Bio-Reclamation of Strategic and Energy Critical Metals from Secondary Resources

Metals with an average crustal abundance of <0.01 ppm, which are high in supply shortage due to soaring demand, can, under the excessive environmental risk and <1% recycling rate of their production, be termed as ‘critical’ in a limited geo-boundary. A global trend to the green energy and low carbon technologies with geopolitical scenario is challenging for the sustainable reclamation of these metals from secondary resources. Among the available processes, bio-reclamation can be a sustainable technique for extracting and concentrating these metals. Therefore, in the present paper, the potential reclamation of critical metals (including rare earth elements, precious metals, and a common nuclear fuel element, uranium) via their interaction with microbe/s has been reviewed.


Introduction
The rare earth elements (REEs) and precious metals (PMs) have remained in metallurgical attraction for a long time.The tendency to occur together in nature, difficulties in their extraction and separation with specific area of applications has placed these metals in the list of critical metals.However, in the recent past, the definition of criticality is certainly not limited to the difficult metallurgy and abundance in the earth's crust (<0.01 ppm).In this technological era, the metals required in advanced materials and technologies for the transition towards a sustainable post-fossil society facing high supply risk due to the market complexities, lack of supply diversity, and geopolitical scenarios are termed as 'critical metals' [1].Metals in the list of criticality changes with region or country.The organizations like, the American Physical Society and Materials Research Society have termed 'energy-critical elements' (ECEs) as the elements necessary for emerging renewable energy whose unavailability could limit future research & development (R&D) or deployment of a technology [2].On the other hand, the European Union (EU) has accounted for the political and economic stability of producing countries along with their weak environmental performance to calculate the supply shortage of a particular metal [3].Hence, commonly a metal can be labelled 'critical' which is facing high shortage in supply, excessive environmental risk and be of significant economic importance under the availability of a limited geo-boundary.In that case, the criticality of metal can simply be presented as follows [4]: Criticality = Supply risk × Vulnerability = Likelihood of supply disruption × Economic Consequences (1) Notably, the availability of these metals largely influences the energy supply; country's economy, export business, job creation and geopolitical relation of two individual countries [5], hence can also be pronounced as 'strategic critical metals'.Figure 1 presents the list of such metals, including uranium (the major source of non-fossil, nuclear fuel) and gold (widely used for plating other conductor materials besides its economic importance in global trade) [2,3,6].In the scenario of a mineral deficit country like Korea, all the metals shown in Figure 1 can be on the country's critical-list.Most of these metals are currently being exploited through mining and metallurgy of their fast depleting primary ores in their respective region.Hence, the sustainable and cost-effective processing of these metals from the waste/end-of-life/scrap materials as their alternative sources is an absolute necessity of time.Moreover, metal contamination from waste materials is a major concern because: metals are non(bio)degradable substances which can transform to form their carcinogenic and toxic compounds to transfer across the trophic levels of food-chain and bioaccumulating in living organisms [7][8][9].Therefore, reclamation of critical metals from their alternative secondary resources can be a game-changer by overcoming the geo-boundary limitation, mitigating the supply risk and controlling the environmental damage by mining of their primary ores.
Notably, the availability of these metals largely influences the energy supply; country's economy, export business, job creation and geopolitical relation of two individual countries [5], hence can also be pronounced as 'strategic critical metals'.Figure 1 presents the list of such metals, including uranium (the major source of non-fossil, nuclear fuel) and gold (widely used for plating other conductor materials besides its economic importance in global trade) [2,3,6].In the scenario of a mineral deficit country like Korea, all the metals shown in Figure 1 can be on the country's criticallist.Most of these metals are currently being exploited through mining and metallurgy of their fast depleting primary ores in their respective region.Hence, the sustainable and cost-effective processing of these metals from the waste/end-of-life/scrap materials as their alternative sources is an absolute necessity of time.Moreover, metal contamination from waste materials is a major concern because: metals are non(bio)degradable substances which can transform to form their carcinogenic and toxic compounds to transfer across the trophic levels of food-chain and bioaccumulating in living organisms [7][8][9].Therefore, reclamation of critical metals from their alternative secondary resources can be a game-changer by overcoming the geo-boundary limitation, mitigating the supply risk and controlling the environmental damage by mining of their primary ores.A variety of reclamation routes have been explored and reviewed so far, including high calorific smelting, large chemical intensive hydrometallurgy, and energy intensive electrometallurgy [6,[10][11][12].However, the microbe-to-metal/material interactions have attracted renewed attention for a sustainable reclamation of metals from diversified materials [9].Bio-reclamation including bacterial leaching, control of redox reaction using bacterial treatment, metal adsorption and (impurity) removal by employing dead biomass as the potential sorbents can facilitate the recycling of various critical and valuable metals from diverse secondary materials [13,14].In this article, we have reviewed the literatures on bio-reclamation techniques (which includes microbial leaching, sorption, reduction and accumulation processes from non-primary sources) of critical metals; wherein the microbes-to-metal interaction, process sustainability and future challenge for the practical implementation of these processes has been discussed.

Potentially Important Microbes and Mechanism of Bio-Reclamation
From a bio-reclamation perspective, potentially important bacteria belong to the genus Acidiphilium, Acidithiobacillus, Sulfobacillus and Leptospirillum [15].The most vital bio-reclamating A variety of reclamation routes have been explored and reviewed so far, including high calorific smelting, large chemical intensive hydrometallurgy, and energy intensive electrometallurgy [6,[10][11][12].However, the microbe-to-metal/material interactions have attracted renewed attention for a sustainable reclamation of metals from diversified materials [9].Bio-reclamation including bacterial leaching, control of redox reaction using bacterial treatment, metal adsorption and (impurity) removal by employing dead biomass as the potential sorbents can facilitate the recycling of various critical and valuable metals from diverse secondary materials [13,14].In this article, we have reviewed the literatures on bio-reclamation techniques (which includes microbial leaching, sorption, reduction and accumulation processes from non-primary sources) of critical metals; wherein the microbes-to-metal interaction, process sustainability and future challenge for the practical implementation of these processes has been discussed.

