeneity of a Pyrrhotite (FeS to 9 K pH 2.7 Fe10S11) Iwasaki, 1983 mineral and the fact that the electrochemical behavior of the solid is Galena (PbS) 0.9 K Jyothi et al., 416a directly related to the properties of the electrolyte were frequently not inoculated 1989 1 M H2SO4 considered. 20 Mehta and Murr, 280 It has to be noted that mineral sulfides are determined as electrical 1983 0.9 K Jyothi et al., 266a semiconductors (Koch, 1975; Tributsch and Rojas-Chapana, 2000). uninoculated 1989 However, the influence of semiconducting materials with respect to Sphalerite (ZnS) 0.9 K Jyothi et al., 191a galvanic corrosion is poorly researched. In addition to the rest potential, inoculated 1989 the measurement of the galvanic current between two galvanically 0.9 K Jyothi et al., 11a interacting minerals is a more suitable option. uninoculated 1989 1 M HCIO4 20 Mehta and Murr, -240 1983 a recalculated from vs. SCE sat. KCl (-241 mV). b recalculated from vs. Ag/AgCl 3 M NaCl (-209 mV). C. Tanne and A. Schippers Hydrometallurgy 202 (2021) 105603 3.2. Monitoring of galvanic current densities between chalcopyrite and leaching consortium. This was probably due to microbial sulfur com- pyrite pound oxidation as layers of the non-metal sulfur (or probably also other sulfur compounds) act as electrical insulator and/or probably cause a The potential difference between chalcopyrite and pyrite caused a "passivation" being under debate (Ahmadi et al., 2012; Olvera et al., coupling current to flow since both were in electrical and electrolytic 2014; Wang et al., 2016; O'Connor and Eksteen, 2020; Zeng et al., 2020; contact. This was measured using a potentiostat in ZRA (zero resistance Wang et al., 2021). It has to be noted that chalcopyrite with a low rest ammeter) mode. Coupling currents were measured over several days in potential (chalcopyrite from Quebec) lead to much higher galvanic the absence (chemical) and in the presence (biological) of the microbial current densities in the absence as well as in the presence of microor- leaching consortium. The electrolyte (= microbial medium) contained ganisms. This clearly demonstrated the importance of a preferably high 25 mM ferric iron (Fe3+ ions) to increase the galvanic current flow via potential difference between rest potentials of an anodic and cathodic oxidative attack.
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The minerals chalcopyrite or pyrite were each con- mineral if galvanic assisted bioleaching is intentionally applied. A nected to an electrode made of the same or the other mineral. A selection higher potential difference leads to higher corrosion currents which of detected coupling currents is shown in Fig. 3 as a function of time. therefore results in enhanced dissolution of the anodic mineral. If chalcopyrite or pyrite were coupled to an electrode of the same Such galvanic currents between metal sulfides are often postulated in mineral, the currents remained very low and close to zero in the absence reports ("galvanic interaction occurred") or are given by time- of the leaching consortium. In contrast, the chalcopyrite-pyrite coupling independent current values. Measurements of the galvanic current initially showed clearly higher galvanic coupling currents in the abiotic over time are rather rare. Mostly, galvanic current measurements are experiment. This was observed for both chalcopyrite samples. The cur- short or are only examined in the context of chemical leaching (Yelloji rents decreased over time. This was probably due to an increasing Rao and Natarajan, 1989; Liu et al., 2018). Measurable galvanic "passivation" of the anodic electrode surface. Considering the pyrite- coupling currents are shown here. Therefore, this effect should affect pyrite coupling, the galvanic current remained very low in the pres- galvanically assisted leaching of chalcopyrite. ence of the microorganisms. Initially, this also applied to the chalcopyrite-chalcopyrite coupling for the Bad Grund mineral sample 3.3. Comparison of galvanically assisted leaching in the presence and in under the same conditions. However, this changed after three days, the absence of microorganisms since the current rose slightly and remained at the higher level. The galvanic behavior was considerably different for chalcopyrite-pyrite In this study, the galvanic interaction between chalcopyrite and coupling in the presence of the microorganisms. The galvanic coupling pyrite was demonstrated by long-term measurements. Many hydro- current started at a high level and remained high over the complete metallurgical reports assume such electrochemical interactions or measuring time. consider them as responsible for increased corrosion/dissolution effects. The results initially show that the pyrite electrodes were made of a One parameter which enhances galvanic corrosion is a large ratio of very homogeneous mineral sample. This explains the low currents for cathode area to anode area. The larger the cathode area, the more pyrite anode vs. pyrite cathode in the absence as well as in the presence extended should be the dissolution of the anodic mineral. of the microbial cells. However, the electrochemical behavior of chal- For this reason, different quantitative ratios of granulated chalco- copyrite was different. The used chalcopyrite from Bad Grund was pyrite BG and pyrite of the same size fraction (63 to 125 μm) repre- rather heterogeneous. This lead to a greater chemical imbalance in the senting different mineral surface areas were leached in this study. The chalcopyrite-chalcopyrite coupling as the electrode surfaces were not chalcopyrite content was 100, 75, 50 or 0%, the remaining content was chemically identical. Consequently, the chemical imbalance was elec- provided by pyrite. trically compensated in the form of an increased coupling current. Fig. 4 shows the development of the pH value, the ferric iron con- High coupling currents of the chalcopyrite-pyrite coupling were centration in solution and of the solution redox potential during observed during their galvanic interaction, both, in the absence and in galvanically assisted chemical leaching and bioleaching. During chem- the presence of microorganisms. Similar conclusions from abiotic ical leaching, the pH value increased if chalcopyrite was present. During leaching experiments of chalcopyrite with pyrite are reported in the bioleaching, the pH dropped due to the sulfur-oxidizing activity of the literature (Liu et al., 2018). However, in our experiments the current microbial leaching consortium. In the chemical assay, the solution redox exclusively remained continuously high in the presence of the microbial potential remained low and almost unchanged over the experimental time. The solution redox potential only increased in the presence of microbial cells due to iron-oxidizing activity. This increased the oxida- 150 tive character of the solution, which resulted in enhanced metal sulfide PyrvsPyr(abio.) dissolution. The Cu recovery results of chemical leaching and bio- 125 Pyr vs Pyr(bio.) leaching are summarized in Fig. 5. The extraction of Cu from chalco- 100 pyrite is shown for each leaching approach. Obviously, tests with 100% -Cpy BG vs Cpy BG (abio.) pyrite did not show Cu in solution. The increase in Cu recovery with the 75 pyrite content for bioleaching as well as for chemical leaching likely Cpy BG vs Cpy BG (bio.) triggered by galvanic corrosion. The recovery of Cu during bioleaching -Cpy BG vs Pyr (abio.) was usually higher compared to the chemical leaching results. 25 It has to be noted that also the pyrite dissolution increased the Cpy BG vs Pyr (bio.) concentration of iron in solution providing a higher ferric iron concen- tration as oxidant for both metals sulfides due to biological ferrous iron -25 Cpy Que vs Pyr (abio.) oxidation activity. This effect might superimpose the galvanic corrosion t[d] -50+ Cpy Que vs Pyr (bio.) of chalcopyrite. However, this effect should not be pronounced since the 0 1 2 3 ferric iron concentration was much lower in the biological assay with only pyrite (BL-COP4, Fig. 4b) than in the other three biological assays Fig. 3. Galvanic coupling current vs. time between massive mineral anode and with different mixtures of both metal sulfides (BL-C3P1, BL-C2P2) or cathode in the absence (abio) and in the presence (bio) of microbial leaching consortium (Cpy BG - chalcopyrite from Bad Grund, Cpy Que. - chalcopyrite chalcopyrite alone (BL-C4PO). For these three assays the ferric iron from Quebec, P - Pyrite). The legend shows anode vs. cathode coupling. The concentration was similar but the mixtures of pyrite with chalcopyrite electrolyte was stirred microbial growth medium with 25 mM ferric iron at showed higher Cu bioleaching than chalcopyrite alone (Fig. 5a) 42 °C and aerobic conditions. explainable by galvanic corrosion. 5 C. Tanne and A. Schippers Hydrometallurgy 202 (2021) 105603 C 3.0 20 450 18 2.8 16 425 BL-C4P0 14 —BL-C3P1 2.5 400 BL-C2P2 M12 三10 BL-COP4 2.3 -CL-C4P0 2.0 350 6 ·CL-C3P1 -CL-C2P2 1.8 325 ·CL-COP4 2 1.5 300 0 5 10 10 15 20 0 5 10 15 20 S [d] t[d] t[d] Fig. 4. Time-dependent development of pH (a), Fe3+ concentration (b) and solution redox potential (c) of bioleaching (solid lines) and chemical leaching (dotted lines) of chalcopyrite BG and pyrite. Error bars represent values from three independent leaching experiments each. 20 20 120 18 16 16 100 BL-C4P0 14 BL-C3P1 阿 80 12 12 BL-C2P2 10 ·C4Q0 BL-K4P0 10 60 -BL-COP4 -·C3Q1 +BL-K2P2 D -CL-C4P0 ·C2Q2 40 -CL-K4P0 6 -CL-C3P1 -·C0Q4 -CL-K2P2 -CL-C2P2 20 -CL-C0P4 10 15 20 0 5 10 15 20 5 10 t[d] t[d] t[d] Fig. 5. a) Cu recovery from chalcopyrite BG of bioleaching and chemical leaching in the presence of different proportions of pyrite. b) Cu recovery from chalcopyrite BG in chemical control leaching with different amounts of quartz instead of pyrite. c) Cu recovery from copper concentrate in the absence and the presence of pyrite. Error bars represent values from three independent leaching experiments each. In an additional experiment, pyrite was completely replaced by 3.4. Comparison of corrosion potential and corrosion currents of leaching quartz. The Cu recovery increased with a higher quartz content (Fig. 5b). residues Quartz is an electrical insulator in contrast to the semiconductor pyrite but slightly harder than pyrite.
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Thus, abrasivenes due to shear forces A typical electrochemical corrosion test is the determination of the may favor the corrosion of chalcopyrite in case of quartz addition, or corrosion potential and the corrosion current using potentiodynamic silica may have a catalytic effect on abiotic chalcopyrite dissolution. The polarization and the fitting of Tafel plots. This was done for unprocessed Cu recovery increase with quartz is similar to that with pyrite addition metal sulfides (Fig. 6) and their mixtures as well as for the residues from for the lower amounts of mineral addition to chalcopyrite. However, for chemical leaching and bioleaching. The samples were examined in an the highest amount of added quartz the Cu recovery was lower iron-free medium, thus these corrosion parameters refer to oxidation compared to that with pyrite. with dissolved oxygen and not ferric iron. The galvanic effect in the coupling between chalcopyrite and pyrite The results are summarized in Fig. 7. The corrosion potential (Fig. 7a is relatively small. Chalcopyrite seemed to be rather recalcitrant to be and c) increased with increasing pyrite content. However, in comparison dissolved. Electrochemically, this can be explained by the small rest potential differences between the two minerals. The galvanic driving force for dissolution is therefore rather low. For this reason, a more pyrite -copperconcentrate active substrate, namely a copper concentrate, was used and galvani- chalcopyriteBG 500 cally leached with pyrite. Fig. 5c shows the results. The copper [Aw] 450 concentrate was chemically leached to a large extend (40%) in a few days. No galvanic effect could be observed in the presence of pyrite in 400 the abiotic experiment, however the concentrate itself already contains 350 pyrite which may explain that the additional pyrite did not show an 300 effect in this case. The bioleaching results confirm that the concentrate 250 was leached much faster and to a larger extend when galvanically 200 assisted bioleaching was applied. 0.000 0.010 1.000 100.000 1[μA] Fig. 6. Examples of typical potendynamic scans of unleached pyrite (solid line), copper concentrate (dashed line) and chalcopyrite BG (dotted line). C. Tanne and A. Schippers Hydrometallurgy 202(2021) 105603 500 500 10.0 450 450 400 400 8.0 350 300 6.0 300 250 250 200 4.0 200 150 100 2.0 50 50 0 0.0 0 b.b.b.b, err P 2 4 d 50 45 40 # 10 Fig. 7. Corrosion potential of Bad Grund chalcopyrite (a) and copper concentrate (c) and corrosion current densities of Bad Grund chalcopyrite (b) and copper concentrate (d) of carbon paste electrodes containing unprocessed or leached mineral samples (unpro - unprocessed; bio - bioleached; chem - chemically leached). Error bars for potential and current were calculated from three independently prepared and measured electrodes. the corrosion potential of residues from chemical leaching was lower for interaction with other (anodic) metal sulfides in bioleaching studies, chalcopyrite. For copper concentrate this potential was increased too. On the other hand, pyrite is known as a wellsuited substrate for compared to unprocessed samples. The corrosion current (Fig. 7b and d) acidophilic bioleaching microorganisms. However, the type of pyrite was highest for unprocessed mineral samples. It has to be noted that all may have to be taken into account. Single-crystalline pyrite cubes were copper concentrate samples (especially the unprocessed ones) showed used in this study. These may be (electro)chemically more inert and, higher current density values compared to the chalcopyrite from Bad thus, are probably more difficult to leach than other pyrite types like, for Grund. Exclusively, samples of 100% pyrite showed very low corrosion example, framboidal pyrite. currents in all cases. Corrosion currents from the leached residues were significantly smaller. Samples with 100% chalcopyrite and 100% copper 3.5. Comparison of electrode surface redox activity of leaching residues concentrate showed the highest currents. The increase in corrosion potential with increasing pyrite content Another option to obtain information about the leachability of metal can be explained by the mixed potential theory. Hence, all components sulfides is the cyclic voltammetric analysis of the electrode surface redox of the electrode surface contribute to the measured electrode potential. activity (Cordoba et al., 2008; Wang et al., 2016; Tanne and Schippers, Since pyrite is nobler than chalcopyrite and the minerals in the copper 2019b; Zeng et al., 2020). Overall the cyclic voltammetric data should concentrate, the corrosion potential increased with the pyrite content. be carefully interpreted since they were recorded for a wide potential The lower corrosion potential of chalcopyrite residues from chemical range in these studies as well as in this current study while mineral leaching compared to that of bioleached residues is consistent with the leaching takes place in a much narrower potential range. In order to observations from a previous study (Tanne and Schippers, 2019b). observe the redox activity of the surface, samples were examined in iron- Lowered corrosion currents of leached samples are probably due to free solution in this study. The results are shown in Fig. 8 which clearly "“passivation" effects. Chalcopyrite is less noble than pyrite and, there- shows that unprocessed samples of chalcopyrite in the range above 300 fore, is considered to be a “more active” corrosion material. This may mV vs. Ag/AgCl were easily oxidized (increased oxidation currents). explain that samples with 100% chalcopyrite showed the highest This did not apply to 100% pyrite. For the same potential range, it could corrosion currents. However, the electrochemical “activity” of the cop- be seen that the oxidation peak currents of bioleached residues (Fig. 8b) per concentrate by far exceeded the “activity” of chalcopyrite. This fact as well as of chemically leached residues (Fig. 8c) were significantly indicates the increased susceptibility of the copper concentrate to decreased. Interestingly, the oxidation currents of electrodes with bio- corrosion/dissolution by galvanic assisted bioleaching. leached residues of chalcopyrite showed higher oxidation currents Interestingly, the smallest corrosion current was measured with compared to chemically leached residues at the highest potentials 100% pyrite. From an electrochemical point of view, this can be examined. In comparison, the anodic cyclic voltammetric signal of un- explained by the high corrosion potential and the nobler character of processed copper concentrate resulted in significant higher currents pyrite. This property of pyrite is frequently used to explain the galvanic (Fig. 8d). Thus, the concentrate was much easier to dissolve compared to 7 C.Tanne and A. Schippers Hydrometallurgy 202 (2021) 105603 C4PO_abic C3P1_abio C2P2_abio COP4_abio 4PO_bio 4P0_abio K2P2_bio 2P2_abic 1500 1500 2000 2500- E vs. Ag/AgCI [mV] E vs. Ag/AgCI [mV] E vs. Ag/AgCI [mV] Fig. 8. Cyclic voltammograms of unprocessed (a), bioleached (b) and chemically leached (c) Bad Grund chalcopyrite and of unprocessed (d), bioleached (e) and chemically leached copper concentrate (f). For each cyclic voltammogram, three independently prepared electrodes were combined to an average signal and to calculate error bars. This standard deviation of each current data point is displayed in the respective transparent color. the used chalcopyrite due to a more anodic behavior. However, studies are needed in (bio)hydrometallurgy. For example, the here increased corrosion/dissolution could result in an increased precipita- observed very low corrosion susceptibility to pyrite was striking. This tion of sulfur compounds on the mineral surface which may cause a so- study suggests that this is due to the high crystallinity of pyrite (single called “"passivation" (C6rdoba et al., 2008; Tanne and Schippers, 2019b; crystals were used), and therefore studies to investigate different pyrites O'Connor and Eksteen, 2020; Zeng et al., 2020; Wang et al., 2021).
