Abstract
The involvement of metals (both directly and indirectly) in microorganisms’ growth, metabolism, and differentiation are interdependent to the metal species and microbial environment as well. A variety of properties that exhibit the changes in metal species and mobility through the metal-to-microbe interaction, mineral transformation, and deterioration often follow certain mechanisms that are important to natural bio-geo-chemical cycles of metal-bearing resources like auriferous and radionuclide ores. This chapter is, therefore, devoted to the investigations of microbial interactions with gold and uranium in solid and aqueous systems. Microbes mediate gold and uranium solubilization from solid systems via excretion of various metabolites such as amino acids, cyanide, thiosulfate, and by redox transformations which this chapter explains in detail. Additionally, microbial capability to precipitate metal ions intra−/extracellular products is also discussed. Furthermore, the microbial genomic and biochemical responses addressing the toxic metal complexes from surrounding aquatic environment are also discussed.
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1 Microbial Interaction with Metals
Metals, metalloids, and minerals are essential to human existence. They are ubiquitous in the biosphere with a key role in infrastructure, transportation, and consumer goods to ensure the sustainable development goals (SDGs). In addition, metals are allocated in terrestrial and aquatic habitats because of the industrial revolution and landfill disposal of end-of-life (EoL) products (Srivastava et al. 2020). A direct/indirect involvement of metals in every aspect of microbial growth, its metabolism, and differentiation through surface interaction in a natural and synthetic environment can significantly alter their physiochemical states (Gadd 2010). Microorganisms are usually intimately associated with metals, and associated elements, wherein the activities can result in mobilization and/or, immobilization of metal ions depending upon the mechanism pathways and the microenvironment where the organism(s) are located (Gadd 2002). Some of the typical metal-to-microbe interactions are shown in Fig. 11.1. A variety of properties that exhibit the changes in metal species and mobility through the metal-to-microbe interaction, mineral transformation, and deterioration often follow certain mechanisms that are important to natural bio-geo-chemical cycles of metal-bearing resources like auriferous and radionuclide ores.
2 Microbial Interactions with Gold
Gold is precious and among one of the ten rarest elements of this planet. On average, 0.005 parts per million (ppm) of gold content in the solid material of Earth’s crust and a concentration range of 0.02 ~ 0.2 parts per billion (ppb) gold in natural waters has been identified. However, the nonuniform distribution of gold which often gets enriched in a mineralized zone to potentially form the economically viable deposits in terms of primary reserves, e.g., skarn type-, vein type-, and disseminated deposits (Boyle 1979). This deposition in primary minerals commonly takes place through the metal-rich hydrothermal fluids, which circulate in open pores of rock-veins and gets deposited in resultant of the consecutive cooling and/or heating effects. Microbes interact with gold from solid and aqueous systems in the following ways:
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(i)
Microbes mediate gold solubilization from solid systems and via excretion of a number of metabolites which can affect the solubilization and deposition of gold (e.g., amino acids, thiosulfate, and cyanide).
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(ii)
Direct genomic and biochemical responses that deal the gold complexes from the surrounding aquatic environment.
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(iii)
Precipitating gold’s intra−/extracellular products (e.g., EPS and sulfide minerals).
2.1 Microbial Interaction with Gold in Solid Systems
After interacting with metal-constituent bodies in the environment, microbes can act to: (i) binding the metal species which influences the cell surface; (ii) carrying microbes into the cell for producing various intercellular functions; and (iii) forming various metabolic products which can be used for chelating the metal ions. Furthermore, the oxidation of refractory gold-containing ores and removal of disrupting ore constituents is an act following either direct (physical) or indirect (metabolic) mechanisms or, a combination of both as well. The pre-treatment mechanism of microbial activities associated with gold bio-oxidation has been further clarified by as follows:
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(i)
The attached microbes onto mineral surface can oxidize the mineral bodies (usually sulfides) by releasing H2SO4.
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(ii)
The attached microbes oxidize Fe2+ ions to Fe3+ ions in order to mediate the liberation of metal from sulfide minerals.