Potentially Important Microbes and Mechanism of Bio-Reclamation
From a bio-reclamation perspective, potentially important bacteria belong to the genus Acidiphilium, Acidithiobacillus, Sulfobacillus and Leptospirillum [15].The most vital bio-reclamating Metals 2017, 7, 207 3 of 17 mesophiles belong to Acidithiobacillus, including sulfur and iron oxidizing Acidithiobacillus ferrooxidans and sulfur oxidizing Acidithiobacillus thiooxidans.Acidithiobacillus ferrooxidans supplied with a broad metabolic capacity was the first acidophilic bacteria which was used for the bio-metallurgical perspectives.The investigations at the putative boundary of mesophilic and moderately thermophilic conditions at a temperature of 45 • C, showed Acidithiobacillus caldus being a dominant sulfur oxidizer; whereas Leptospirillum dominates as iron oxidizer.The role of Fe-oxidizing, Leptospirillum ferrooxidans in bio-reclamation was lately recognized due to its poor enrichment from samples as compared with the Acidithiobacillus ferrooxidans.The prior importance of Leptospirillum ferrooxidans in bio-reclamation was due to its mix culture with Acidithiobacillus thiooxidans, which could oxidize pyrite on a faster rate than using Acidithiobacillus ferrooxidans alone.Such behavior was ascribed to: its high propensity to attach with materials to be leached, a high affinity for Fe 2+ and the low sensitivity to inhibition by Fe 3+ [16,17].
Association between the microbial activity and exothermic reaction caused in sulfur containing materials points out the relevance of thermophiles in bio-reclamation process.Moderately thermophilic iron and sulfur-oxidizing microbes were primarily cultured from the mining conditions or hot springs [18,19] and subsequently from the mine-sites of iron ore [20].Advancement in moderate thermophiles such as Sulfobacillus thermosulfidooxidans continues in recent mining operations, including refractory gold heaps undergoing biooxidation [21] and in bio-reclamation of electronic wastes [20,22].Nowadays extremely thermophilic microorganisms in acidic, sulfidic hot springs have been used for their exceptional ability to oxidize the hard-to-treat materials.These microorganisms have enlarged the bio-reclamation options in terms of temperature and metal tolerance capacity. Figure 2 depicted various modes of microbial-metal interactions for metal mobilization or immobilization.
Metals 2017, 7, 207 3 of 17 mesophiles belong to Acidithiobacillus, including sulfur and iron oxidizing Acidithiobacillus ferrooxidans and sulfur oxidizing Acidithiobacillus thiooxidans.Acidithiobacillus ferrooxidans supplied with a broad metabolic capacity was the first acidophilic bacteria which was used for the bio-metallurgical perspectives.The investigations at the putative boundary of mesophilic and moderately thermophilic conditions at a temperature of 45 °C, showed Acidithiobacillus caldus being a dominant sulfur oxidizer; whereas Leptospirillum dominates as iron oxidizer.The role of Feoxidizing, Leptospirillum ferrooxidans in bio-reclamation was lately recognized due to its poor enrichment from samples as compared with the Acidithiobacillus ferrooxidans.The prior importance of Leptospirillum ferrooxidans in bio-reclamation was due to its mix culture with Acidithiobacillus thiooxidans, which could oxidize pyrite on a faster rate than using Acidithiobacillus ferrooxidans alone.Such behavior was ascribed to: its high propensity to attach with materials to be leached, a high affinity for Fe 2+ and the low sensitivity to inhibition by Fe 3+ [16,17].Association between the microbial activity and exothermic reaction caused in sulfur containing materials points out the relevance of thermophiles in bio-reclamation process.Moderately thermophilic iron and sulfur-oxidizing microbes were primarily cultured from the mining conditions or hot springs [18,19] and subsequently from the mine-sites of iron ore [20].Advancement in moderate thermophiles such as Sulfobacillus thermosulfidooxidans continues in recent mining operations, including refractory gold heaps undergoing biooxidation [21] and in bio-reclamation of electronic wastes [20,22].Nowadays extremely thermophilic microorganisms in acidic, sulfidic hot springs have been used for their exceptional ability to oxidize the hard-to-treat materials.These microorganisms have enlarged the bio-reclamation options in terms of temperature and metal tolerance capacity. Figure 2 depicted various modes of microbial-metal interactions for metal mobilization or immobilization.Mostly acidophilic autotrophs generate ferric iron and sulfuric acid for biooxidation and enhanced dissolution of associated metals (M) or metal oxide (MO) by direct, indirect, thiosulfate and poly-sulfide mechanisms after additional supplementation of sulfur source as in Equations ( 2)-( 6) and Figure 3 [23,24].Other than the acidophilic autotrophs, some heterotrophic microbes (Pseudomonas fluorescens, Chromobacterium violaceum) and fungi (Penicillium simplicissimum, Aspergillus niger) have also shown potential in bio-reclamation of metals.Employing the heterotrophic microorganisms, metals are usually reclaimed by displacement with H + ions or formation of soluble metal species/chelates or the cyanidation with biogenic CN − [25,26].
M + H SO + 0.5O MSO + H O (4) Mostly acidophilic autotrophs generate ferric iron and sulfuric acid for biooxidation and enhanced dissolution of associated metals (M) or metal oxide (MO) by direct, indirect, thiosulfate and poly-sulfide mechanisms after additional supplementation of sulfur source as in Equations ( 2)-( 6) and Figure 3 [23,24].Other than the acidophilic autotrophs, some heterotrophic microbes (Pseudomonas fluorescens, Chromobacterium violaceum) and fungi (Penicillium simplicissimum, Aspergillus niger) have also shown potential in bio-reclamation of metals.Employing the heterotrophic microorganisms, metals are usually reclaimed by displacement with H + ions or formation of soluble metal species/chelates or the cyanidation with biogenic CN − [25,26]. (2)