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This and their properties related to electrochemistry are on demand. The may explain why for bioleaching residues (Fig. 8e) a very low oxidation option of running electro-bioreactors and galvanic support in combi- current was measured. In contrast, chemically leached copper concen- nation should also be examined to a larger extend. Further, it should be trate (Fig. 8f) showed that its oxidation behavior was similar to that of investigated to what extent different types of conductive minerals could the unprocessed chalcopyrite. The anodic current density near 400 mV act as electron mediators (e.g. activated carbon, Oyama et al., 2020), so was even slightly higher. Thus, the chemically leached concentrate still that galvanic interaction over several potentials may occur more effec- showed a high electrochemical "activity."" tively step by step. It turned out that the redox activity of the electrode surfaces could be made clearly visible by cyclic voltammetry. However, the redox currents decreased with a higher pyrite content. With 100% pyrite, only charging Declaration of Competing Interest currents occurred (charging and discharging of the electrochemical The authors declare that they have no known competing financial double layer at the electrode-electrolyte interface). This is similar to a interests or personal relationships that could have appeared to influence noble metal electrode. the work reported in this paper. Residues from chemical leaching with a higher amount of chalco- pyrite showed slightly higher oxidation currents than bioleaching resi- Appendix A. Supplementary data dues near 300 mV. This argues for an advanced mineral dissolution during bioleaching. This effect occurred to a larger extend for the electrochemically more “active” copper concentrate. Supplementary data to this article can be found online at https://doi. org/10.1016/j.hydromet.2021.105603. 4. Conclusion and outlook References This study illustrates the effect of the galvanic interaction between Ahmadi, A., Ranjbar, M., Schaffie, M., 2012. Catalytic effect of pyrite on the leaching of anodic chalcopyrite and cathodic pyrite. This was investigated twice, by chalcopyrite concentrates in chemical, biological and electrobiochemical systems. long-term electrochemical measurements of the galvanic coupling cur- Miner. Eng. 34, 11-18. https://doi.org/10.1016/j.mineng.2012.03.022. rent, and by chemical leaching and bioleaching. Thus, this study shows Arduini, F., Cinti, S., Scognamiglio, V., Moscone, D., Palleschi, G., 2017. How cutting- edge technologies impact the design of electrochemical (bio)sensors for through measurable electrochemical data and leaching data that both, environmental analysis. A review. Anal. Chim. Acta 959, 15-42. https://doi.org/ biology and galvanic effects, can support chalcopyrite leaching. This is 10.1016/j.aca.2016.12.035. especially true for galvanic coupling of minerals with a high rest po- Berry, V.K., Murr, L.E., Hiskey, J.B., 1978. Galvanic interaction between chalcopyrite and pyrite during bacterial leaching of low-grade waste. Hydrometallurgy 3, tential difference. In this context, acidophilic microorganisms played a 309-326. https://doi.org/10.1016/0304-386X(78)90036-1. key role. They kept the solution redox potential high and likely Chmielewski, T., Kaleta, R., 2011. Galvanic interactions of sulfide minerals in leaching of decomposed electrically insulating sulfur layers. Increased levels of flotation concentrate from Lubin concentrator. Physicochem. Prob. Mineral Process. 46, 21-34. pyrite in the mixed mineral system resulted in increased Cu recovery. Cordoba, E.M., Munoz, J.A., Blazquez, M.L., Gonzalez, F., Ballester, A., 2008. Leaching of As requested in other reports, more fundamental electrochemical chalcopyrite with ferric ion. Part I1. General aspects. Hydrometallurgy 93, 81-87. C. Tanne and A. Schippers Hydrometallurgy 202 (2021) 105603 Donati, E.R., Sand, W., 2007. Microbial Processing of Metal Sulfides. Springer, Olvera, O.G., Quiroz, L., Dixon, D.G., Asselin, E., 2014. Electrochemical dissolution of Dordrecht. fresh and passivated chalcopyrite lectrodes.Effectof pyrite onthereductionof F Figueira, R., 2017. Electrochemical sensors for monitoring the corrosion conditions of ions and transport processes within the passive film. Electrochim. Acta 127, 7-19. reinforced concrete structures: a review. Appl. Sci. 7, 1157. https://doi.org/ https:/doi.org/10.1016/j.electacta.2014.01.165. 10.3390/app7111157. Oyama, K, Shimada, K., Ishibashi, J., Sasaki, K., Miki, H., Okibe, N., 2020. Catalytic Harnisch, F., Holtmann, D. (Eds.), 2019. Bioelectrosynthesis. Advances in Biochemical mechanism of activated carbon-assisted bioleaching of enargite concentrate. Engineering/Biotechnology 167. Springer International Publishing, Cham. Hydrometallurgy 196, 105417. https://doi.org/10.1016/j.hydromet.2020.105417. Hedrich, S., Guezennec, A.-G., Charron, M., Schippers, A., Joulian, C., 2016. Quantitative Payne, N.A., Stephens, L.1., Mauzeroll, J., 2017. The application of scanning monitoring of microbial species during bioleaching of a copper concentrate. Front. electrochemical microscopy to corrosion research. Corrosion 73, 759-780. https:/ Microbiol. 7, 2044. https://doi.org/10.3389/fmicb.2016.02044. doi.org/10.5006/2354. Hedrich, S., Joulian, C., Graupner, T., Schippers, A., Guezennec, A.-G., 2018. Enhanced Popov, K.I, Djokic, S.S., Grgur, B.N., 2002. Fundamental Aspects of Electrometallurgy. chalcopyrite dissolution in stirred tankreactorsby temperature increase during Kluwer Academic Publishers, Boston, MA. https:/doi.org/10.1007/b118178. bioleaching. Hydrometallurgy 179, 125-131. https:/doi.org/10.1016/j. Saavedra, A., Garcia-Meza, J.V., Corton, E., Gonzalez, I., 2018. 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Electrochemical Tanne, C.K., Schippers, A., 2019b. Electrochemical investigation of chalcopyrite (bio) simulation of redox potential development inbioleaching of a pyritic chalcopyrite leaching residues. Hydrometallurgy 187, 8-17. https://doi.org/10.1016/j. concentrate. Hydrometallurgy 144-145, 7-14. https://doi.org/10.1016/j. hydromet.2019.04.022. hydromet.2013.12.003. Tributsch, H., Rojas-Chapana, J.A., 2000. Metal sulfide semiconductor electrochemical Koch, D.F.A., 1975. Electrochemistry of sulfide minerals. In: Bockris, J.O.M., Conway, B. mechanisms induced by bacterial activity. Electrochim. Acta 45, 4705-4716. E. (Eds.), Modern Aspects of Electrochemistry, 10. Springer US, Boston, MA, https://doi.0rg/10.1016/S0013-4686(00)00623-X. Pp. 211-237. Wang, J., Gan, X., Zhao, H., Hu, M., Li, K., Qin, W., Qiu, G., 2016. Dissolution and Liu, Q., Chen, M., Zheng, K., Yang, Y., Feng, X., Li, H., 2018. 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Science of the Total Environment 908 (2024) 168210 Contents lists available at ScienceDirect Science Science of the Total Environment ELSEVIER Review Biomining for sustainable recovery of rare earth elements from mining waste: A comprehensive review Phong H.N. Vo a*, Soroosh Danaee b, Ho Truong Nam Hai , Lai Nguyen Huy d, Tuan A.H. Nguyen , Hong T.M. Nguyen f, Unnikrishnan Kuzhiumparambil a, Mikael Kim a, Long D. Nghiem &, Peter J. Ralph a Climate Change Cluster,Faculty of Science,University of Technolog Sydney,15Broadway,Ultimo,NW2007,Australi BiotechnologyDepartment,IranianResearchOrganizationforScience andTechnology,Tehran3353-5111,Iran FacultyfErersty fci2yuistrhiini dEnvironmentalEngineeringandManagement,AsianInstiuteofTechlogy,KlongluangathmthaniThaild SustainableMineralsnstitutThUiversitofQuensandrisbaneQuensland7,Austal QueenslandAllnceforEnvronmentalHealthciencesQAEH),hUniverstyfQueenslandQuesland2,Austal 8Centre for Technology in Water and Wastewater, University of Technology Sydney, Ultimo, NSW 2007, Australia HIGHLIGHTS GRＡPHICＡＬABSＴRＡCT ·Bioleaching has high extraction effi- ciency (>80 %) and high selectivity for REEs. Mining waste Stage 1: Stage 2: Recover soluble REES ·Bioleaching has low environmental impact but is time-consuming, from months to years. · Yttrium, cerium, and neodymium are the most common REEs found in mining waste streams (50-300 μg/L). Bioaccumulation · Heavy and light REEs are more effec- tively recovered at low and neutral pH Bioflotation respectively. · Coal ash is the most profitable mining waste stream. SolubleREEs ARTICLEINＦＯ ABSTRACT Editor: Jay Gan Rare earth elements (REEs) are essential for advanced manufacturing (e.g., renewable energy, military equip- ment, electric vehicles); hence, the recovery of REEs from low-grade resources has become increasingly Keywords: important to address their growing demand. Depending on specific mining sites, its geological conditions, and Biomining sociodemographic backgrounds, mining waste has been identified as a source of REEs in various concentrations Rare earth elements and abundance. Ytrium, cerium, and neodymium are the most common REEs in mining waste streams (50 to Bioleaching 300 μg/L). Biomining has emerged as a viable option for REEs recovery due to its reduced environmental impact, Biosorption along with reduced capital investment compared to traditional recovery methods. This paper aims to review (i) Bioaccumulation the characteristics of mining waste as a low-grade REEs resource, (i) the key operating principles of biomining technologies for REEs recovery, (i) the effects of operating conditions and matrix on REEs recovery, and (iv) the sustainability of REEs recovery through biomining technologies. Six types of biomining wil be examined in this * Corresponding author. E-mail address: phong.vo@uts.edu.au (P.H.N. Vo). https://doi.org/10.1016/j.scitotenv.2023.168210 Received 28 August 2023; Received in revised form 23 October 2023; Accepted 27 October 2023 Available online 2 November 2023 0048-9697/? 2023 Elsevier B.V.All rights reserved. P.H.N. Vo et al. Science of theTotalEnvironment908(2024)168210 review: bioleaching, bioweathering, biosorption, bioacumulation, bioprecipitation and bioflotation. Based on a SWOT analyses and techno-economic assessments (TEA), biomining technologies have been found to be effective and efficient in recovering REEs from low-grade sources. Through TEA, coal ash has been shown to return the highest profit amongst mining waste streams. 1. Introduction 2. Low-grade REEs resources from mining wastes Rare earth elements (REEs) are a group of 17 metallic elements, Mining waste is a matrix of solids, minerals and REEs, and can be including scandium (Sc) and yttrium (Y), in addition to 15 lanthanides. classified into two categories: (i) the processing side streams, such as red REEs have unique chemical and physical properties useful for electrical, mud slurry; and (i) the extraction side streams, such as acid mine optical, and magnetic applications. Hence, REEs are essential for drainage (AMD). Due to the presence of REEs, mining waste has been advanced manufacturing (e.g., renewable energy industries and elec- attracting attention in recent years for its potential as a source of low- tronic equipment manufacture) in forming products with unique prop- grade REEs (Table 1). Importantly, the abundance and concentration erties (e.g., catalytic, metallurgical, electrical, magnetic, ，and of REEs is dependent on the characteristics of the mining waste, such as; luminescence). Given their essential role in modern industry, REEs have the specific mining site where the mining waste was sourced, geological exceptionally high commercial value, with recent valuation estimates of conditions of the site, and sampling locations (such as internal mine $2 billion USD in 2020 (Department of Industry, 2021). In 2017, the drains, site-level wastewater, open pits, and drainage of waste rock tails global production of REEs was 130,000 tons, of which China accounted or piles). for 80 %, with an expected increase in worldwide demand for REEs of up In addition, the composition and abundance of the ore deposit and to 210,000 tons by 2025 (Mwewa et al., 2022). Most REEs are dispersed the relevant processing technologies play a critical role in forming the in the Earth's crust at low concentrations, so they are unsuitable for characteristics of mining waste. For example, the concentration of total extraction using conventional mineral processing techniques (Storm- REEs (>REE) in AMD of closed uranium mines, was significantly higher croW., 2020). Further, the security of REE supply chains is under sig- than other mining wastewater. This high REEs concentration stems from nificant threat due to uneven geographical distribution, uncertainty in accumulation over long time spans (Felipe et al., 2021). The variation of global geopolitics, challenges in the purification of REEs at industrial REEs in mining waste is also subject to geochemical and sociodemo- scale (Mwewa et al., 2022; Xie et al., 2014). graphic conditions. The highest concentration of REEs in coal mine Given the uncertainty of future availability of REEs, there is waste streams was mostly Y; while Ce was the most dominant in mineral increasing interest in REEs extraction from low-grade resources to meet ores (e.g., Au, Zn, Pb) (Table 1). A comprehensive assessment of the the projected demand. Due to economic and technical constraints, this literature indicates that light and medium weight REEs are predomi- strategy is preferable to finding a replacement element for REEs or new nantly present in mining waste (Myagkaya et al., 2016; Prudencio et al., REE deposits. Mining wastes such as gypsum, red mud, and acid mine 2015; Shahhosseini et al., 2017; Vass et al., 2019). drainage are typically low-grade resources for REEs; fortunately, the Other chemistry factors in mining waste such as pH and ligands, also concentrations of REEs in mining wastewater are approximately 10,000 impact the presence of REEs (Gammons et al., 2003; Olias et al., 2018). times higher than in natural waters such as lakes and rivers (Cao et al., Ligand complexes in mining waste can be classified into four predomi- 2021). In Australia, there are over 52,000 abandoned mines (Unger nant classes: REEs-sulfate complexes, free metal species, REEs-car- et al., 2012), providing a scalable opportunity for commercial produc- bonate complexes, and inorganic complexes. Studies have reported that tion of REEs, while simultaneously allowing for environmental reme- stable REE-SO4 and REE-SOz2 complexes are the dominant species in diation. Similarly, red mud, a by-product of the aluminum extraction acidic conditions with pH < 5 (Migaszewski et al., 2019; Xia et al., 2023), followed by REEs complexes with free metal species (Royer- process, contains up to 500 mg/kg of cerium (Ce). However, only 2 % of the 150 million tons of red mud produced per year is reused (Cizkova Lavallée et al., 2020). The reason for the substantial presence of these et al., 2019).
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Therefore, the current mining residue/waste recycling rate ligand complexes in mining waste is low pH (<3), along with the atomic is still very modest compared to its vast potential. number of associated REEs, as REEs presence decreases with increasing Existing methods for REEs recovery such as hydro-, thermal- and atomic number (Zhao et al., 2007). electro-metallurgical technologies, are associated with substantial sec- In addition, the sulfate and acid levels in mining waste affects REEs ondary pollutants (e.g., thorium (Th), uranium (U)), as well as being concentration (Mwewa et al., 2022). A good example is the difference in chemically and energy-intensive (Cizkova et al., 2019). Biomining pro- the distribution of REEs in the above and below ground drainage of vides a potential solution that mitigates these issues as biomining ex- mining waste streams (Vass et al., 2019). Lower pH can be observed in ploits a microorganisms' biogeochemical processes to recover REEs. the above-ground drainage of mining waste streams, resulting in higher Significant progress in biomining of heavy metals has been reported REEs concentrations (Agboola et al., 2020). This is caused by higher with relevance to a wide range of microorganisms such as: bacteria, concentrations of sulfate, whereby formation of their stable complexes microalgae, macroalgae, fungi and higher plants. However, there is still inhibit the precipitation of REEs (Royer-Lavallée et al., 2020). In no systematic review regarding the progress in biomining research, and contrast, the below ground drainage of mining waste streams is alkaline understanding of biomining technologies for REEs recovery (Abashina due to limited pyrite oxidation in aqueous conditions and the accumu- and Vainshtein, 2023; Liapun and Motola, 2023). Apart from systematic lation of bicarbonate buffer. When pH increases (pH > 5), carbonate improvements in biomining technologies, the influence of operating complexes are formed which leads to a depletion of REEs, especially conditions on REEs recovery efficiency is also needed. In addition, it is light REEs, due to their re-adsorption into metal oxides and hydroxide essential to perform an in-detail analysis of treatment technologies for colloids, and subsequent precipitation (Mwewa et al., 2022). their strength, weakness, opportunity, and threat (SWOT); and a techno- economic analysis to establish a baseline for universal usage. 3. Key principles of biomining technologies for REEs recovery This paper aims to review (i) the characteristics of mining waste as a low-grade REEs resources, (i) the fundamental working principle of Biomining technologies for REEs recovery include; bioleaching, biomining technologies for REEs recovery, (i) the effects of operating bioweathering, biosorption, bioaccumulation, bioprecipitation, and conditions and matrix on REEs recovery, and (iv) sustainable ap- bioflotation. Each of these technologies are applicable for specific proaches for REEs recovery from low-grade resources. mining waste, and at specific stages of the recovery processes (Fig. 1). P.H.N. Vo et al. Science of the Total Environment 908(2024)168210 Bioleaching and bioweathering are the first stages in which REEs in [t solids (e.g., red mud) are solubilized by the lixivia - acidic excretion - of 3刀 3 2 microbes. The soluble REEs in lixivia can be recovered in subsequent 48 stages via biosorption, bioaccumulation, bioprecipitation, and bio- flotation, with additional help from a range of organisms (e.g., bacteria, 9 9t9 2.9 microalgae, macroalgae and plants). Regarding REEs present in soluble form in mining wastewater, biosorption, bioaccumulation, bio- precipitation, and bioflotation technologies can be used to recover REEs without an initial extraction stage. 740 3.1.Bioleaching Bioleaching is characterized by the mobilization of REEs from the 20 89 solid to liquid phase. A solid matrix (such as ore deposits) containing REEs is solubilized by microbial activity, which releases REEs. (Fig. 2), (6007) followed by mobilization of REEs via three biochemical processes: redoxolysis, acidolysis, and complexolysis. Redoxolysis is a two-step 6 9 2 reaction consisting of either contact or non-contact mechanisms. Con- 07 t tact redoxolysis involves an oxidative reaction of Fe2+ to Fe3+ under nm aerobic conditions, which stems from the transfer of electrons from minerals to microorganisms. Non-contact redoxolysis involves an 17158 3 oxidative dissolution of REEs, resulting in REEaq). Acidolysis involves .2 acid dissolution of REEs from minerals by sulfur-oxidizing or phosphate- oxidizing bacteria. Where sulfur-oxidizing bacteria oxidize sulfide to 66 -08 [[] produce sulfuric acid, phosphate-oxidizing bacteria release phosphate. Complexolysis involves the solubilization of REEs via microbial organic acids and siderophores. Microbial organic acids are released to dissolve -LD the REEs from solid minerals, while extracellular siderophores function 11S3 as iron-carriers to transport iron back into the cell from the environ- ment, thereby forming stable complexes with REEs, which allows for further release of REEs. 003 5 From an industrial viewpoint, bioleaching of REEs from ore deposits (1 and e-waste needs to be validated under pilot-plant conditions (Barnett et al., 2020; Brown et al., 2023). Bioleaching is an effective industrial technique for extracting copper and gold ores, but it has not been widely developed for REEs extraction. Different bioreactors, such as rotating drums, stirred tanks and fluidized bed reactors have been applied in 0099 81 t bioleaching of metals (Adetunji et al., 2023; Roberto and Schippers, 7'0 07 TZ7 2022). In contrast, bioleaching of REEs is limited to laboratory-scale [] applications, highlighting the need for further development work such 888 2 as environmental impact assessments, before the technology can be 0 applied to an industrial scale (Tezyapar Kara et al., 2023). As the process upscaling of bioleaching would be based on the identification of effec- 77-t1 t tive microorganisms as well as optimum conditions of operation, an 9. 4 overview of microorganisms applied for bioleaching is presented next. Hd 13 t There is a wide range of microorganisms that are suitable for bio- leaching applications, including (i) Fe—S oxidizers, (i) heterotrophic pnu bacteria, and (i) cyanogenic bacteria (Brown et al., 2023) (Table 2). 8 Each microorganism group mentioned, has a unique biochemical func- 13 tion to solubilize metallic substances, including iron/sulfur oxidation, organic acid extrusion, and cyanide based lixiviant production. The ipo literature shows that heterotrophic cultures are preferred for producing acid for REEs solubilization, likely as they are more resilient to mining waste (Tayar et al., 2022). This is demonstrated by reduced leaching 1 efficacy of Fe—S oxidizing bacteria due to interference from components 2 in ore deposits compared to the leaching efficacy of heterotrophic bac- 1 teria. Acidithiobacillus ferrooxidans, a typical Fe—S oxidizer, is only W .n effective in clay-rich bauxite sources (Barnett et al., 2020), whereas a 1111 6 eqn pue culture of heterotrophs produces a range of metabolites that can be more 8 effective for REEs leaching than a sole organic acid (Antonick et al., .n 2019). For example, Aspergillus niger and Yarrowia lipolytica produce sods citric acid, which leaches 90 % of REEs. Oxalic acid produced by A. niger is also beneficial for REEs recovery by forming soluble Ce in concen- trations >1.37 mg/L (Bahaloo-Horeh and Mousavi, 2022). Several carbon sources have been used as a nutrient source for het- erotrophic microbes to enhance the production of organic acid. With P.H.N. Vo et al. Science of the Total Environment 908(2024) 168210 glucose as a carbon source, A. niger was found to reach its highest and respiration controlled the rate of acidification.
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It was reported that leaching efficiency of 91 %, whereas when sucrose was used, A. niger and disrupting a single gene within the phosphate signalling control of Y lipolytica reached a leaching efficiency of 66 %, and 34 % respectively biolixiviant production, increased bioleaching by 18 %; however, dis- (Shen et al., 2023). The organic acids excreted by A. niger is comprised of rupting the supply of the pyrroloquinoline quinone (PQQ) cofactor to oxalic, citric, and succinic acid and a trace amount of malic acid. the membrane-bound glucose dehydrogenase, significantly impaired Y. lipolytica excretes a lixiviant with a more straightforward matrix, bioleaching by up to 94 %. This investigation offers great insight into comprising of citric, malic, and succinic acid. Therefore, the composi- improving the performance of bacteria for bioleaching purposes, as the tion of other lixiviants needs to be further investigated, given the bio- production rate of lixiviant must be increased to overcome a critical leaching efficiency of heterotrophic microbe derived lixiviants are very limitation of bioleaching technology: the long production time promising (Park and Liang, 2019). (Petersen, 2016). Subsequently, more genetic engineering interventions The operation of bioleaching is executed in two ways: (i) contact/ are still required to develop a new mutant that can simultaneously direct reaction in which microbes and ore deposits directly interact, and produce a more acidic biolixiviant at a faster rate than the wild-type. (i) noncontact/indirect reaction in which the lixiviant of microbes is Another strategy to improve the recovery of REEs is co-culturing extracted and applied for bioleaching. Application of in-situ direct with autotrophic bacteria such as A. ferrooxidans, or the fungi Penicil- contact bioleaching is limited due to difficulty in site access, compro- lium sp. CF1 (Corbett et al., 2018). The consortium of heterotrophic mising system setups, and proper operation and maintenance re- Enterobacteraerogenes and autotrophic A.ferrooxidans can improve REES quirements. Alternatively, indirect bioleaching can be applied offsite leaching to a final concentration of up to 40 mg/L (Fathollahzadeh et al. and under more controlled environments. Interestingly, indirect bio- 2018b). The underlying mechanism is the synergistic effect of mixing leaching of REEs showed a higher REE leaching efficiency (98 % Nd, 60 organic acid and sulfuric acid produced by the heterotrophic and % Ce, and 58 % La) compared to direct bioleaching (28 % Nd, 17 % Ce, autotrophic bacteria. Through imaging techniques such as electrostatic and 18 % La) (Tayar et al., 2022). force microscopy (EFM) and atomic force microscopy (AFM), the mixed Compared to traditional extraction and purification methods, bio- cultures were shown to have produced more extracellular polymeric leaching's performance still lags behind thermochemical processes. substances than the monocultures (Florian et al., 2010). Recent efforts to improve the extraction efficiency of bioleaching have There are several known acid-tolerant microalgae (e.g, Stichococcus included genetic engineering of acid-producing microbes such as Glu- bacillaris, Chlamydomonas acidophila, Chlamydomonas pitschmannii,Vir- conobacter oxydans (Schmitz et al., 2021). Genome knockout experi- idiella fridericiana) that can survive at a pH below 3, and can also be co- ments were conducted on wild-type G. oxydans to identify genes cultured with heterotrophic bacteria to improve the REEs leaching yield responsible for its acidification capability. Researchers found that 304 (Abiusi et al., 2022). It should be noted that microalgae cannot produce genes were involved in the biosynthesis of acidic bio-lixiviant (Schmitz acidic lixiviant, however they can support the growth of heterotrophic et al., 2021). Mutant strains were identified that produced either more bacteria via the production of extracellular polymeric substances (EPS) acidic biolixiviant or a faster rate of acidification than the wild-type. and oxygen, which act as a nutrient source for the heterotrophic bacteria Disruption of genes involved in the phosphate-specific transport sys- (Aditya et al., 2022). This synergistic relationship between microalgae tem led to the development of mutant strains that produced a more and heterotrophic bacteria is an emerging research field in biomining acidic biolixiviant, whereas genes related to carbohydrate metabolism and is therefore worth further investigation. Mining waste Stage 1: Stage 2: Recover soluble REEs SolubilizeREEs Biosorption Bioleaching Red mud Bioaccumulation Bioflotation Acid mine drainage Bioweathering Bioprecipitation Soluble REEs Fig. 1. Process diagram of REEs recovery using various biomining technologies. P.H.N. Vo et al. Science of theTotal Environment 908(2024)168210 Intracellular Extracellular precipitation precipitation Insoluble Soluble Complexation REES REES with EPS on cell surface HCO3 OH- HS 無海 Leaching in reactor Bioleaching Biosorption Bioprecipitation REEs attachto bubble Insoluble Soluble REES REES Leaching on ore surface Bioweathering Bioaccumulation Bioflotation Extracellularpolymeric Acidexcr Bacteria substances(EPS) Fig. 2. Mechanisms of REEs recovery by biomining processes from leachate. 3.2. Bioweathering 2021). In addition, the level of bioweathering occurring in minerals depends on the type of mineral. For example, goethite crust with quartz Bioweathering is the erosion, decay, and decomposition of minerals was more prone to bioweathering than the calamine-type rock, with the mediated by living microbes, through biomechanical and/or biochem- underlying reason being the presence of goethite and smithsonite in the ical invasion of the minerals. The mechanism of bioweathering is similar minerals which can be dissolved to a greater extent than the other ele- to bioleaching in which microbes excrete lixiviant such as organic acid ments. A. thiooxidans and A. ferrooxidans can also be bioaugmented to to accelerate the solubilization of the elements in the ores/rocks (Fig. 2). accelerate bioweathering of pyrite and biotite-like minerals, with the Bioweathering occurs under natural conditions, whereby microbes and result of bioaugmentation being a 30 % mobilization of metals (Liu minerals come into direct contact without artificial intervention, while et al., 2021). As the bioweathering process is not conducted in an arti- bioleaching requires the mineral to be ground and actively cultured in a ficial bioreactor, bacteria are the most viable organism for this tech- bioreactor. There are some reports of microbial weathering at the lab- nology, potentially in conjunction with plants, while microalgae are oratory scale to find the effects of different parameters (He et al., 2023; unlikely to be feasible in this context due to contamination concerns. Kang et al., 2021; Sachan, 2019); however, bioweathering in a labora- tory setting is meaningless because, as mentioned, it occurs in natural environments. Interestingly, the implementation of bioweathering in a 3.3.Biosorption wide-spread area can be done at a level that is commercially viable (Parnell et al., 2023). Biosorption involves a liquid phase containing a culture of suspended Bioweathering studies have focused on elucidating microbial com- organisms that are active (alive) or inactive (dead) in which the biomass munities' influence on bioweathering leaching efficacy, with the popular acts as the biosorbent material. The surface of the microorganisms plays bacteria strains being: Nocardioides, A. thiooxidans, Pseudomonas, a crucial role in this proces by offering negative (such as carboxyl, Sphingomonas, Bacillus, and Paenibacillus (Chikkanna et al., 2021; Potysz hydroxyl, and phosphate) and positive (such as amine) functional et al., 2020; Sun et al., 2020). Although research in bioweathering is groups.