Bio-Reclamation of Rare Earth Elements
The rare earth elements (REEs) are a combination of 17 chemically similar elements, comprised of 15 lanthanides (Z, 57 to 71), scandium (Z, 21) and yttrium (Z, 39), and exhibiting the characteristics of magnetism, fluorescence, and superconductivity.REEs are being used in rechargeable batteries, permanent magnets, catalysts, lamp phosphors, and biomedical applications.Based on the importance, they are sub-grouped as light (La to Sm) and heavy (Eu to Lu) REEs.The heavy REEs are technologically vital for the electronics, defence, and low-carbon renewable energy, and identified as the most critical raw materials with an aggregate demand of ~210,000 tonnes by 2015 [27].Figure 4 depicts the probable interaction of microbes with REEs and their subsequent leaching.However, exact understanding of the interactions is still not well documented despite a clear interest for developing biotechnology in clean recovery from the mine-sites.Consequently, only a few literatures have reported reclaiming REEs from secondary resources.A study involving the bio-reclamation of REEs from red mud describes the use of Penicillium tricolor at 2% (w/v) pulp density, could result in the maximum extraction of REEs and radioactive elements [28].The maximum extraction was achieved under a two-step bio-reclamation process using 10% pulp density.This study provides a basis for seeking the bio-reclamation of REEs from other secondary resources, including the electronic wastes.The bioleaching in presence and absence of Fe/S oxidizing bacteria (Acidithiobacillus ferrooxidans) has been studied for yttrium extraction from the waste cathode ray tube (CRT) glass [29].Notably, the effect of ferric ions can be understood by its ability to influence the redox potential of a bioleaching system [30].The results revealed a linear enhancement in Y extraction with time, which could reach

Bio-Reclamation of Rare Earth Elements
The rare earth elements (REEs) are a combination of 17 chemically similar elements, comprised of 15 lanthanides (Z, 57 to 71), scandium (Z, 21) and yttrium (Z, 39), and exhibiting the characteristics of magnetism, fluorescence, and superconductivity.REEs are being used in rechargeable batteries, permanent magnets, catalysts, lamp phosphors, and biomedical applications.Based on the importance, they are sub-grouped as light (La to Sm) and heavy (Eu to Lu) REEs.The heavy REEs are technologically vital for the electronics, defence, and low-carbon renewable energy, and identified as the most critical raw materials with an aggregate demand of ~210,000 tonnes by 2015 [27].Figure 4 depicts the probable interaction of microbes with REEs and their subsequent leaching.However, exact understanding of the interactions is still not well documented despite a clear interest for developing biotechnology in clean recovery from the mine-sites.Consequently, only a few literatures have reported reclaiming REEs from secondary resources.A study involving the bio-reclamation of REEs from red mud describes the use of Penicillium tricolor at 2% (w/v) pulp density, could result in the maximum extraction of REEs and radioactive elements [28].The maximum extraction was achieved under a two-step bio-reclamation process using 10% pulp density.This study provides a basis for seeking the bio-reclamation of REEs from other secondary resources, including the electronic wastes.

Bio-Reclamation of Rare Earth Elements
The rare earth elements (REEs) are a combination of 17 chemically similar elements, comprised of 15 lanthanides (Z, 57 to 71), scandium (Z, 21) and yttrium (Z, 39), and exhibiting the characteristics of magnetism, fluorescence, and superconductivity.REEs are being used in rechargeable batteries, permanent magnets, catalysts, lamp phosphors, and biomedical applications.Based on the importance, they are sub-grouped as light (La to Sm) and heavy (Eu to Lu) REEs.The heavy REEs are technologically vital for the electronics, defence, and low-carbon renewable energy, and identified as the most critical raw materials with an aggregate demand of ~210,000 tonnes by 2015 [27].Figure 4 depicts the probable interaction of microbes with REEs and their subsequent leaching.However, exact understanding of the interactions is still not well documented despite a clear interest for developing biotechnology in clean recovery from the mine-sites.Consequently, only a few literatures have reported reclaiming REEs from secondary resources.A study involving the bio-reclamation of REEs from red mud describes the use of Penicillium tricolor at 2% (w/v) pulp density, could result in the maximum extraction of REEs and radioactive elements [28].The maximum extraction was achieved under a two-step bio-reclamation process using 10% pulp density.This study provides a basis for seeking the bio-reclamation of REEs from other secondary resources, including the electronic wastes.The bioleaching in presence and absence of Fe/S oxidizing bacteria (Acidithiobacillus ferrooxidans) has been studied for yttrium extraction from the waste cathode ray tube (CRT) glass [29].Notably, the effect of ferric ions can be understood by its ability to influence the redox potential of a bioleaching system [30].The results revealed a linear enhancement in Y extraction with time, which could reach The bioleaching in presence and absence of Fe/S oxidizing bacteria (Acidithiobacillus ferrooxidans) has been studied for yttrium extraction from the waste cathode ray tube (CRT) glass [29].Notably, the effect of ferric ions can be understood by its ability to influence the redox potential of a bioleaching system [30].The results revealed a linear enhancement in Y extraction with time, which could reach the maximum yield of 40% and 70% after a 16 days of bioleaching in the presence and absence of ferric ions, respectively [29].The improved extraction of Y in the absence of ferric ions, attributed to the bacterial activity, was the highest with 3 × 10 8 cells/mL.A decrease in Y extraction with increase in pulp density indicated its negative effect on bacterial growth.The toxicity generated by the high metal content [31] in CRT (43% Zn and 23% Y) has been identified as the technological limit of this process.Hopfe et al. [32] recently reported the bioleaching of REEs from waste fluorescent powder (12.1% Y, 1.4% Ce, 0.8% Gd, 3.4% La, 0.7% Eu, 0.6% Tb) by using tea fungus Kombucha.The highest leaching yields were obtained in shake cultures either by using the entire Kombucha-consortium or with the supernatant of Kombucha, compared to the leaching yields of isolated Zygosaccharomyces lentus and Komagataeibacter hansenii.A primarily and effective leaching of Y and Eu indicated the red dye of Y 2 O 3 :Eu 3+ could be leached selectively.Approximately 60% and 68% Y was leached after 15 days of bioleaching in stationary and shaken mode, respectively; however, only 0.01% La could be released in both modes.Initially in both cases, a rapid decrease in pH was observed due to the in-situ generation of organic acids, mainly the acetic and gluconic acid.After a prolonged time (over 3 days) it slowed down due to the buffering effect of weak acids.Similar trends on pH profile with in-situ production of organic acids in the bioleaching of electronic waste, red mud, cracked catalysts and monazite ores have been observed in earlier studies [28,[33][34][35][36]. Reed et al. [36] reported that 60% of the organic acids, mainly gluconic acid, can be produced within the initial 24 h.Using the isolated microbial culture BH1, Acinetobacter calcoaceticus GSN8; BH24, Pseudomonas frederiksbergensis 37; and A1, Talaromyces purpureogenus for producing gluconic acid were however less effective in bioleaching of REE than the bacterium Gluconobacter oxydans.Abiotic control experiments showed that an increasing concentration of gluconic acid from 10 to 90 mM could increase the total leaching efficiency of REE from 24% to 45%.The supernatants of Gluconobacter B58, containing an average 12.5 mM gluconic acid were more effective for solubilizing the REE from a fluid catalytic cracking (FCC) catalyst than abiotically prepared solutions of 30 and 90 mM gluconic acid (Figure 5) [36].
Metals 2017, 7, 207 5 of 17 the maximum yield of 40% and 70% after a 16 days of bioleaching in the presence and absence of ferric ions, respectively [29].The improved extraction of Y in the absence of ferric ions, attributed to the bacterial activity, was the highest with 3 × 10 8 cells/mL.A decrease in Y extraction with increase in pulp density indicated its negative effect on bacterial growth.The toxicity generated by the high metal content [31] in CRT (43% Zn and 23% Y) has been identified as the technological limit of this process.Hopfe et al. [32] recently reported the bioleaching of REEs from waste fluorescent powder (12.1% Y, 1.4% Ce, 0.8% Gd, 3.4% La, 0.7% Eu, 0.6% Tb) by using tea fungus Kombucha.The highest leaching yields were obtained in shake cultures either by using the entire Kombucha-consortium or with the supernatant of Kombucha, compared to the leaching yields of isolated Zygosaccharomyces lentus and Komagataeibacter hansenii.A primarily and effective leaching of Y and Eu indicated the red dye of Y2O3:Eu 3+ could be leached selectively.Approximately 60% and 68% Y was leached after 15 days of bioleaching in stationary and shaken mode, respectively; however, only 0.01% La could be released in both modes.Initially in both cases, a rapid decrease in pH was observed due to the in-situ generation of organic acids, mainly the acetic and gluconic acid.After a prolonged time (over 3 days) it slowed down due to the buffering effect of weak acids.Similar trends on pH profile with in-situ production of organic acids in the bioleaching of electronic waste, red mud, cracked catalysts and monazite ores have been observed in earlier studies [28,[33][34][35][36]. Reed et al. [36] reported that 60% of the organic acids, mainly gluconic acid, can be produced within the initial 24 h.Using the isolated microbial culture BH1, Acinetobacter calcoaceticus GSN8; BH24, Pseudomonas frederiksbergensis 37; and A1, Talaromyces purpureogenus for producing gluconic acid were however less effective in bioleaching of REE than the bacterium Gluconobacter oxydans.Abiotic control experiments showed that an increasing concentration of gluconic acid from 10 to 90 mM could increase the total leaching efficiency of REE from 24% to 45%.The supernatants of Gluconobacter B58, containing an average 12.5 mM gluconic acid were more effective for solubilizing the REE from a fluid catalytic cracking (FCC) catalyst than abiotically prepared solutions of 30 and 90 mM gluconic acid (Figure 5) [36].The interactions of REEs with biogenic phosphates and specific transporter uptake are two recently disclosed processes having the potential to recover the REEs from aqueous waste streams.Firstly, the sorption on, or the encapsulation into the biogenic phosphate nano-minerals and the formation of REE-phosphate complexes were demonstrated using biofilms of Serratia strains [37,38].Using an extremophile, acidophilic methanotrophic Methylacidiphilum fumariolicum, Pol et al. [39] observed that the function of methanol dehydrogenase (MDH) in this bacterium strictly depends on the presence of REEs.The analysis of protein structure and alignment of amino acid sequences has revealed that the REE-binding motifs in this particular MDH were also present in other MDH enzymes.This largely indicated that many MDHs are lanthanide dependent.It was assumed that by modifying the structure of protein, the specificity and binding efficiency of protein towards the The interactions of REEs with biogenic phosphates and specific transporter uptake are two recently disclosed processes having the potential to recover the REEs from aqueous waste streams.Firstly, the sorption on, or the encapsulation into the biogenic phosphate nano-minerals and the formation of REE-phosphate complexes were demonstrated using biofilms of Serratia strains [37,38].Using an extremophile, acidophilic methanotrophic Methylacidiphilum fumariolicum, Pol et al. [39] observed Metals 2017, 7, 207 6 of 17 that the function of methanol dehydrogenase (MDH) in this bacterium strictly depends on the presence of REEs.The analysis of protein structure and alignment of amino acid sequences has revealed that the REE-binding motifs in this particular MDH were also present in other MDH enzymes.This largely indicated that many MDHs are lanthanide dependent.It was assumed that by modifying the structure of protein, the specificity and binding efficiency of protein towards the substrate could be improved [40,41].Henceforth, a REE-specific transporter to only recognize one particular REE could artificially evolve to concentrate REE in its cell.These approaches may be especially useful in recovering REEs from the aqueous waste streams.
Working with a mixed solution of La, Eu and Y, Texlier et al. [42] observed a preferential adsorption of europium ions onto the dead biomass of Pseudomonas aeruginosa.An investigation on the influential presence of metal cations viz.Al 3+ , Ca 2+ , Na + , K + and anionic salts viz.NO − 3 , SO 2− 4 , Cl − exhibited that the Al 3+ was more inhibitive cation for adsorbing REEs by Pseudomonas aeruginosa.Nevertheless, the presence of thorium or uranyl ions could greatly decrease lanthanum adsorption (at pH ≈ 1.0) by Mycobacterium smegmatis [43].Fungal biomasses of Rhizopusarrhizus, Saccharomyces cerevisiae, Aspergillus niger were also examined for biosorption of REEs from various solutions.It has been observed that the presence of glutamate, sulfate, phosphate, chloride, carbonate and ethylenediamine tetraacetate (EDTA) in sorbate solution with metal ratios up to 15, can greatly affect the sorption of lanthanum onto fungal biomass [44].Table 1 summarizes the R&D works for the biosorption of rare earth elements from various solutions.Using bioaccumulation technique, an acidophilic fungal strain Penidiella sp., isolated through enrichment procedures to accumulate Dy, revealed the occurrence of REEs' accumulation onto the cell surfaces.Except for Sc, the strains were found to be accumulated with Dy, Nd, Y, Eu, Pr, Yb, and Tb.The fungal cells, however, did not accumulate the base metal ions viz.Mn 2+ , Co 2+ , Cu 2+ , Al 3+ , Zn 3+ , Ga 3+ [53].The accumulation of lanthanum onto the surface of Pseudomonas aeruginosa inducing crystalline precipitation has been reported by Mullen et al. [48].Regarding the bio-remediation of rare earths, Ce 3+ and La 3+ are primarily required in the oxidation of methanol in microbes thriving on plant leaves via utilizing the methanol exudates [54].The presence of La 3+ supports the enrichment and isolation of methylotrophic bacteria, and uses single carbon compounds for energy acquisition to growth.A better knowledge of the microbial role of REEs and their acquisition by microbes will certainly lead to the development of the bioremediation strategies for a clean-up job of rare earth's mine-sites and their recovery from divergent waste streams.