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While ion-exchange is responsible for binding negatively popular for other elements (e.g., Fe, P, Si), research into REEs recovery is charged groups to metal cations, electrostatic interactions or hydrogen still limited (Chikkanna et al., 2021). binding forces are responsible for the adsorption of anions. Additionally, A typical bacterium strain for bioweathering for REEs recovery is amine groups can also chelate cations. In this sense, the adsorption of A. niger, whereby evidence of A. niger colonization was observed on the REEs on the cell wall falls into four sub-categories: electrostatic inter- surface of monazite ores in the form of etched patterns. This bio- action, ion exchange, surface complexation, and surface precipitation weathering is possible due to the excretion of organic acids such as (Fig. 2). oxalic acid (46 mM) and citric acid (5 mM) (Kang et al., 2021). This This process is an economical, simple, and environmentally friendly study showed that after 4 weeks of incubation, the concentration of REEs process for pre-concentration and separation of REEs; although there are in the biomass increased from 0.4 mg/L to 1.1 mg/L. extensive studies on the potential of biosorption of REEs from various To accelerate the bioweathering process, comparison experiments resources, the application of the process is limited to laboratory scale using biostimulation, bioaugmentation, root exudates, and water were studies. This raises the question of how feasible this technology is conducted. It was found that bioaugmentation using A. thiooxidans and commercially (Brown et al., 2023; Liapun and Motola, 2023; Sachan, root exudate was the most effective for metals leaching (Swed et al., 2019). 5 P.H.N. Vo et al. Science of the Total Environment 908 (2024)168210 Table 2 saline wastewater, with varying salinity and temperature conditions Bioleaching of REEs by different microbes. having no significant effect on La3+ adsorption. Additionally, the sorp- Microbes Lixiviants Leaching REEs resources Ref. tion kinetics is fast (8 min) and can be recycled for 5 cycles (Mohammadi efficiency et al., 2022). Phosphogypsum Other bacteria that have been used for REEs recovery include Bacilus Acidithiobacillus Sulfuric acid 39-98 % [1-3] thiooxidans Gold mine tailing licheniformis, A. niger, Acutodesmus acuminatus, and E. coli. A. niger is Aspergillus sp. Bauxite, Electronic Organic acid 31-91 % [4-8] notable for its recovery of up to 3500 mg La/L (Rezk and Morse, 2023), waste, Coal fly ash, with a biosorption performance of 99.9 % uptake, even in the presence Rare earth ore, of competing ions and interference from other metals. This strain was Fluorescent also highly effective in biosorption of other REEs such as Ce, Nd, and Dy powder Acidithiobacillus Bauxite, Phosphate Sulfuric acid 26.2-62.8 [4, 9, (Kazak et al., 2021). In another study, polyethyleneimine-coated poly- ferrooxidans rock % 10] sulfone-E. coli can uptake 121.2 mg Ru/g, which is significantly higher Gluconobacter Phosphogypsum, Phosphoric 16-100 % [11, than conventional ion exchange resins such as M 500 (17.9 mg/g), oxydans Rare earth ore acid, Sulfuric 12] Amberjet 4200 (31.2 mg/g), and TP 214 (61.9 mg/g) (Kim et al., 2016). acid, Organic acid A. acuminatus has the highest biosorption capacity of Eu (174.2 mg Eu/ Yarrowia lipolytica Rare earth ore Organic acid 34-91 % [6] g) (Furuhashi et al., 2019), however, it should be noted that biosorption Candida Fly ash n.d. 28-63 % [13] capacity is highly dependent on the matrix effect, such as temperature, bombicola pH, and the presence of competing ions. The real matrices consist of Phanerochaete highly acidic mixtures of metals, along with various inorganic and chrysosporium Cryptococcus organic components. In most cases, the leachate solution comprises curvatus much higher concentrations of base metals than those of REEs. In such Enterobacter Monazite Organic acid 0.4-40 mg [9, cases, the biosorption of the target metals is influenced by the compet- aerogenes REEs/L 14, itive interactions amongst different REEs and metal species for binding 15] Penicillium sp. Monazite Organic acid 12.3-23.7 [15] sites, except in rare cases such as A. niger as mentioned above. Pantoea mg REEs/L Molecular and genetic engineering has been explored to improve agglomerans REEs recovery by biosorption with promising results. A common mo- Pseudomonas lecular engineering technique is to transform cells to express specific putida Burkholderia Monazite Rhamnolipids [16] proteins which enhance REEs extraction, such as lanthanide-binding thailandensis tags (LBT). Typical LBTs include Lanmodulin, silica-binding protein, References: [1] Tayar et al. (2022), [2] Hong et al. (2023), [3] Hosseini et al. and OmpA protein, with E. coli being the ideal host for recombinant (2022), [4] Barnett et al. (2020), [5] Bahaloo-Horeh and Mousavi (2022), [6] plasmid production. An engineered strain of Yarrowia lipolytica that had Shen et al. (2023), [7] Ma et al. (2023), [8] Castro et al. (2023b), [9] Fathol- competent cell that expressed the REE-binding protein Lanmodulin lahzadeh et al. (2018b), [10] Tian et al. (2022b), [11] Antonick et al. (2019), bound to the cell surface, showed a superior biosorption capacity (Xie [12] Gao et al. (2023), [13] Park and Liang (2019), [14] Fathollahzadeh et al. et al., 2022b). Further, Y. lipolytica was shown to have excellent multi- (2018a), [15] Corbett et al. (2018), [16] Castro et al. (2023a). component biosorption capacity of up to 49.8 mg Yb/g, 50.3 mg Tm/g, 49.9 mg Er/g, and 48.7 mg Tb/g. Lanmodulin also allowed for high 3.3.1. Active biomass for adsorption selectivity absorption of REEs, particularly in acidic conditions. This is Active biomass for REEs adsorption involves microalgae, macro- done via chelation with phosphate/carboxylate groups and excessive algae, plants, and bacteria. Typically, green microalgae are used, such binding sites introduced in the protein. Further, a transformed E. coli as: Chlorella vulgaris, Calothrix brevissima, Chlorella kessleri, and Spirulina. strain that expressed an LBT and silica-binding protein, showed a Tb However, those microalgae strains have a wide variation of adsorption adsorption capacity maximum of 42 mg Tb/g dried biomass, along with capacity. C. vulgaris can absorb Nd to a maximum of 126.1 mg Nd3+ /g, other REEs of which, up to 90 % was recovered (Xie et al., 2022a). which is roughly 2 times higher than activated carbon (Kucuker et al., Another binding tag is OmpA protein. This protein increased biosorption 2017). A comparison study was conducted to assess the REEs adsorption efficiency 2 to 10-fold, while the affinity for heavy REEs was also capacity of two microalgae strains (C. brevissima, C. kessleri) and one improved. LBT-producing bacteria therefore exhibit superior REEs bio- moss (Physcomitrella patens), with the highest REEs adsorption being sorption via increased biosorption sites. The binding tags also possess a found in P. patens at 0.74 mmol Nd3+/g and 0.48 mmol Eu3+/g (Heil- 2-fold higher REEs biosorption stability constant compared to common mann et al., 2021). Spirulina is also a popular strain applicable for REEs carboxyl functional groups (Chang et al., 2020). This indicates a po- adsorption. The commercial powder form can take up a maximum of tential application for low-grade REEs sources (Park et al., 2017). In 38.2 mg Ce+3/g, while the endemic strain shows an uptake maximum of addition to LBT, a genetically-engineered E. coli and native Arthrobacter 18.1 mg Ce+3/g (Sadovsky et al., 2016). Other potential cyanobacteria nicotianae were tested for REEs biosorption capacity, resulting in a total strains for REEs adsorption are Anabaena sp. and Anabaena cylindrica of 80 %, and over 90 % recovery of total REEs, and middle to heavy REEs (Fischer et al., 2019), particularly in the biosorption of Eu, Sm and Nd. respectively (Park et al., 2020). Macroalgae such as Ulva sp., also work well for REEs recovery from wastewater. Kinetic modelling showed that Ulva sp. can adsorb Ce the 3.3.2.
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Inactive biomass for biosorption fastest, at a rate of up to 92 %. In this case, REEs were primarily localized Besides active biomass, inactive biomass is another biosorbent with in the outer fraction, and bonded to the sulfated polysaccharide of Ulva potential for REEs recovery. The inactive biomass can be either the dried sp. (Viana et al., 2023). To enhance REEs sorption, polysulfone was biomass of microalgae (Galdieria sulphuraria) or the extraction of mac- immobilized onto Turbinaria conoides macroalgae, and through mono roalgae with or without modification (Ulva sp.). For example, a bead was and binary aqueous solution tests, the polysulfone-immobilized macro- produced from extracting inactive biomass (e.g., sericin, alginate, and algae demonstrated a competitive sorption capacity of 98.9 % Pr3+ and poly(ethylene glycol) diglycidyl ether) to recover REEs, with a bio- 99.5 % Tm3+ (Rangabhashiyam et al., 2021). sorption capacity that ranges from 0.28 mmol Eu3+/g to 0.63 mmol Magnetic bacteria are the prevailing microbes for REEs recovery, Eu3+ /g (da Costa et al., 2023). Freeze-dried biomass of G. sulphuraria with Magnetospirillum magneticum capable of adsorbing 37.2 mg La3+ /7 microalgae was used to effectively recover REEs (Palmieri et al., 2022), g. Further, M. magneticum also has the potential for REEs recovery in while dead Ulva sp. biomass recovered 90.7 % La, 95.1 % Ne, and 93.8 % Dy (Arul Manikandan and Lens, 2022). Interestingly, desorption using P.H.N. Vo et al. Science of the Total Environment 908 (2024) 168210 HCl and EDTA can recycle the sorbent six times. and 50 % respectively. Another promising microalga strain for REEs Although biosorption studies on multi-element synthetic solutions recovery is Nannochloropsis oculata, which exhibits an excellent stress provide a more comprehensive assessment of the performance of bio- tolerance to REEs. It can accumulate 83.4 % of Ce at an initial concen- sorbents, studies using real wastewater matrices are scarce. Most bio- tration of 6.0 mg/L (Wu et al., 2022). The red alga Galdieria sulphuraria sorption research has been conducted using binary or ternary metal can also accumulate REEs at significant levels (26 μg Ce/g, 15 μg Nd/g, solutions, hence underestimating the effect of anions on the competitive 11 μg La/g, and 11 μg Y/g) (Nahlik et al., 2022). biosorption of these metals. Another point for improvement is the Bioaccumulation of REEs result in changes in biochemical functions limited usage of other microbes other than bacteria. Since bacteria have in microalgae cells due to REEs-induced stress, likely due to protein been used for REEs biosorption extensively, microalgae and macroalgae misfolding in the endoplasmic reticulum. In cases where REEs mixtures receive little attention. This is despite microalgae and macroalgae are present in the microalgae culture media, transcriptomic analysis demonstrating a comparative biosorption capacity compared to bacte- suggests REEs compete with each other for bio-uptake, resulting in the ria, up to 180 mg REEs/g biomass (Table 3); hence there is great po- inhibited expression of genes involved in carbon fixation and ribosome tential in microalgae and macroalgae REEs biosorption, necessitating biogenesis, which are critical pathways in REEs related stress resistance further investment in research to popularize microalgae and macroalgae (Morel et al., 2021). A transcriptomic analysis of N. oculata (XJ006) usage in biomining. exposed to cerium (Ce), showed that Ce exposure inhibited the expres- sion of genes in the carbon fixation and photosynthesis pathways in conjunction with the expression of ribosome biogenesis genes. Further, 3.4. Bioaccumulation glycerol kinase and acetyl-CoA biosynthesis-related genes were upre- gulated, thereby enhancing resistance of REEs related stress in response Bioaccumulation is the intracellular uptake of REEs through various to Ce exposure via lipid accumulation (Wu et al., 2022). metabolic pathways of the host microbes (Fig. 2). A fundamental Macroalgae (e.g., Ulva lactuca, Ulva intestinalis, Fucus spiralis, Fucus mechanism of uptake is the intracellular transport of REEs by carrier vesiculosus, Osmundea pinnatifida and Gracilaria sp.) can also accumulate biomolecular substances such as proteins, in addition to endocytosis REEs, with U. lactuca the only macroalgae able to accumulate all REEs (Kohl et al., 2023). After intracellular accumulation, REEs are bound to tested such as: Y, Ce, Pr, Nd, Eu, Gd, Tb and Dy (Pinto et al., 2020). In several substances including proteins, lipids, chlorophyll, and peptide addition, this macroalgae strain is able to remove >60 % to 90 % of all ligands (Rezanka et al., 2016; Shen et al., 2002), along with accumu- studied REEs. The removal kinetic also shows that reduction happens lating in cellular vacuoles and organelles that are localized in the rigorously in the first 24 h. Though macroalgae are capable of accu- chloroplast and cytoplasm of cells. To alleviate the stress induced by mulating REEs, green (Codium tomentosum, Ulva rigida), red (Gracilaria REEs, cells start replacing other divalent cations (e.g., Ca+ and Mg2+) gracilis, Osmundea pinnatifida, Porphyra sp.), and brown species (Sacco- with REEs (Wu et al., 2016). REEs accumulation then enhances the rhiza polyschides, Undaria pinnatifida) show a different level of REEs enzymatic activity of cells via increasing activity of superoxide dis- accumulation as well as the ratio of light:heavy REEs accumulated in the mutase, peroxidase, and catalase. The most popular candidates for REEs cells (Milinovic et al., 2021). The REEs accumulation in green and red bioaccumulation studies are bacteria, microalgae, macroalgae, and macroalgae ranges from 0.7 to 1.7 μg/g which is much higher than in plants; however, bioaccumulation of REEs has also been reported in other species (0.1-0.2 μg/g). The ratio of light:heavy REEs in brown other hosts (e.g., eel, oyster, mussel, fish). Given that studies reporting macroalgae was higher than in green macroalgae, indicating brown bioaccumulation of REEs in hosts other than bacteria, microalgae and macroalgae preferentially accumulate heavy REEs. macroalgae focus on toxicity rather than REEs recovery, these studies Higher plants also have the potential for REEs recovery from mining are considered to be outside the scope of this review and have therefore wastewater (e.g., Salix myrsinifolia, Salix schwerini, P. americana, and been excluded. P. marigold). Salix species (Salix myrsinifolia and Salix schwerini) can Microalgae have been studied extensively for REEs bioaccumulation uptake a range of REEs such as La, Y, Nd, Dy and Tb effectively, with La with a wide range of strains and REEs of interest. Three microalgae accumulation of up to 8400 μg/g dry weight in root tisue alone (Mohsin strains (e.g.,， Desmodesmus quadricauda, Chlamydomonas reinhardti, et al., 2022). They also display phytostabilization potential through Parachlorella kessleri) were assessed for their REEs accumulation effi- translocation and bioconcentration factors. Other plants such as ciency (Cizkova et al., 2019). It was found that D. quadricauda demon- P. americana, can accumulate REEs in leaves at concentrations of up to strated the highest REEs accumulation capability, up to 27.3 mg/kg/d, 1040 μg/g (Liu et al., 2021). Variation of REEs accumulation in plants which is higher than C. reinhardti and P. kessleri by approximately 10 % Table 3 The performance of different microalgae for REEs recovery. Specie name Groups of organisms Resource Sorbate Qma Mechanism Ref. C. vulgaris Microalgae Industrial waste Nd 188.68 mg/g Langmuir isotherm [1] Pseudo-second order C. brevissima, C. kessleri Microalgae Spiked solution Nd, Eu Nd: 0.74 mmol/g Langmuir isotherm [2] Eu: 0.48 mmol/g Freundlich isotherm Arthrospira sp. Cyanobacteria Spiked solution Ce 18.1-38.2 mg/g Langmuir isotherm [3] Freundlich isotherm Ulva sp. Macroalgae Industry wastewater Y, Eu, La, Ce 382 mg Y/g Pseudo second order [4] 198.2 mg La/g 184.9 mg Eu/g 191.5 mg Ce/g Uva sp.