Bio-Reclamation of Precious Metals
Commercial bioprocessing units use oxidizing conditions and iron or sulfur oxidizers (such as Acidithiobacillus ferrooxidancs, Acidithiobacillus thiooxidans, sulfobacillus thermosulfidooxidans) to generate ferric iron and sulfuric acid to accelerate metals dissolution via direct, indirect, thiosulfate and poly-sulfide mechanisms of biooxidation [24,55].After initial removal of heavy metal impurities using biooxidation, the precious metals are subjected to biogenic cyanidation as depicted in Figure 6.Precious metals include palladium, Pd; platinum, Pt; rhodium, Rh; iridium, Ir; osmium, Os; ruthenium, Ru and gold, Au can be extracted through biogenic cyanide leaching of wastes/secondary materials.Glycine is a direct precursor of biogenic cyanide that can be produced via the oxidative decarboxylation of glycine performed by the cyanogenic bacteria.The biogenic cyanidation leaching has the advantages to replace the chemical cyanidation in gold leaching under an alkaline condition, making metal's recovery much more efficient, reducing the reagents and transportation costs, and minimizing the environmental issues of chemical cyanidation.This stems from the fact that the cyanogenic bacteria yielded cyanide from glycine for short periods at the late exponential or early stationary phase of its growth.The CN − produced by Chromobacterium violaceum, a cyanogenic bacteria, is substantially used for gold recovery from the various waste streams, as with Equation ( 7) [26,55].
Metals 2017, 7, 207 7 of 17 single carbon compounds for energy acquisition to growth.A better knowledge of the microbial role of REEs and their acquisition by microbes will certainly lead to the development of the bioremediation strategies for a clean-up job of rare earth's mine-sites and their recovery from divergent waste streams.

Bio-Reclamation of Precious Metals
Commercial bioprocessing units use oxidizing conditions and iron or sulfur oxidizers (such as Acidithiobacillus ferrooxidancs, Acidithiobacillus thiooxidans, sulfobacillus thermosulfidooxidans) to generate ferric iron and sulfuric acid to accelerate metals dissolution via direct, indirect, thiosulfate and poly-sulfide mechanisms of biooxidation [24,55].After initial removal of heavy metal impurities using biooxidation, the precious metals are subjected to biogenic cyanidation as depicted in Figure 6.Precious metals include palladium, Pd; platinum, Pt; rhodium, Rh; iridium, Ir; osmium, Os; ruthenium, Ru and gold, Au can be extracted through biogenic cyanide leaching of wastes/secondary materials.Glycine is a direct precursor of biogenic cyanide that can be produced via the oxidative decarboxylation of glycine performed by the cyanogenic bacteria.The biogenic cyanidation leaching has the advantages to replace the chemical cyanidation in gold leaching under an alkaline condition, making metal's recovery much more efficient, reducing the reagents and transportation costs, and minimizing the environmental issues of chemical cyanidation.This stems from the fact that the cyanogenic bacteria yielded cyanide from glycine for short periods at the late exponential or early stationary phase of its growth.The CN − produced by Chromobacterium violaceum, a cyanogenic bacteria, is substantially used for gold recovery from the various waste streams, as with Equation ( 7) [26,55].In a preliminary study, Faramarzi et al. [26] reported the feasibility of gold recovery from waste printed circuit boards (PCBs) by Chromobacterium violaceum.The biogenic cyanidation of 5 mm × 10 mm sized PCBs, containing 10 mg of gold in each piece, could mobilize 15% gold as dicyanoaurate, Au CN in an alkaline solution.However, the microbe-mediated gold dissolution in presence of Chromobacterium violaceum with low metal mobilization did not show the formation of Au CN [56].Further studies done by Brandl and Faramarzi [57] showed a better performance of Chromobacterium violaceum for mobilizing 68.5% gold in 7 days from waste PCBs.In contrast, Pseudomonas fluorescens and Pseudomonas plecoglossicida formed lower amount of dicyanoaurate.The gold complex was more specifically unstable with Pseudomonas fluorescens due to the sorption of dicyanoaurate onto dead biomass or metal-cyanide's degradation [57].A substantial amount of copper dissolution from ewaste was also obtained due to its high content in the waste and a faster kinetics of cyanidation.Recovery of other precious metals viz.silver and platinum from the e-waste was not very promising because of their resistance and toxic effects on microorganisms.Using wild culture of In a preliminary study, Faramarzi et al. [26] reported the feasibility of gold recovery from waste printed circuit boards (PCBs) by Chromobacterium violaceum.The biogenic cyanidation of 5 mm × 10 mm sized PCBs, containing 10 mg of gold in each piece, could mobilize 15% gold as dicyanoaurate, Au(CN) − 2 in an alkaline solution.However, the microbe-mediated gold dissolution in presence of Chromobacterium violaceum with low metal mobilization did not show the formation of Au(CN) − 2 [56].Further studies done by Brandl and Faramarzi [57] showed a better performance of Chromobacterium violaceum for mobilizing 68.5% gold in 7 days from waste PCBs.In contrast, Pseudomonas fluorescens and Pseudomonas plecoglossicida formed lower amount of dicyanoaurate.The gold complex was more Metals 2017, 7, 207 8 of 17 specifically unstable with Pseudomonas fluorescens due to the sorption of dicyanoaurate onto dead biomass or metal-cyanide's degradation [57].A substantial amount of copper dissolution from e-waste was also obtained due to its high content in the waste and a faster kinetics of cyanidation.Recovery of other precious metals viz.silver and platinum from the e-waste was not very promising because of their resistance and toxic effects on microorganisms.Using wild culture of Chromobacterium violaceum, Chi et al. [58] obtained 13% gold and 37% copper in 8 days from mobile phone PCBs of content 0.025% Au and 34.5% Cu.They suggested an improved bio-reclamation of gold can be achieved by reducing the cyanide consumption from the copper containing material, and hence, proposed to substantially decrease copper content prior to undergo for biogenic cyanidation of precious metals.Recently, Tay et al. [59] could produce 70% more cyanide by metabolically-engineered strains of Chromobacterium violaceum, pTAC and pBAD in as compared to the cyanide generated by wild culture of Chromobacterium violaceum.Such a high amount of cyanide yielded more than twice the amount of gold leaching as well.Moreover, the cyanide production could be decoupled from quorum control by using the exogenous promoters.Modulations in proteome, resulting in a decreased cyanogenesis and an enhanced cyanolysis, may lead to a high amount of cyanide production.Moreover, the increase in cyanide production by the engineered strain does not change the protein levels of these enzymes, associated either directly or indirectly with the cyanolytic pathways.The study demonstrated that for the sustainable and effective bio-reclamation of precious metals from secondary sources, the genetically engineered microbes would be beneficial within their inherent capacity of cyanide production.
Other than the bacterial leaching of precious metals from secondary sources, bio-reduction of metal oxides to their metallic phase has also been studied in some cases.It has been observed that the microbial activity is helpful to generate an in situ reducing environment for metal ion reduction and the subsequent catalytic reactions as well [60][61][62].Lenz et al. [63] showed the important role of metal species in reduction potential and bacterial uptake efficiency.For example, bio-reduction of various palladium species has shown the influence of reduction potential for obtaining the reduced Pd 0 nanoparticles using microbes (viz.Geobacter), biofilms, and granular sludge [60,64].In a continuous recovery of palladium from granular sludge in an up-flow anaerobic bed reactor, Pat-Espadas et al. [61] showed the practical feasibility of the bio-recovery.Using Serratia sp.biofilms, developed on the polyurethane foam, palladium was recovered as biofilm-Pd 0 nanocatalyst from industrial wastes [65].The biorecovery of Pd(II) occurs in three concomitant steps: (i) biosorption with biomass via interactions with surface functional groups viz.carboxyl, phosphoryl, and amines; (ii) initial reduction to form Pd 0 nucleation sites; and (iii) the growth of Pd 0 on nuclei surfaces via the autocatalytic reduction of Pd(II) [66].The results were in line with microbial activity of enzymes such as formate dehydrogenase and hydrogenase used for the bioreduction of Pd(II) [67][68][69][70].Subsequent studies demonstrated that the metabolic activity of microorganisms is not essential to form the bio-Pd 0 [60,66].The applicability of metal-reducing bacteria like Shewanella alga, Desulfovibrio vulgaris in manufacturing the nanoparticles of gold and platinum has also been explored, but yet to be explored with waste streams [71].The uses of native and palladized Desulfovibrio desulfuricans in recovery of precious metals have shown selectivity for Au over Pt and Pd from an e-waste leachate [72].
Employing the biosorption technique for ruthenium recovery from a metal-plating effluent and process streams of acetic acid production by Rhodopseudomonas palustris and Corynebacterium glutamicum strains has given inspiring results.The experimental results showed that an acid pre-treatment of Rhodopseudomonas palustris cells could improve Ru-loading from 86 to 145 mg/g dry cells along with good selectivity over the co-existing metals Ni and Zn in effluent [73].Polyethyleimine (PEI)-coated Corynebacterium glutamicum fibers yielded 110 mg/g Ru-loading from an acetic acid solution.This result was a 16.5-fold higher efficiency than the commercially used ion-exchange resin [73], and 6.9-fold higher with the surface modified biomass blended with chitosan [74].The R&D works performed on reclamation via biosorption of precious metals from various secondary sources have been summarized in Tables 2-5.By analyzing the presented Tables, it can be stated that the use of specific microbes along Metals 2017, 7, 207 9 of 17 with their surface modification strategies may lead to the selective binding of these critical metals from their waste streams of complex nature.