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Macroalgae Spiked solution La, Nd, Dy 171 mg La/g Langmuir isotherm [5] 187 mg Nd/g 189 mg Dy/g Pseudo-second order Magnetospirillum magneticum Bacteria Spiked solution La 6.0 mg/g Langmuir isotherm [6] Bacillus licheniformis Bacteria Spiked solution Ce 38.93 mg/g Freundlich model [7] Pseudo-second order Acutodesi ninatus Bacteria Industrial waste Eu 174.2 mg/g Langmuir isotherm model [8] References: [1]: Kucuker et al. (2017); [2]: Heilmann et al. (2021); [3]: Sadovsky et al. (2016); [4]: Viana et al. (2023); [5]: Arul Manikandan and Lens (2022); [6]: Mohammadi et al. (2022); [7]: Cheng et al. (2022); [8]: Furuhashi et al. (2019). ： P.H.N. Vo et al. Science of the Total Environment 908 (2024) 168210 can be attributable to a range of factors, including available P, pH, and addition, bioprecipitation is unique to bacteria and does not work with TOC (Zhang et al., 2023). microalgae, macroalgae, and plants. Biosorption (active biomass) and bioaccumulation technologies A comprehensive investigation reveals that processes of bio- complement each other to recover the chemicals of interest in an precipitation have been developed at a pilot scale for resources of metals aqueous solution. Like biosorption, bioaccumulation is best suited for during hydrometallurgical processing (Sethurajan and Gaydardzhiev, bacteria (and plants) as they thrive well in the harsh conditions of 2021), which shows the maturity of this technique for metal extraction. mining waste. As mentioned above, some microalgae strains can adapt In contrast, REE bioprecipitation has been implemented mostly in well to similarly harsh conditions (Abiusi et al., 2022; Nahlik et al., controlled conditions, making the upscaling process of bioprecipitation 2022) and can therefore be applied in various forms of microalgae-based unsuitable as the operating parameters are widely variable (Kachieng'a technologies. These technologies include; flat plate and tubular photo- and Unuofin, 2021). bioreactors, high-rate algae ponds, or even membrane photobioreactors, following the bioleaching stage (Vo et al., 2019). This hybrid system is 3.6.Bioflotation promising as microalgae produce pigment which has high commercial value and grow faster than some bacteria. Currently, most microalgae Bioflotation is the process in which microbial metabolism and the biotechnology focuses on recovering nitrogen and organic carbon from bioproducts (such as surfactants or froth) is used to harvest minerals and mining wastewater rather than REEs (Geng et al., 2022; Wang et al. metals of interest (Fig. 2). This is achieved by altering the surface state of 2023). Like other techniques for REE biomining, bioaccumulation has REEs which significantly contributes to a high yield flotation. not been fully developed to offer a cost-effective, feasible alternative for The first form of bioflotation is using microorganisms that act as recycling REEs commercially (Opare et al., 2021). inhibitors. For instance, Rhodococcus opacus attached to the surface of malachite, changes the hydrophobicity of this mineral which contributes 3.5. Bioprecipitation to the recovery of 93 % of minerals after bioflotation (Kim et al., 2017). Similarly, A. ferrooxidans bacteria degrades pyrite in galena and sphal- In conventional REE extraction technologies, REEs are precipitated erite minerals (Mehrabani et al., 2011). by adding chemicals, whereas in bioprecipitation, microorganisms play Microbial metabolism is the second form of bioflotation for REEs a critical role in the oxidative-reductive reaction for precipitation to recovery. A typical example of this bioflotation form is Fe(Il) oxidation occur. Carbonate, phosphate, sulphide, etc. are produced by microbial from pyrite to Fe(IIl) by Thiobacillus ferrooxidans. Again, the surface metabolisms that precipitate REEs. Moreover, bacterial oxidation pre- characteristics of minerals were altered by T. ferrooxidans, allowing for cipitates biogenic minerals (e.g., silica, iron oxides, manganese oxide) the recovery of REEs through flotation (Hosseini et al., 2005). Another that absorb REEs, which then co-precipitates with them (Fig. 2). Phos- study used a group of bacteria (Halobacillus sp. and Marinobacter sp.) to phate precipitation is a common process of bioprecipitation. When oxidize surface pyrite and chalcopyrite to form hematite. The hematite enough organic phosphate is supplied in the medium, phosphatase surface, together with both types of bacteria, promoted pyrite deposition located externally in the microbial polymeric matrix, precipitates REEs and chalcopyrite buoyancy (Gonzalez-Poggini et al., 2021). In addition, by catalyzing REEs' binding to this phosphate. microbial oxidation also changes the hydrophobicity of the mineral Some typical strains of bacteria that facilitate the precipitation of surface. Citrobacter sp. was found to oxidate sulfur in the galena (PbS) metals are Desulfosporosinus acididurans, Desulfosporosinus acidiphilus, and sphalerite (ZnS) ores, leading to a significant recovery of 80-90 % of Thermodesulfobium narugense, Thermodesulfobium acidiphilum, Acine- metals (Sanwani et al., 2021). tobacter sp. H12 (Frolov et al., 2017; Sanchez-Andrea et al., 2015; Wu The last form of bioflotation involves using microorganism by- et al., 2021). The sulfate-reducing bacteria A. thiooxidans has also been products that act as a biopolymer in the form of extracellular poly- shown to precipitate 90 % of soluble metals via the formation of metal meric substances (EPS). EPS facilitates the fixation of REEs surrounding sulfates (Fang et al., 2011). Bioprecipitation also works in conjunction the cells and in some cases, where excreted EPS is foamable, REEs can be with biosorption in microbial consortia in recovering metals. It was recovered by collecting the foam. found that the wild type strains of Paraclostridium bifermentans and Alicyclobacillus sp. have been found to secrete surfactants that have Klebsiella pneumoniae) can remove between 83.8 %-91.1 % of soluble contributed to the recovery of 80-90 % of metals (Sanwani et al., 2021). metals after 30 h (Saikia et al., 2022). However, the metal precipitates Similarly, Staphylococcus carnosus, through the secretion of some exo- formed are microbial strains specific. The sulfate salt and zerovalent polymers, were found to change the surface charge of coal, allowing for metals are the primary precipitates driven by P. bifermentans, whereas the recovery of up to 90 % of metals in 12 h (Ramos-Escobedo et al., chloride and phosphate salts are the main products of K. pneumoniae. 2016), while crude biosurfactant extracted from Rhodococcus opacus has Further, the composition and concentration of the leaching solution been found to support the buoyancy of hematite, allowing for approxi- strongly effects the chemical form of the precipitates. The symbiotic mately 95 % recovery of hematite through bioflotation at pH 5. The interaction of sulfate-reducing, metal-reducing, sulfur-oxidizing, and addition of R. opacus also made hematite more hydrophobic in an acidic denitrifying bacteria participates in the whole process of bio- environment (Puelles et al., 2021). precipitation (Cilliers et al., 2022). In addition, metals can also be Bioflotation technology efficiently recovers minerals and metals such precipitated through a calcium precipitation process catalyzed by Aci- as iron, copper, lead, zinc, etc. However, this technology is still under netobacter sp. H12 (Wu et al., 2021). Some of the precipitation was consideration for REEs recovery applications as the concentrations of facilitated by bacteria to form biocrystal seeds. In addition, some REEs is comparatively low, while the purification of REEs in the su- microorganism strains can simultaneously precipitate REEs and fix ni- pernatant will add to the recovery cost making this method lessefective trogen which is beneficial to the environment (Sakpirom et al., 2019). than other methods.
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Furthermore, there are some limitations in the Further, bioprecipitation derived biogenic sulfides are more effective upscaling process that are mostly related to the direct usage of micro- than chemically derived sulfides in precipitating metals, with up to organisms in flotation. The application of biosurfactants can prevent the 44-60 % of metals vs 4-6 % of metals being precipitated via biogenic limitations related to operational issues; however, environmental and sulfides or chemically derived sulfides respectively (Saikia et al., 2022). economic investigations are still needed to evaluate the feasibility of However, there is little published research related to bioprecipitation of pilot and commercial developments (Asgari et al., 2022). REEs and other heavy metals to date. The underlying reason might be attributable to the trace concentrations of REEs in the ore, which is technically challenging to harvest using the right precipitate. As a result, leaching is the primary solution for recovering high-purity REEs. In P.H.N. Vo et al. Science of the Total Environment 908 (2024) 168210 4. Effects of operating conditions and matrix on REEs recovery proportional to the adsorption capacity (Gupta et al., 2019; Iftekhar et al., 2017). Sorption is suppressed at temperatures ranging from 20 to 4.1.pH 35 °C, while higher temperatures increase sorption capacity via elevated surface activity and energy kinetics of REEs (Vijayaraghavan and Yun, One of the most critical physicochemical factors impacting REEs 2008). However, high temperatures beyond the tolerance level of mi- recovery is pH. It significantly affects speciation of REEs in solution, crobes will inhibit microbe growth and result in cellular damage. In this with most studies indicating a pH range of 1 to 7 as the optimum range sense, it is challenging to screen microorganism strains that are tolerant for the speciation of REEs. Conversely, at higher pH, insoluble hydrox- to high temperatures for a more selective and faster REEs recovery ides will form which decreases REEs recovery through different bio- (Engelbrektson et al., 2018; Sethurajan et al., 2018). For example, systems (Abd El-Magied et al., 2017; Rasoulnia et al., 2021). This G. sulphuraria and Thermus scotoductus SA-01 have been successfully explains why microbes (e.g., A. ferrooxidans, A. thiooxidans) were used for REEs recovery at 42 °C (Ciniglia et al., 2014; Minoda et al., applied to leach REEs, as their lixiviant can reduce the pH of a solution 2015) and 65 °℃ (Maleke et al., 2019b). Meanwhile, increasing the down to 1.8-2 (Hosseini et al., 2022; Tian et al., 2022a). pH also has a temperature to 75 °C enhances REEs sorption in the culture of Cupria- reverse relationship with redox potential; whereby decreasing pH will vidus necator (Adekanmbi et al., 2020). The same results were reported increase redox potential and support the leaching of REEs (Castro et al., for bioleaching of Y, Sc, and La, where an increase in temperature from 2020). Due to this importance of pH in biomining technologies, the 28 to 45 °C increased the leaching of REEs (Muravyov et al., 2015). In operating conditions of the relevant technologies should be optimized the case of bioaccumulation or biosorption using active cells, an optimal for the desired microorganism. For example, sustainable production of temperature to keep the cells alive is necessary (Dhankhar and Hooda, sulfuric acid excreted by A. ferrooxidans in order to maintain a low pH 2011; Panda et al., 2021). level has been found to require optimal operating conditions (640-680 mV Eh, pH 1.3-1.5, 4-6 d HRT and 6 % pulp ratio) in order to maintain 4.3.Presence of metals consistent acid production (Sarswat et al., 2022). In addition, based on the type of biomining technologies, pH also Metals can compromise REEs recovery for two reasons: (i) causing needs proper adjustment to avoid negatively impacting REEs recovery. toxicity to the microbial community and (i) competing with REEs in the For example, when REEs sorption is a downstream process after the sorption process. The toxicity effects of metals can be classified into two bioleaching process, the pH will need to be adjusted after the bio- levels: substitution of intracellular essential ions in enzymatic or leaching process depending on the REEs of interest and the applied nutrient transport systems; and an impediment in microbial metabolism sorbents (Castro et al., 2020). Increased pH compromises the sorption due to intracellular accumulation and enzymatic inhibition (Jia et al., capacity due to the low affinity to the cell surface, while a neutral pH 2019; Monballiu et al., 2015). For instance, substituting vital calcium increases the sorption of light REEs. In comparison, a low pH increases ions with REEs adversely impacted bacterial growth (Homer and Mor- the sorption of heavy REEs. For example, Y and lanthanide are prefer- timer, 1978; Yang et al., 2016). This is why a higher concentration of entially adsorbed at pH 4.5 to 6.5, whereas the optimal pH for Sc is from REEs leads to a decrease in microbial growth. The metal toxicity issue 3 to 5 (Lozano et al., 2020). In addition, there is a preferential range of can also be expanded to other metal ions in the solution (Vijayaraghavan pH in which each type of microbes can absorb REEs at a maximum level. and Yun, 2008). For example, concentrations of Eu3+ higher than 16.7 At pH 3-5, the availability of oxygen-rich functional groups on the cell mg/L adversely affected the growth of Clostridium sp. 2611 (Maleke surface is substantial, such as carboxyl in gram-negative bacteria or et al., 2019a). Moreover, concentrations of Ce3+ and Gd3+ higher than phosphate in gram-positive bacteria (Kazy et al., 2006). The range of pH 6.4 mg/L had a toxic effect on Vibrio fischeri (Kurvet et al., 2017). should therefore be determined according to the type of REEs, the The presence of competing ions (e.g., Cs+ and Cu2+) decreased Nd3+ microorganism, and the process conditions. recovery due to competition for available active sites on biosorbent surfaces (Hisada and Kawase, 2018). The biosorption capacity was 4.2. Temperature found to be influenced by the electronegativity of the cations; Cu (1.90), Nd (1.14), Na (0.93), and Cs (0.79), with higher electronegativity Temperature is also a complicated factor considering that it also enhancing the sorption of ionic atoms on the charged surface of a bio- impacts various aspects such as chemical reactions, solubility of REEs, sorbent. Cu can easily replace Na in -COONa rather than H in -COOH, and the growth rate of microorganism. Based on the optimal growth leading to a more significant impact on biosorption efficiency (Hisada temperature, microorganisms can be classified into three main groups: and Kawase, 2018). psychrophilic, mesophilic, and thermophilic (Cao et al., 2021; Dev et al., 2020). Each biomining technology also requires a specific range of 4.4.Aeration temperature. A typical energy-efficient temperature range for REEs re- covery is between 17 °C and 32 °C (Gupta et al., 2019). Chemolithotrophic microorganisms used in REEs recovery obtain Solubility of most REEs complexes decreases with an increase in their energy for growth and proliferation by oxidation of inorganic temperature, except for complexes of REE-chlorides and nitrates (Cao molecules. In this regard, oxygen utilized as the terminal electron et al., 2021; Das et al., 2017; Das et al., 2019; Meshram et al., 2016; acceptor must be sufficiently supplied (Barros et al., 2019; Dev et al., Muravyov et al., 2015). In addition, the solubility of oxygen and carbon 2020). It has been reported that high-rate aeration could provide enough dioxide, which are essential for bioactivity, also decreases with oxygen in bioleaching by A. ferrooxidans (Gu et al., 2017). However, the increasing temperature.