Bio-Reclamation of Other Critical Metals
Due to the extensive uses of selenium and tellurium in electronics, semi-conductors and solar cells, their scarcity and uneven distribution, it necessitates the recovery methods of these metals from waste materials/solutions [94,95].The microorganism Pseudomonas mendocina can reduce tellurium from its higher oxidation states (+2, +4 and +6) to Te 0 [96,97].In an integrated process of recovery of critical metals from used CdTe solar cells, Rajwade and Paknikar [96] firstly employed fungal strains for selective removal of silver and cadmium from acidic solution.Then, Pseudomonas mendocina could lead to reductive precipitation of Te 0 .In a recent study, Te 0 was directly recovered using Pseudomonas sp.(strain EPR3) from the divergent sources, anode slime of copper, and TeO 2 /CdTe/Bi 2 Te 3 used material [97].The occurrence of several inter-related and coupled processes was observed during the bacterial speciation of tellurium.In the presence of microbial cultures, the soluble metal species diffuse across the cell membrane, inside which a reversible redox reaction simultaneously takes place with the methylation.As a result of this, an internal bacterial precipitation of Te 0 occurs.Some of the gaseous species of tellurium diffused out through the cell membrane which may volatize to atmosphere or reform the soluble tellurite by following the Challenger mechanism [97].However, the microbial volatilization of metals like Te and Se poses serious risks to the environment and human health.
Uranium from its resources including the waste materials is processed by chemical/bacterial leaching in sulfuric acid by following Equation (8) below.UO Extraction of uranium from various sources has been a long-term quest due to its strategic importance in defence, and civil nuclear industry.The anthropogenic activities from mining to generation of spent fuel have led to uranium contamination in the environment [98][99][100].Therefore, the microbial strategy has been explored not only to reclaim but also for remediation purposes.The interactions between uranium and bioorganism involve different mechanisms, certainly not limited to biosorption on the cell surface, bioprecipitation as hydrogen uranyl phosphate (HUO 2 PO 4 ), bioaccumulation in polyphosphate granules, and bioreduction as uraninite (UO 2 ).Bio precipitation of uranium as HUO 2 PO 4 from waste streams using bacterial phosphate has long been studied for hydrolytic release of inorganic phosphates [100].To improve the economy of bioprecipitation, Paterson-Beedle et al. [38] used phytic acid, a waste product of plants as the phosphate source in the system.Furthermore, the phosphatase activity of microbial cultures was improved by the overexpression of phosphatase through genetic engineering.The bacterial reduction of uranium from the +6 to +4 state is a potent method of bioremediation for in situ immobilization and remediation of subsurface environment [101].This approach is cost-effective compared to the pump and treat remediation; however, supply of electron donors, maintenance of proper redox environment and long durability of bio reduced uranium (+4) precipitates have been found to be challenging.The exploitation of 349 mg U/kg black shale using Acidithiobacillus ferrooxidans has been investigated by comparing the effect of inoculation and non-inoculation reactor [102].It was observed that the batch-type reactor inoculated with microbial cells exhibited a higher redox potential, lower pH and higher quantity of ferric ions than that which was observed for the non-inoculated reactor until 200 h.The condition facilitated by microbial activity could efficiently improve the bioleaching of uranium; however, with sufficient nutrients and Fe 3+ as energy source, the indigenous microorganisms in non-inoculated black shell could also be activated over time.The study revealed a scope of cost reduction by the means of lower consumption of Fe 2+ and nutrients in the system [102].
Rhenium, one of the energy-critical elements has a prime use in Pt-Re catalysts [103].A study on rhenium extraction from spent Pt-Re catalyst using Bacillus megaterium as a cyanogenic bacterium has been reported by Motaghed et al. [104].The response surface methodology was applied by keeping pulp density and initial glycine concentration as two main influential parameters for extracting the critical metals; however, it was found to be better only to extract the Re.After seven days of bioleaching under the optimal condition of 40 g/L pulp density and 12.8 g/L initial concentration of glycine, 98% Re could be leached with only 16% Pt in leach liquor.During the bioleaching, an increase in free cyanide concentration to 3.6 mg/L under the varied pH (6.7 to 9.0) and dissolved oxygen concentration (2 to 5 mg/L) clearly demonstrated the growth characteristics of Bacillus megaterium.A lower leachability of Pt can be attributed to its resistance to being mobilized using the cyanogenic microorganisms [26,105].Recovery of Re from a waste water employing biosorption technique has also been studied.Using the brown algae Laminaria japonica in its modified cross-link gel structure exhibited a maximum 97% sorption with the capacity 37.2 mg/g at pH 6.0 [106].The result showed a higher affinity for Re in comparison with the earlier used sorbents of persimmon and orange peel [107,108].This indicated the positive effect of H 2 SO 4 -modified structure on rhenium adsorption that was resultant of the increased surface area of the sorption sites on algae cell walls.

Prospects for the Bio-Reclamation of Critical Metals from Secondary Resources
The stringent regulations on environmental pollutions and constraints on practicing the current operations will create demand for new methodologies to recover the critical metals from waste streams, providing an ideal situation for bio-reclamation approaches.Notably, the particular microbe-to-REE interactions and leaching mechanism have hardly been focused upon and we are facing challenges as their bio-geo-chemistry is stable towards the redox transformations.For such a challenging task, a multidisciplinary approach of various research communities belonging microbiology, metallurgy, and chemistry to unfold the complexation of critical metals with biogenic lixiviants and/or their enrichment/separation using the bio-accumulation/sorption/reduction would be much needed.
Reclamation of critical metals by heterotrophic bioleaching is far less discussed, despite its distinctive potential.Heterotrophic bio-reclamation using indigenous fungal species could be feasible to recover REEs from solid wastes.Biogenic organic acids coupled with biogenic chelators could be efficiently employed to liberate the REEs from divergent wastes.Extensive uses of microorganisms in leaching of precious metals have been restricted by the limited exploitation of cyanogenic microbes only to Chromobacterium violaceum.Therefore, the construction of a metabolic engineered strain of related microbial cultures can produce more cyanide in lixiviant that may enhance the recovery by several fold compared to using the wild culture.Immobilization of bacterial cells on supports, like polyurethane foam and design of integrated-column operations can lead to efficient recovery of metals.The critical metals able to form insoluble phosphates can be amenable for recovery via the precipitation-crystallization route through the biogenic production of high phosphate ligands locally.Employing the biosorption technique, the microbial biomass and its constituents (viz.bacteria, yeast, fungi, algae, derived from activated sludge or fermentation waste, including fast growing microorganism crab shells and seaweeds) can be potential sorbent material for critical metals recovery.
Overall, the most important factor is the practical implementation of lab scale technology to the actual systems.Indeed, microbe-to-metal interactions have been efficiently employed in exploitation of primary ores, but are not sufficiently investigated to be commissioned for reclamation of strategic and energy critical metals from secondary sources.In an actual system, the conditions of waste streams like extreme acidic/alkaline pH, high amount of total dissolved solids, strong ionic strength, presence of organics and undesired toxic metals are the bottlenecks which can deviate the reclamation efficiency of critical metals, because most of the lab studies are performed under ideal conditions using synthetic solutions.Notably, critical/scarce metals in the waste solutions remain in trace amounts, sometimes as micro-sized colloids, and are sorbed onto suspended materials or as complex compound in solid wastes like alloys, scraps, metallurgical slags; hence, bio-reclamation should furthermore focus on "unfavorable" conditions and combination of metals that cannot be separated well by either the pyro or hydro(chemical) route of metallurgy.

Conclusions
Bio-reclamation of critical metals from the secondary/urban mine resources can be attractive in economic and technical terms.The microbial approach does not require high capital to invest, energy for smelting or electro-reduction; and a minimized generation of new waste compared to the conventional extraction route of REEs and other critical metals are major advantages which can mitigate their supply risk in a sustainable manner.However, the complex nature of secondary materials with a minor amount of critical metals compared to the other co-engineered metals is the most difficult challenge.Bioleaching of REEs from the urban mined sources is quite different than using the phosphate solubilizing bacteria in the case of primary ores, despite the organic acid producing microorganisms being useful to leach the REEs.In the case of precious metals like Au, Ag, Pt, and Pd, the biogenic cyanidation is the promising one.Reclaiming the precious metals of very low concentration from various waste stream solutions, biosorption and bioaccumulation techniques have been employed frequently to get the prominent recovery of critical metals.In some cases, like for Pd and Te, the bio-reduction has also been reported to directly recover the critical metals in nano-sized metallic form.Nevertheless, the reported literature on bio-reclamation critical metals belongs to only lab scale basic research; therefore, a lot of efforts are needed to get the real benefit of microbial strategy for treating the urban mined secondary materials.

Figure 1 .
Figure 1.Periodic table indicating the critical and scarce metals taken into this study [1-3].

Figure 1 .
Figure 1.Periodic table indicating the critical and scarce metals taken into this study [1-3].

Figure 2 .
Figure 2. A typical representation of various modes of bio-reclamation process.

Figure 2 .
Figure 2. A typical representation of various modes of bio-reclamation process.

Figure 3 .
Figure 3. Interaction of Acidithiobacillus ferrooxidans with metals on surface of source material [23].

Figure 4 .
Figure 4. Bio-reclamation of rare earth elements by interactions with heterotrophic microbes.

Figure 3 .
Figure 3. Interaction of Acidithiobacillus ferrooxidans with metals on surface of source material [23].

Figure 3 .
Figure 3. Interaction of Acidithiobacillus ferrooxidans with metals on surface of source material [23].

Figure 4 .
Figure 4. Bio-reclamation of rare earth elements by interactions with heterotrophic microbes.

Figure 4 .
Figure 4. Bio-reclamation of rare earth elements by interactions with heterotrophic microbes.

Figure 6 .
Figure 6.The production route of cyanide by microorganism with the subsequent use in cyanidation of precious metals (arrows are denoting the metabolic pathway of Chromobacterium violaceum).

Figure 6 .
Figure 6.The production route of cyanide by microorganism with the subsequent use in cyanidation of precious metals (arrows are denoting the metabolic pathway of Chromobacterium violaceum).

Table 1 .
A summary of various biosorption processes of rare earth elements (T = temperature; t = contact time; B.D. = biomass dosage).

Table 2 .
A summary for the biosorption studies of gold by dead biomass of algae (T = temperature; t = contact time; B.D. = biosorbent dosage).

Table 3 .
A summary of the biosorption studies of gold and silver by dead biomass of fungi and yeast (T = temperature, t = contact time, B.D. = biosorbent dosage).

Table 4 .
A summary of the biosorption studies of precious metals using protein biomass (T = temperature, t = contact time, B.D. = biosorbent dosage).

Table 5 .
A summary of the biosorption studies of precious metals using dead bacterial biomass (T = temperature, t = contact time, B.D. = biosorbent dosage).