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In contrast, chemical reactions increase with a way to introduce air into bioreactors which are influenced by their type temperature rise; thus, it positively affects REEs extraction (Rasoulnia and configuration, should also be considered. For example, baffles are et al., 2021). As a result, gas solubility and chemical reactions work used on the wall of bioreactors to create high turbulence, however sig- against each other in relation to temperature. In terms of biochemical nificant shear stress becomes a factor for microbial attachment and function, at optimal temperature, an extra benefit is an increased pro- biofilm formation (Dev et al., 2020). duction of extracellular polymeric substances, escalating the microbes' Traditionally, atmospheric air at low and medium temperatures is attachment to the metal surface (Bellenberg et al., 2015; Kachieng'a and purged into the system to supply dissolved oxygen for microbes; how- Unuofin, 2021). Considering the multi-dimensional effects of tempera- ever, the high loading of suspended solid and sulfide necessitates an ture on REEs recovery, the optimal range of temperature should be increase in dissolved oxygen supply in order for bacteria to thrive. determined based on the desired circumstances. Oxygen-enriched air is an alternative given that, at a specific solid load Sorption is an endothermic process in which temperature is directly of 20 % (w/w), the dissolved oxygen level in the culture is maintained at 9 P.H.N. Vo et al. Scienceof theTotalEnvironment908(2024)168210 4-13 ppm (Guezennec et al., 2017). Beyond 17 ppm, the microbial ac- component, which is much simpler than in the DT’ mine tailing (e.g., tivity significantly decreased and compromised leaching efficiency. quartz, pyrite, gypsum, silicate). This suggests that the complicated Therefore, efficient bioleaching operation is also linked to the aeration matrix of mining tailings can compromise bioleaching efficacy (Table 4). regime and bioreactor configuration. 5. Sustainability of biomining technologies for REEs recovery 4.5. Other factors Biomining is undoubtedly beneficial for industry, the economy, and the environment, particularly from a sustainability standpoint. Sus- Another factor that is crucial for efficient REEs recovery is pulp tainable biomining should be comprised of four main criteria: (i) pro- density. Pulp density (as %) is defined as the mass of a mineral per moting environmental resilience, (i) cost-effectiveness and high volume unit. Pulp density is an important factor since it not only limits revenue, (i) viability of technologies, and (iv) availability of low-grade the input flux of oxygen and carbon dioxide, but it reduces microbial REEs sources. The below SWOT and Techno-economic assessment are growth when heavy metal concentrations are high (Brandl et al., 2016; discussed based on these criteria. Wang et al., 2014). Pulp densities higher than 5 % in red mud have been shown to elevate the pH of the solution during REEs recovery due to the following reasons: i) the higher pulp density intensified microbial 5.1. SWOT analysis toxicity resistance, and i) enhanced acid-neutralizing capacity of red mud. This affects the efficiency of REEs bioleaching, with a red mud pulp SWOT analyses were conducted to assess biomining technologies' density of 20 g/L allowing for the most efficient bioleaching (Qu and sustainability and suitability for recovery of REEs (Table 5). Three Lian, 2013). Further, an increase in pulp density from 1 % to 5 % criteria are used in this review: technical, environmental, and economic significantly reduces La recovery from 63 % to 33 % (M. and Baral, aspects. About 25 peer-reviewed articles out of 45 searched articles were 2019). selected for SWOT analysis. The other essential factor in using live cells is balancing culture The result of SWOT analysis indicates that biomining is a sustainable media and essential nutrients (Dhankhar and Hooda, 2011). Although approach for REEs recovery from low-grade resources with low envi- the cost of organic nutrients can be high, cheaper alternatives such as ronmental impact. Biomining comes with the added benefit of reducing sugar cane bagasse, vinasse, whey, and molasses can be used to reduce the CO2 footprint of pyro- and hydrometallurgy technologies and recy- costs when recovering REES from mining wastewater (Panda et al., cling wastes from other sources (e.g., agricultural waste, food waste, 2021). For example, bagasse which is rich in sucrose, was used as a industrial waste) by utilising them as a nutrient source for microbes. carbon source in the REEs bioleaching process using A. niger and Biomining technologies also do not produce hazardous by-products P. simplicissimum (Shah et al., 2020). The additional nutrients not only unlike traditional REEs recovery methods. Regarding the economic improved the growth of microbes, but also accelerated the REEs aspect, biomining is a low-cost technology requiring low ongoing extraction process. Similarly, glucose, glycerol, and NH4Mo+2 can operational costs, energy, and workforce requirements. Biomining effectively increase siderophore production, which is central to bio- technologies are expected to be partly or close to fully automated in the extraction and release of REEs from mineral sources (Sethurajan et al., future; however, this depends on the market requirement of REEs purity, 2018). which would affect the overall cost of post-processing. For example, 1 kg Bioleaching efficiency is also mining-site specific. For instance, the of Sc metal costs $3000 USD/kg (99.99 % purity) or $6000 USD/kg maximum leaching efficiencies of light and heavy REEs were 54 % and 6 (99.999 % purity) (ISE, 2019). % respectively in the DT' site (Ontario, Canada); whereas they reached Regarding technical feasibility, biomining has been demonstrated to 58 % and 14 % in the RAT' site (Ontario, Canada) (Reynier et al., 2021). be highly efficient and selective for REEs recovery. However, it does The leading cause of this discrepancy was the composition of the tailing have a long operational time from months to years and is not versatile in between two ores. The tailing of the ‘RAT' mine has quartz as the main harsh environmental conditions which are significant limitations that Table 4 Key technical principles of biomining treatment technologies. Technologies REEs resources Participated pH Temparature Pulp REEs Country References microorganisms (°C) density extraction (w/v) efficiency Bioleaching Inactive uranium mine, Sulfur- and iron-oxidizing 2 30-50°℃ 10 % 14-89 % Canada [1-3] monazite, phosphogypsum, bacteria, fungi bauxite Biosorption Wastewater, ore leachate Bacteria, cyanobacteria, 2-5.6 20-60°℃ 99 % China, China, [4-10] microalgae, macroalgae, 182 mg/kg Japan moss Bioaccumulation Red mud, mining waste Microalgae, macroalgae, 10 % v/v 26 °℃ 83.4 % China, Italy [11-13] plant HNO3 11-26 mg/kg Bioprecipitation Mining wastewater Incomplete oxidizers, pH 5.5 USA [14-17] complete oxidizers, sulfate- reducing bacteria Bioflotation Pyrite, sphalerite - galena Bacteria pH 8.0 25-50 % 70-80 % Indonesia, [18, 19] mineral India Bioweathering Monazite, basalt, rhyolite, Bacteria, biotic respiration Oxalic 2 % 0.4-1 mg/L United [20, 21] granite and schist acid (~46 5.246.8 Kingdom, mM) nmol/g Canada Citric acid biomass. (~5 mM) References: [1] Reynier et al. (2021); [2] (Shen et al., 2023), [3] Park and Liang (2019), [4] Giese and Jordao (2019), [5] Liang and Shen (2022), [6] Kim et al. (2011), [7] Heilmann et al. (2021), [8] Fischer et al. (2019), [9] Viana et al. (2023), [10] Mohammadi et al. (2022), [11] Wu et al. (2022), [12] Nahlik et al. (2022), [13] (Cizkova et al., 2019), [14] Murray et al. (2015), [15] Saikia et al., (2022), [16] Cilliers et al. (2022), [17] Sanchez-Andrea et al., (2015), [18] Sanwani et al. (2016), [19] Vasanthakumar et al. (2012). 10 P.H.N. Vo et al. Science of the Total Environment 908(2024)168210 Table 5 SWOT analysis of biomining technologies for REEs recovery.
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Considered Considered criteria Strengths Weaknesses Opportunities Threats aspects Technical Overall treatment High extraction efficiency Slow reaction times Optimal reaction time High cell densities required aspects performance (>80 %). High temperature required. identified via optimal for leachate. High selectivity for a range Effects of functional groups on microbial growth. Maintain optimal microbial of REEs. biosorption is not fully High throughput screening is growth conditions and Genetic engineering investigated. necessary. continuous organic carbon enhances recovery Low chemical resistance and Immobilized cells is supplements. efficiency (56-87 %). mechanical strength preferable for industrial Complicated microbial- Biosorption coupled with Low resilience to harsh applications. mineral interactions (e.g.. other techniques increases operating conditions. redoxolysis, acidolysis, extraction efficiency. complexolysis). Bioflotation is applicable to Wide variation of applied seawater. bacteria strains, cell wall composition, and reaction conditions. Operating conditions Temperature: 30-35 °C. Overly high temperature Increasing temperature will Wide fluctuation of Optimal pH is metal- compromises oxidation of increase biosorption rate (3 to temperature and pH inhibits specific. elemental sulfur. 4-fold at 70 °C). microorganisms. Maximum recovery depends on Biosorption requires specific whether processes are pH and temperature. endothermic or exothermic. Extraction and recovery Bioleaching and Extraction and recovery Reducing CAPEX and OPEX Bioelectrical technology has efficiency biosorption are matured effciencies vary amongst costs rather than pyro- and low resilience to mining technologies. technologies and target hydrometallurgy wastewater. elements. technologies. Challenge in applying Bioelectrochemical and bioelectrical technology for bioflotation still immature. real wastewater. Toxicity Considered n.a. n.a. n.a. environmentally friendly. Bioreagents are less toxic. Environmental Impact on aquifer/ Reduce hazardous waste Targeted at metal recovery, Address national priorities, Requires a large land aspects existing environment and impacts to the rather than environmental such as job creation and footprint. environment. remediation. resource recovery. Economic Status of development Focus on high-value metals n.a. Economic viability at a Bioflotation: still at (Nd, Sc). commercial scale (e.g.. aspects laboratory scale. Reuse phytic acid for bioleaching, biosorption). Unclear techno-economic bioprecipitation. assessment. Treatmentcost Appropriate n.a. Lower expenditure on carbon Costs of some organic carbon microorganisms' usage emission and energy. feed are still high (44 % reduces OPEX cost (60 %). overall cost). Do not rely on expensive and aggressive reagents. Resilient to difficult Resilient to harsh red mud Cyanobacteria are vulnerable conditions (Tunnels, waste (Galdieria to high alkalinity wetlands, riparian zones, sulphuraria). populated zones). Data for SWOT analysis were retrieved from the previous section. must be addressed (Petersen, 2016). A potential solution would be the process environmentally and economically friendly and sustainable. To development of a high throughput screen, which would allow for the make biomining sustainable, it is required that the loop of REEs recovery rapid identification of an optimal strain of microorganism for a specific should be closed, meaning the waste of biomining should be circulated REEs resource recovery application. Currently in the US, there is no back into the recovery process. This is challenging as the characteristics prototype at a technology readiness level higher than 4 (scale 1-9) for of REE secondary sources (e.g., concentration and abundance) vary biomining of REEs, although biomining has been commercially wide- widely. spread for precious metals (e.g., Au, Ag, Cu) recovery (Brown et al., The cost breakdown of the whole biomining process typically con- 2023). Countries such as Finland, Chile, and Uganda progressively use sists of processing/primary leaching (77.1 %), biosorption (19.4 %), biomining technologies (Marcos, 2018), with one example being a two precipitation, and roasting (3.5 %) (Jin et al., 2017). The profitability of stage biohydrometallurgy process. The first stage involves the use of REEs extraction depends on a few factors: REEs concentration in the acidophilic iron, and sulfur-oxidizing microbes to extract base metals, ores, the composition of the feedstocks, the cost of pre-treatment, and and the second stage involves the solubilization of rare earth and mining waste management. Processing of minerals always occupied the precious metals (Magoda and Mekuto, 2022). Biomining technologies highest fraction of overall cost, especially for the low-grade ores; how- are also scalable, which allows for varying amounts of REEs to be ever, this can be offset by the high value of minerals in the ores (Spooren extracted. This makes biomining technologies more flexible to adapt to et al., 2020). For the feedstock, an extensive study has been conducted to local geographical conditions. Many biomining technologies, such as investigate which feedstock returns the highest profit. Results indicated bioflotation, bioprecipitation, bioelectrochemical, have not been well that coal ash, which contains substantial REEs fractions, returned the studied despite their immense potential. highest profit, while high-grade ores do not return as much profit as the other feedstocks due to high material cost. The high cost of the primary 5.2. Techno-economic assessment leaching stage can be attributed to the carbon source (e.g., glucose) used for feeding bacteria, as this can contribute up to 44 % of the total cost REEs recovery process should incorporate standards to make the (Thompson et al., 2018). Wastewater from corn stover returns the 11 P.H.N. Vo et al. Science of the Total Environment 908 (2024) 168210 highest revenue amongst other carbon sources (Fig. 3). The major sociodemographic conditions. Hence, the application of biomining discrepancy between corn stover and other carbon sources is that the for REEs recovery would require proper calibration to maximize its collection cost is low, and the energy cost is low as burning lignin res- performance and revenue. idues offset electricity costs. The characteristic of REE sources also im- · Bioleaching using bacteria is a mature technology with high pacts the techno-economic feasibility of technologies. REEs from fly ash extraction efficiency (>80 %); however, it is a time-consuming has low solubility, so its techno-economy feasibility when using some process (months to years) and is currently applied to other metals specific sorbents such as PEGDA beads and Si sol-gels for REEs recovery at full scale. is unlikely to be appreciated (Alipanah et al., 2020). · Biosorption and bioaccumulation comprise a range of hosts (e.g., At this stage, there are few TEA analyses related to REEs biomining in bacteria, microalgae, macroalgae, plant). There is a lack of pilot and the literature. The above discussion has indicated the importance of, and full-scale applications. the need for comprehensive TEA analysis being conducted before com- · The recovery stage using bioprecipitation and/or bioflotation seems mercial deployment of biomining. Based on the TEA analysis, several to be far off from full-scale application. solutions have been proposed to make biomining a more realistic option · sSWOT and techno-economic assessment results indicate biomining for REEs recovery, including proper pulp ratio, optimization of mineral is a sustainable approach for recovery of REEs from low-grade re- processing, and alternative for high cost lixiviants. sources with low environmental impact. The carbon source for bac- teria occupies 44 % of the total cost. Amongst mining waste, coal ash 6. Conclusion is shown to have the highest profit. Biomining for REEs recovery is a viable and sustainable alternative.
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Given the success in REEs recovery from published biomining There are some critical points that must be addressed: studies, conducting more in-depth research and technology transfer is necessary to further optimize biomining technologies. It is recom- · The abundance and concentration of REEs in mining waste vary mended that efforts in screening efficient strains and metabolic engi- widely depending on the specific mining sites, and geochemical and neering need to be improved for greater REEs recovery efficiency. While Refined glucose 4 Corn Stover Potato waste 3.5 Glucose 3 2.5 S n 2 100 1.5 0.5 0 Total cost Revenue Net profit Fig. 3. Total cost, revenue, and net profit for bioleaching process by Glucobacter oxydans of industrial waste using different feedstock (i.e., refined glucose, corn stove, potato waste, and glucose). Data was retrieved from various sources (Jin et al., 2019; Thompson et al., 2018). The scenario is built upon 285 tons of REEs being produced per year using 19,000 tons of raw material. P.H.N. Vo et al. Science of the Total Environment 908 (2024) 168210 bacteria have been applied widely in biomining, further investigation in Barros, O., Costa, L., Costa, F., Lago, A., Rocha, V., Vipotnik, Z., Silva, B., Tavares, T., microalgae/macroalgae driven REEs recovery is needed as they can also 2019. Recovery of rare earth elements from wastewater towards a circular economy. Molecules 24 (6), 1005. add further value through pigment production. Apart from technological Bellenberg, S., Barthen, R., Boretska, M., Zhang, R., Sand, W., Vera, M., 2015. improvement, relevant social, environmental, and economic assess- Manipulation of pyrite colonization and leaching by iron-oxidizing Acidithiobacillus ments must also be performed in order to provide a comprehensive species. Appl. Microbiol. Biotechnol. 99 (3), 1435-1449. Brandl, H, Barmettler, F., Castelberg, C., Fabbri, C., 2016. Microbial mobilization of rare understanding of sustainable biomining. earth elements (REE) from mineral solids: a mini review. AIMS Microbiol. 3 (2), 190-204. CRediT authorship contribution statement Brown, R.M., Mirkouei, A., Reed, D., Thompson, V., 2023. Current nature-based biological practices for rare earth elements extraction and recovery: bioleaching and biosorption. Renew. Sust. Energ. Rev. 173, 113099. Phong H.N. Vo: Conceptualization, Formal analysis, Investigation, Cao, Y., Shao, P., Chen, Y., Zhou, X., Yang, L., Shi, H., Yu, K., Luo, X., Luo, X., 2021. Methodology, Writing - original draft. Soroosh Danaee: Writing - A critical review of the recovery of rare earth elements from wastewater by algae for resources recycling technologies. Resour. Conserv. Recycl. 169, 105519. original draft. Ho Truong Nam Hai: Writing - original draft. Lai Castro, L., Blazquez, M.L., Gonzalez, F., Munoz, J.A., 2020. Bioleaching of phosphate Nguyen Huy: Writing - original draft. Tuan A.H. 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Bioresource Technology Reports 17 (2022) 100992 Contents lists available at ScienceDirect BEORESOLURCE REPORTS Bioresource Technology Reports ELSEVIER -technology-reports Orotic acid production from crude glycerol by engineered Ashbya gossypii Rui Silva, Tatiana Q. Aguiar, Lucilia Domingues CEB - Centre of Biological Engineering, University of Minho, 4710-057 Braga, Portugl LABBELS -Associate Laboratory, Braga, Gumaraes, Portugal ARTICLEINFO ABSTRACT Chemical compounds studied in this article: Orotic acid is an intermediate of the de novo pyrimidine biosynthesis that plays a crucial role in several nutra- Orotic acid (PubChem CID: 967) ceutical supplements. In some microorganisms, blockage of this pathway downstream the dihydroorotate de- Keywords: hydrogenase (DHOD) leads to orotic acid accumulation. Here, the Ashbya gossypi Agura3 pyrimidine auxotroph Orotic acid was shown to accumulate and excrete orotic acid (~1.5 g/L), and this trait was further explored for the pro- De novo pyrimidine biosynthesis duction of orotic acid from raw substrates. Metabolic engineering of this strain combined with culture conditions Ashbya gossypii optimization led to a 3.6-fold increase in orotic acid production from crude glycerol. The mitochondrial DHOD Saccharomyces cerevisiae encoded by AgURA9 was shown to be determinant for this phenotype. Heterologous expression of AgURA9 in URA9 Dihydroorotate dehydrogenase engineered S. cerevisiae enabled the accumulation and excretion of orotic acid (~0.5 g/L). This study demon- strates the potential of A. gossypi for the valorization of crude glycerol to orotic acid and discloses the molecular determinants for its biosynthesis in fungi. 1. Introduction it is a key intermediate of the de novo pyrimidine biosynthesis, it is used as a precursor of nucleotides and pyrimidine-derived compounds (Car- Orotic acid is an intermediate of the de novo biosynthetic pathway of valho et al., 2016). pyrimidine ribonucleotides that plays an important role as a nutraceu- Several bacteria have been reported to accumulate orotic acid and its tical. It was firstly isolated from cow's milk at the beginning of the last biotechnological production has been explored with pyrimidine auxo- century (1905) (Takayama and Furuya, 1989) and designated at the trophs of the bacterium Corynebacterium glutamicum (Takayama and time as vitamin B13. However, as its synthesis occurs not only in mi- Furuya, 1989; Takayama and Matsunaga, 1991). In these prokaryotes, croorganisms but also in humans, this classification was abandoned blockage of the pyrimidine biosynthesis downstream the DHOD, (Takayama and Furuya, 1989; Wishart et al., 2018b). Orotic acid is a generally at the orotidine 5'-phosphate decarboxylase level, is a minor constituent of the diet that is mainly found in dairy products and requiring factor for their orotic acid-producing phenotype. However, some vegetables (such as carrots and beets). The commercial interest in when biotechnological important fungi are inspected, additional un- this chemical relies on the use of its salt, orotate. Orotate is the conju- known factors appear to be involved in this phenotype. For instance, gated base of orotic acid and, for a matter of simplicity, independently of Scura3 uracil-auxotrophs of the model yeast Saccharomyces cerevisiae its state, it will be mentioned as orotic acid (Carvalho et al., 2016). (Fig. 1) do not display orotic acid accumulation and excretion (Nezu and Orotic acid is used in combination with minerals such as magnesium, Shimokawa, 2004). On the other hand, the equivalent mutant of the pre- calcium, and lithium, acting as a carrier to improve their transport into whole genome duplication (pre-WGD) yeast Kluyveromyces lactis cells (Wishart et al., 2018a). In general, these formulations are widely (Klura34) produces orotic acid in standard yeast extract-peptone- appreciated as supplements for athletes and common people but are also glucose (YPD) media (Carvalho et al., 2016). In this work, the deletion valuable in clinical contexts. For instance, magnesium orotate has been of the mitochondrial DHOD (EC 1.3.5.2) encoded by KIURA9, which is successfully used as adjuvant therapy in the treatment of severe heart lacking in S. cerevisiae, was shown to be detrimental to orotic acid failure (Stepura and Martynow, 2009), while lithium orotate has bene- production. Conversely, deletion of the KlURAl gene encoding the ficial effects for the mental health, being clinically used to reduce the cytosolic DHOD (EC 1.3.98.1), which is the only DHOD present in symptoms of bipolar disorder (Lakhan and Vieira, 2008). In addition, as S. cerevisiae, did not affect orotic acid production (Carvalho et al., 2016). * Corresponding author at: CEB - Centre of Biological Engineering, University of Minho, 4710-057 Braga, Portugal; LABBELS - Associate Laboratory, Braga, Guimaraes, Portugal. E-mail address: luciliad@deb.uminho.pt (L. Domingues). https://doi.org/10.1016/j.biteb.2022.100992 Received 15 November 2021; Received in revised form 20 February 2022; Accepted 21 February 2022 Available online 25 February 2022 2589-014X/? 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND licer .org/licenses/by nc-nd/4.0/). R. Silva et al. Bioresource Technology Reports 17 (2022) 100992 L-glutamine DHOD, encoded by AgURA9 (Fig. 1). This fact suggests that an orotic acid-producing phenotype can be displayed by A. gossypi. This could AgURA2 cURA2 lead to the biotechnological exploration of the Agura3 pyrimidine auxotroph of this filamentous fungus (Aguiar et al., 2014) for orotic acid Carbamoyl phosphate production and give experimental evidence of the factors involved in orotic acid production in Saccharomycetales. Moreover, A. gossypi AgURA2 ScURA2 presents a good native ability to grow in glycerol (Ribeiro et al., 2012), a capacity that was recently explored for the production of lipids (Diaz- N-carbamoyl-L-aspartate Fernandez et al., 2019). Glycerol is a by-product accumulated in several industrial processes, namely in biodiesel and bioethanol production processes (Klein et al., 2016; Luo et al., 2016). Biodiesel production had its golden period be- Dihydroorotic acid tween 2005 and 2015, where it grew at an annual rate of 23% (Naylor Pyrimidine Biosynthesis and Higgins, 2017). The latest data indicates that despite a slowdown, AgURA9 | ScURA1 mtDHOD √cytDHOD biodiesel production will stay steady, with an annual production until 2025 around 40,000-46,000 million L per annum even in an era of low oil price (Severo et al., 2019; IEA - International Energy Agency, 2020). H AgURA3 For 10 kg of biodiesel produced, 1 kg (~10%) of crude glycerol is accumulated (Luo et al., 2016). Thus, it is imperative to convert crude Ho →Orotidine-5'p X UMP o PRPP glycerol into higher-value products to improve the economic sustain- H ScURA3 D ability of the biodiesel industry and mitigate the environmental impacts Orotic acid of crude glycerol waste disposal (Luo et al., 2016; Naylor and Higgins, 2017). Fig. 1. Schematic representation of the de novo biosynthetic pathway of py- With this in mind, the production of orotic acid by the pyrimidine rimidines in A. gossypi and S. cerevisiae. Red × marks where the de novo py- auxotroph A. gossypi Agura3 (Aguiar et al., 2014; Silva et al., 2015) was rimidine biosynthetic pathway is blocked in the A. gossypi Agura3 auxotroph here first disclosed. Subsequently, the study pursued two confluent ob- (orotidine 5'-phosphate decarboxylase level). Dashed arrows indicate a multi- jectives: i) development of the potential of A. gossypi for the production step pathway. Relevant gene names are represented in green and with the Ag of orotic acid from glycerol, by improving the innate capacities of this prefix for A. gossypi and in blue and with the Sc prefix for S. cerevisiae.
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Acro- fungus through metabolic engineering and culture conditions optimi- nyms near the gene names represent the corresponding enzyme: mtDHOD, zation; i) understanding the genetic factors for orotic acid accumulation mitochondrial dihydroorotate dehydrogenase; cytDHOD, cytosolic dihydroor- and excretion in fungi, which are for long unknown (Nezu and Shimo- otate dehydrogenase; PRPP: phosphoribosyl pyrophosphate; UMP: uridine kawa, 2004) and may have impaired the development of biotechno- monophosphate. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) logical processes for the production of this commercially valuable chemical. For this, the pyrimidine biosynthesis pathway of S. cerevisiae was engineered at the DHOD level. Pyrimidine-requiring mutants from Neurospora crassa also display an orotic acid-producing phenotype (Mitchell et al., 1948). The genome of 2. Materials and methods this fungus encodes both a cytosolic (NCBI: XP_960964.2) and a mito- chondrial (NCBI: XP_961804.1) DHOD. Uracil auxotrophs from Candida albicans and Yarrowia lipolytica, whose genomes encode only a mito- 2.1.Strains chondrial DHOD, CaUra9p (NCBI: XP_723522.1) and YALI0D18920p The A. gossypistrains used and generated during this study are listed (NCBI: XP_503008.1), have been also reported to accumulate and in Table 1. The pyrimidine auxotroph studied A. gossypi Agura3 (Aguiar excrete orotic acid (Gojkovic et al., 2004; Nezu and Shimokawa, 2004; Swietalski et al., 2021). However, C. albicans only displayed this et al., 2014) was the core genetic background used. Stock cultures of these strains were kept as spores suspended in spore buffer containing phenotype when YPD was supplemented with acetate (Nezu and Shi- 200 g/L glycerol, 8 g/L NaCl, and 0.25% (v/v) Tween 20 and stored at mokawa, 2004). The presence of different DHODs in fungi is linked to -80 °℃. Spores were prepared as previously described in Silva et al. evolutionary steps towards anaerobiosis. The cytosolic DHOD (encoded (2019b). Yeast strains were maintained at 4 °C on agar plates. by URA1) was acquired by an ancestor of Saccharomyces by horizontal gene transfer from bacteria, which permitted these yeasts to start 2.2. Media and culture conditions for A. gossypi propagating in anaerobic conditions and to lose the mitochondrial/ eukaryotic DHOD encoding gene (URA9) (Gojkovic et al., 2004). A. gossypi is a pre-WGD member of the Saccharomycetaceae family, Ashbya full medium (AFM; 10 g/L yeast extract, 10 g/L tryptone, 1 g/L myo-inositol, and 20 g/L glucose) was the base medium formulation more closely related to S. cerevisiae and K. lactis than to other filamen- tous fungi (Gomes et al., 2014). This fungus is known for its native ca- used for investigating orotic acid production in A. gossypii. In alternative to glucose, synthetic or crude glycerol was also used at different con- pacity to overproduce riboflavin (vitamin B2), for which it is industrially centrations (AFM-glycerol). Additionally, some low-cost medium for- exploited for more than 25 years (Aguiar et al., 2015), and also for its ability to de novo biosynthesize other important chemicals such as fla- mulations were also tested, which contained complex nutrients and/or industrial wastes such as crude glycerol (CG), raw yeast extract (RYE; vours and fragrances (Birk et al., 2019; Silva et al., 2019a, 2021). In this Kelbert et al., 2015), corn steep liquor (CSL; Pereira et al., 2010) and filamentous fungus, unlike the purine biosynthetic pathway, which is strongly connected with the overproduction of riboflavin (Aguiar et al., sugarcane molasses (SM). CG was kindly provided by CVR-Centre for Waste Valorisation (Guimaraes, Portugal), and before use, it was pre- 2015), investigation on pyrimidine biosynthesis is limited. However, treated to eliminate soap and methanol, essentially as described else- A. gossypii presents some interesting singularities regarding the regula- where (Ruhal et al., 2011). CG was first diluted in distilled water (1:4 v/ tion of pyrimidine biosynthesis that deserve attention (Silva et al., v) to reduce the viscosity of the fluid. The pH of the mixture was then 2019b). For instance, the de novo pyrimidine biosynthesis pathway of adjusted to 3 with HCl (6 M) to convert soap into free fatty acids. The this fungus, in contrast with S. cerevisiae and similarly to K. lactis, N. crassa, C. albicans, and Y. lipolytica, owns a putative mitochondrial precipitate formed was separated from the mixture by centrifugation at 7000 rpm for 10 min. Next, the pH was adjusted to 12 with KOH (5 M) R. Silva et al. Bioresource Technology Reports 17 (2022) 100992 Table 1 AgURA2 (ACR263C; NCBI Reference Sequence: NM_209018.2) and The strains of A. gossypi and S. cerevisiae used in this work. AgURA9 (ACL035C; NCBI Reference Sequence: NM_208722.1), the Strains Relevant genotype Parental Reference transformation cassettes used to substitute the native promoter of the strain genes were constructed as follows: the loxP-KanMX-loxP selectable marker, conferring resistance to geneticin (G418), and the promoter A. gossypi ATCC NCBI: txid284811 Prof. P. 10895 Philippsen, sequence of the AgGPD gene was amplified by PCR using specific primers (University of (Section 1 of Supplementary data) from a vector described previously Basel) (Silva et al., 2019a). These primers were used to introduce recombino- A. gossypi Agura3 Agura3△ ATCC10895 Aguiar et al., genic flanks for the locus corresponding to regions starting upstream 50 2014 S.cerevisiae NCBI: txid889517 Nijkamp et al., bp from the start codon and downstream the ATG initiation codon. CENPK113-7D 2012 The overexpression modules were used to transform spores of S.cerevisiae MATa, Scura3-52 S. cerevisiae A. gossypi using the Cre-loxP system (Aguiar et al., 2014). The primary CENPK113-5D CENPK113- heterokaryotic transformants were selected on agar-solidified AFM 7D This work containing 250-300 μg/mL geneticin (G418). The selection of A. gossypii A. gossypii AFL067WpA:l0oxP- ATCC 10895 ATCC_AFL067W KanMX4-loxP-AgGPDp homokaryotic clones was performed through the germination of unin- A. gossypi Agura3A AFL067Wp:: Agura3 ucleated haploid spores obtained from the primary heterokaryotic Agura3_AFL067W loxP-KanMX4-loxP- transformants on agar-solidified AFM-G418. The correct genomic inte- (uG) AgGPDp gration of the cassette, as well as the homokaryotic genotype of each A. gossypi uGU2 Agura34 AFL067WpA: uG (kanmx-) loxP-AgGPDp clone, were confirmed by analytical PCR. For this, a pin-head of myce- AgURA2pA:loxP. lium from single colonies was suspended in 30 μL of extraction buffer KanMX4- loxP-AgGPDp (0.05 M carbonate buffer pH 6.9, 2% (w/v) PVP 40, 0.2% (w/v) BSA and A. gossypii uGU2.9 Agura34 AFL067WpA:: uGU2 0.05% (v/v) Tween 20) and incubated for 10 min at 95 °C. Afterwards, loxP-AgGPDp (kanmx-) the tubes were centrifuged at maximum speed. The supernatant was AgURA2pA:.loxP- AgGPDp AgURA9p,:: used as a template in the PCR reactions using the specific primers listed loxP-KanMX4-loxP- in Section 1 of Supplementary data. AgGPDp S.cerevisiae CENPK113-7D S. cerevisiae 2.4. Construction of integration cassettes, transformation and AgURA9 Scura3△::loxP- CENPK113- KanMX4-loxP-AgGPDp- characterization of engineered S. cerevisiae 7D AgURA9 S. cerevisiae CENPK113-7D S.cerevisiae For the overexpression of the gene AgURA9 (ACL035C; NCBI Refer- AgURA9_△ural Scura3:loxP AgURA9 ence Sequence: NM_208722.1) in the ScURA3 locus (YEL021W; Gen- KanMX4-loxP-AgGPDp- Bank: CM001526.1), the transformation cassette containing the loxP- AgURA9 Scura1△:: loxP-NatMX4-loxP KanMX-loxP selectable marker, conferring resistance to geneticin S.cerevisiae CEN.PK113-5D S. cerevisiae (G418), the promoter sequence of the AgGPD gene and the entire open 5D_△ural Scural△:loxP- CENPK113- reading frame (ORF) of the gene AgURA9 was used to substitute the NatMX4-loxP 5D entire ORF of ScURA3 plus 82 bp upstream the ATG initiation codon.
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This sequence was amplified by PCR using specific primers (Section 1 of and the suspension was filtrated through qualitative filter paper Supplementary data), containing recombinogenic flanks for the ScURA3 (Advantec) to remove suspended debris. Then, the pH of the filtrate was locus, from gDNA of the strain A. gossypii uGU2.9. For the deletion of the adjusted to 6.8-7.0. Finally, the methanol contained in the solution was gene ScURA1 (SCEN_K00200; NCBI Reference Sequence: CP046091.1), removed by evaporation during autoclaving and the concentration of the transformation cassette containing the loxP-NatMX-loxP selectable glycerol was quantified by high-performance liquid chromatography marker, conferring resistance to nourseothricin (clonNAT), was used to (HPLC). GLYcr was then added to medium formulations at a final con- substitute the entire ORF of ScURA1 plus 80 bp upstream the ATG centration equivalent to approximately 25 g/L glycerol. The origin and initiation codon. This sequence was amplified by PCR using specific preparation mode of the RYE and CSL are reported elsewhere (Kelbert primers (Section 1 of Supplementary data), containing recombinogenic et al., 2015; Pereira et al., 2010), respectively. SM was kindly provided flanks for the ScURA1 locus, from a vector of our lab stock containing the by RAR: Refinarias de Acucar Reunidas, S.A. (Porto, Portugal) and used corresponding selection marker (gRNA_pCfB2310-CAN1). at a final concentration of approximately 25 g/L sucrose. Whenever The protocol used for the transformation of yeast was the LiAC/SS indicated, CaCO3 (2 g/L) was used to buffer the medium. All the con- carrier DNA/PEG method (Gietz and Schiestl, 2007). Transformants stituents of each media were sterilized together by autoclaving. were selected on agar-solidified YPD (10 g/L yeast extract, 20 g/L As standard procedure, cultivations were performed in 250 mL shake-flasks peptone, 20 g/L glucose) containing 200 μg/mL geneticin (G418) or 100 with a working volume of 50 mL and carried out at 28 °C in an orbital μg/mL nourseothricin (clonNAT). The correct genomic integrations of shaker at 200 rpm. The inoculum was set to approximately 107 spores/L. the cassettes were confirmed by analytical PCR. For this, a small amount However, since different growth conditions and medium formulations of biomass was suspended in 15 μL of 20 mM NaOH and incubated for were tested, they are described in the “Results and discussion” section 15 min at 95 °C. Afterwards, the tubes were centrifuged at maximum and figures captions. Cell dry weight (CDW) was determined by filtra- speed and the supernatant was used as a template in the PCR reactions tion, collection of the mycelium into a pre-weighed dried tube and using the specific primers listed in Section 1 of Supplementary data. drying at 105 °C until constant weight (~24 h). YPD was the base medium formulation used for accessing orotic acid production in S. cerevisiae. Cultivations were performed in 250 mL shake-flasks with a working volume of 25 mL and carried out at 30 °C in 2.3. Construction of integration cassettes and transformation of an orbital shaker at 200 rpm. The inoculum was set to an initial OD600/ A. gossypii biomass of 0.1, made by an overnight grown pre-inoculum in the same conditions. DNA manipulations were made using standard molecular biology procedures (Domingues, 2017). For the overexpression of the genes AgAFL067W (AFL067W; NCBI Reference Sequence: NM_210835.2), R. Silva et al. Bioresource Technology Reports 17 (2022) 100992 2.5. Radial growth of A. gossypi strains in hyperosmotic stress conditions strain (data not shown). Thus, these results show that: (i) blockage of the de novo pyrimidine biosynthesis downstream the formation of orotic Agar-solidified AFM containing 1 M KCl and 30 mM glycerol were acid (e.g., deletion of AgURA3) leads to the accumulation and subse- inoculated with 10 μL of a suspension of spores (10? spores/mL) and quent excretion of this compound by A. gossypi; (i) when high amounts incubated at 30 °C for 7 days. The control condition consisted of agar- of intermediates of the pyrimidine salvage pathway (such as uridine) are solidified AFM. Colony radial growth was determined daily by present in the medium, this pathway is recruited and the metabolic flux measuring the diameter of colonies in 90 mm diameter Petri dishes in through the de novo biosynthesis is reduced or null (Silva et al., 2019b). tWo perpendicular directions, through two guidelines previously drawn on the lower outer face of the plates (Brancato and Golding, 1953). 3.2. A. gossypii AgURA9 is a determinant for orotic acid production Radial growth measurements were performed in biological duplicates. The biotechnological exploration of orotic acid production in fungi 2.6. Analytical methods has been limited due to two main factors: (i) only a few species are known to be able to accumulate and excrete orotic acid (Carvalho et al., The concentration of glucose, glycerol and sucrose in the supernatant 2016; Nezu and Shimokawa, 2004; Takayama and Furuya, 1989); (ii) of the culture samples was determined by HPLC using a BioRad Aminex the genetic determinants for this phenotype are poorly understood. In HPX-87H (300 × 7.8 mm) column at 60 °C and 0.005 M sulfuric acid as addition to K. lactis (Carvalho et al., 2016), N. crassa (Mitchell et al., eluent in a flow rate of 0.6 mL/min. The corresponding peaks were 1948), C. albicans (Nezu and Shimokawa, 2004) and Y. lipolytica detected using a Knauer-IR intelligent refractive index detector. Orotic (Swietalski et al., 2021), A. gossypii was here shown to be one of the acid was the chemical compound studied (PubChem CID: 967). Orotic fungal species whose pyrimidine auxotrophs display this phenotype. acid anhydrous (98%) from Acros Organics was used as a standard for K. lactis owns two putative DHODs: the cytosolic KIUra1p (EC 1.3.98.1; the UItra High Performance Liquid Chromatography (UHPLC). NCBI: XP_453064.1) and the mitochondrial KIUra9p (EC 1.3.5.2; NCBI: The orotic acid present in the supernatant of culture samples was XP_452611.1) (Carvalho et al., 2016; Gomes et al., 2014) (Fig. 1). The quantified with SHIMADZU Nexera X2 UHPLC chromatography. The N. crassa genome also encodes a cytosolic (NCBI: XP_960964.2) and a column used for separation was a BRISA LC2 C18 (250 mm × 4.6 mm, 5 mitochondrial (NCBI: XP_961804.1) DHOD. In turn, A. gossypii, μm particle size; from Teknokroma, Spain) maintained at room tem- C. albicans and Y. lipolytica only have the mitochondrial DHOD (EC perature. The column effluent was monitored at 280 nm using a SHI- 1.3.5.2): AgUra9p (NCBI: NP_983369.1) (Gomes et al., 2014), CaUra9p MADZU SPD-M20A diode array detector. The eluent used was 25 mM (NCBI: XP_723522.1) (Gojkovic et al., 2004) and YALI0D18920p (NCBI: K2HPO4/KH2PO4 (pH 7.0) at a flow rate of 0.5 mL/min during a total XP_503008.1) (Swietalski et al., 2021), respectively. S. cerevisiae, whose run of 40 min (Carvalho et al., 2016). Samples for orotic acid quantifi- uracil auxotrophs do not accumulate orotic acid, only owns the cytosolic cation were diluted with 500 mM NaOH when appropriate. DHOD (EC 1.3.98.1), ScUra1p (NCBI: NP_012706.1) (Nezu and Shimo- kawa, 2004). Carvalho et al. (2016) advanced the importance of the 2.7. Statistical analyses presence of the mitochondrial DHOD for the K. lactis orotic acid- producing phenotype. In their study, the deletion of the KIURA9 gene GraphPad Prism for IOS version 6.0 was used to carry out the sta- in the K. lactis Klura34 strain reduced orotic acid production by 3-fold, tistical analyses. Differences to a control strain were analysed by one- whereas the deletion of the KlURA1 gene did not affect orotic acid way ANOVA followed by Dunnett's or Tukey's multiple comparison production (Carvalho et al., 2016). Here, to assess if the presence of a test.
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Unless indicated otherwise, statistical significance was established mitochondrial DHOD would turn S. cerevisiae into an orotic acid pro- at p < 0.05 for the comparisons. ducer and thus demonstrate that, beyond the pyrimidine auxotrophy, the presence of this enzyme is determinant for orotic acid accumulation 3. Results and discussion and excretion, the pyrimidine biosynthesis pathway of this yeast was engineered with the A. gossypi AgURA9 gene. 3.1. A. gossypii Agura3 accumulates and excretes orotic acid to the From the prototrophic strain S. cerevisiae CENPK113-7D, an auxo- culturemedium trophic strain for pyrimidines was constructed, strain S. cerevisiae AgURA9, where the ScURA3 locus was substituted by an AgURA9 An initial assessment of orotic acid production by A. gossypi Agura3 expression cassette (Table 1; for details see Section 2.4). However, no in shake-flask cultivations revealed that this strain can produce orotic orotic acid was detected in the cultures of this new strain. Despite the acid in the range of g/L from both glucose and glycerol (Section 2 of presence of AgURA9, S. cerevisiae still maintained intact the native Supplementary data). This orotic acid is virtually all excreted to the cytosolic DHOD encoded by ScURA1. Therefore, it was hypothesized extracellular medium since no relevant differences were found between that the metabolic flux of the de novo pyrimidine biosynthesis would its concentration in the supernatant and total culture broth (lysed cells continue to be made preferentially by the native pathway (ie., via plus supernatant). Similar to what was previously observed with the ScUralp). Consequently, strain S. cerevisiae AgURA9_Aural was subse- yeast K. lactis (Carvalho et al., 2016), time-course analysis of orotic acid quently constructed by further deleting ScURA1 (Table 1). The rationale production by A. gossypi Agura3 showed production kinetics associated followed was that this modification would block the formation of orotic with growth, stabilizing at the stationary phase (Section 2 of Supple- acid by any native enzyme and would thus funnel its biosynthesis mentary data). through the action of AgURA9. With this modification, this new strain The titre of orotic acid produced by A. gossypi Agura3 in glucose accumulated and excreted orotic acid to the medium unlike any other (1.51 ± 0.04 g/L) was slightly higher than that obtained in glycerol S. cerevisiae strain tested (Table 2). (1.23 ± 0.04 g/L). The concentration of orotic acid stabilized after S. cerevisiae AgURA9_△ural was able to excrete 0.53 ± 0.17 g/L approximately 72 h of growth when glucose was already depleted from orotic acid, corresponding to a specific production of 0.21 ± 0.07 g/ the medium and 5.83 ± 0.58 g/L of glycerol remained in the culture. gCDw at 24 h. The absorption spectrum of the peak identified in this Biomass production was similar in glucose (5.52 ± 0.33 gcDw/L) and S. cerevisiae strain matches the spectrum of a pure orotic acid standard glycerol (5.73 ± 0.07 gcdw/L). As expected, orotic acid was not detected chromatogram (Section 3 of Supplementary data). This is the experi- in cultures of the wild strain A. gossypii ATCC 10895 (data not shown). mental evidence that the presence of a mitochondrial DHOD, encoded On the other hand, the addition of 5 mM uridine to AFM, which has been by URA9 genes, is a major factor for orotic acid accumulation and shown to rescue the growth of the A. gossypi Agura3 auxotroph (Silva excretion in fungi. With this in mind, other species encoding a native et al., 2015, 2019b), abolished the production of orotic acid by this mitochondrial DHOD (Gojkovic et al., 2004) will likely be candidates for 4 R. Silva et al. Bioresource Technology Reports 17 (2022) 100992 Table 2 Orotic acid production by engineered S. cerevisiae strains. Cultivations were carried out in YPD at 30 °C and 200 rpm using 250 mL shake-flasks with 10% working volume. Data represent average values ± standard deviations of biological duplicates at 24 h. S. cerevisiae strain AgURA9_△ural AgURA9 5D_△ural (ura-) CENPK113-5D (ura-) CENPK113-7D (WT) Orotic acid (g/L) 0.53 ± 0.17 n.d. n.d. n.d. n.d. Final CDW (g/L) 2.47 ± 0.00 2.15 + 0.33 2.97 + 0.26 2.86 + 0.57 2.80 + 1.16 n.d. - not detected. orotic acid production as well. Beyond those, other species may be engineered using as a basis the rationale used in this study to confer 2.0- S. cerevisiae an orotic acid-producing phenotype: i) blockage of the py- 50 rimidine de novo biosynthesis downstream the formation of orotic acid 1.5- (deletion of ScURA3); i) expression of a gene encoding a mitochondrial 40 DHOD (AgURA9); and i) deletion of the gene encoding the native lvc cytosolic DHOD (ScURA1). 30 cerol 1.0- 20 3.3. Improvement of glycerol consumption and hyperosmotic stress 0.5- C tolerance through AFL067W overexpression 10 -T The development of a microorganism as a cell factory requires the 0.00 optimization of its substrate consumption range, together with the 7296120144168192 0 2448 improvement of its robustness towards industrial conditions (Czajka Time (hours) et al., 2017; Nielsen and Keasling, 2016; Yadav et al., 2012). After +Agura3 Agura3_AFL067W confirming the production of orotic acid by A. gossypi Agura3, it was Agura3 (Gly) Agura3_AFL067W (Gly) interesting to note that the production levels from glycerol were com- parable to those obtained in glucose, even though glycerol is consumed Fig. 2. Orotic acid production and glycerol consumption by A. gossypii Agura3 at slower consumption rates. This demonstrates that this polyol, the and A. gossypi Agura3 _AFL067W in AFM-glycerol. A. gossypi Agura3 is repre- main by-product of the biodiesel industry, could be a suitable carbon sented by circles (O) and A. gossypii Agura3_AFL067W by squares (). Filled source for exploring orotic acid production with this filamentous fungus. symbols represent orotic acid production and empty symbols glycerol con- Glycerol is an important industrial by-product (Klein et al., 2016; Luo sumption. Strains were grown at 28 °C and 200 rpm. Data represent average et al., 2016) and A. gossypi can utilize this carbon source for biotech- values and standard deviations of biological duplicates. Where not seen, error nological purposes (Magalhaes et al., 2014; Diaz-Fernandez et al., bars were smaller than the symbols. The final CDW was 9.7 ± 1.5 gcdw/L for 2019). Therefore, to further explore orotic acid production from glycerol the strain Agura3 and 11.2 ± 1.3 gcpw/L for the strain Agura3_AFL067W. feedstock, a chassis strain with improved utilization of glycerol was firstly sought. stress conditions in S. cerevisiae (Holst et al., 2000; Yu et al., 2010b). In S. cerevisiae, ScGuplp was firstly identified as a glycerol trans- Therefore, to assess if the overexpression of AFL067W could improve the porter by Holst et al. (2000), who reported its role in the growth of this hyperosmotic stress tolerance, the growth of Agura3_AFL067W strain yeast from glycerol, as well as in cell recovery from hyperosmotic stress was monitored on agar-solidified AFM containing an osmotic stress when glycerol was present in the medium. Although other functions agent (1 M KCl) and 30 mM glycerol (Fig. 3). To determine if the effects have been associated with ScGUP1 beyond glycerol metabolism, over- on hyperosmotic stress tolerance were strain-dependent, AFL067W was expression of this gene was revealed to be an effective strategy to in- also overexpressed in the wild strain ATCC 10895 (ATCC_ AFL067W). crease glycerol consumption by S. cerevisiae (Jung et al., 201l; Yu et al. Fig. 3A shows that the overexpression of AFL067W improved the 2010a). A. gossypii owns a syntenic homolog of ScGUP1 - AFL067W. In radial growth of the strains at hyperosmotic stress conditions that previous work, AFL067W and ScGUP1 were overexpressed in A. gossypii completely abolished the growth of the parental strains (Agura3 and ATCC 10895 strain using an episomal multi-copy vector (Silva, 2014). ATCC 10895).
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