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(iii)
The transfer of oxidized Fe3+ ions into bulk mediates the bio-oxidation reaction onto mineral surface in terms of iron liberation and simultaneously gold enrichment in the mineral particles.
There are microbially associated direct mechanisms that are enzyme mediated (oxidases and reductases), whereas indirect mechanisms often are associated with the metabolites (for example, carboxyl-based organic acids or, mineral (inorganic) acids) of the microorganisms (Dew et al. 1999). However, no strong evidence persists for a direct breaking of sulfides by microbial activities (Sand et al. 1995; Tributsch 2001; Watling 2006). The widely accepted mechanism can be understood by the thiosulfate or polysulfate pathways (Rawlings 2005; Srivastava et al. 2020).
After a microbial pre-treatment (usually termed as the bio-oxidation) step, gold leaching in a suitable lixiviant solution can be performed by either using chemical reagents or metabolic products. Figure 11.2 indicated various mechanisms of microbial metal interaction and biogenic lixiviant production.
Microbial mechanisms to solubilize gold from the auriferous material include oxidation followed by gold cyanidation with biogenic cyanide excreted by the HCN synthesis using cyanogenic microorganisms or synthesized by oxidative decarboxylation of glycine. The process leads to form dicyanoaurate complexes, i.e., Au(CN)2− (Rodgers and Knowles 1978; Faramarzi et al. 2004; Faramarzi and Brandl 2006; Habashi 1970) by following the reaction as below:
At a physiological (mild acidic to neutral range of) pH, the cyanide mainly remains in the gaseous form of HCN (pKa, 9.3), which is a highly toxic volatile substance (Faramarzi and Brandl 2006). But in alkaline pH range of more than 10.5, the cyanide remains dissociated as CN− ions in solubilized form. Therefore, the biogenic cyanide captured in a higher alkaline solution can improve gold solubilization by forming the [Au(CN)2−] complex (Faramarzi and Brandl 2006). An in vitro study conducted by Campbell et al. (2001) using the cyanide producing microorganism, Chromobacterium violaceum showed that the biofilm developed onto gold surface could solubilize all gold within 17 days of duration. A final concentration of 35 ppm gold and 14.4 ppm free cyanide was obtained in the leached solution. In another study performed using Pseudomonas plecoglossicida, Faramarzi and Brandl (2006) showed 69% Au leaching from the shredded sample of waste printed circuit boards, which took ~80 h of incubation to produce ~500 ppm Au(CN)2− complex.
Bio-cyanide synthesis and its excretion in soil are commonly observed through the microbial activities exhibited by the bacterium viz. Pseudomonas fluorescens, Chromobacterium violaceum, Pseudomonas chlororaphis subsp. aureofaciens, Pseudomonas plecoglossicida, Pseudomonas aeruginosa, Pseudomonas syringae, Pseudomonas putida, Priestia megaterium, archaea species such as Ferroplasma acidiphilum, and Ferroplasma acidarmanus that produce cyanide via the membrane-bound enzyme complex and HCN syntheses (Faramarzi and Brandl 2006). Notably, metabolic cyanide production is possible only for a shorter duration (of 2 ~ 4 days of early stationary phase) in the presence of glycine (Castric 1981; Kita et al. 2006) as a secondary metabolite independent from the growth phase (Castric 1975). Glycine (NH2CH2COOH) preliminary acts to be a precursor through an oxidative decarboxylation via the enzymatic synthesis of HCN, and remains associated with the cell membrane that represents the cyanogenic group. Further, the oxidative product of glycine forming imino acetic acid (H–C(NH)–COOH) followed by C–C bond splitting with an attendant second dehydrogenase reaction producing metabolic HCN and CO2 as depicted in Fig. 11.5 (Laville et al. 1998). To trap this volatile HCN, an alkaline trap is required to simultaneously build up the cyanide concentration therein the solution.
In this manner, glycine has been found to be a common metabolic precursor to progress the microbial cyanidation process (Knowles 1976; Rodgers and Knowles 1978). After 20 days of incubation duration, the highest glycine concentration in Tomakin Park Gold Mine soil microcosms has been detected (soil incubation; oxic or anoxic, unamend or amend with Au pellet- or cycloheximide in a 1:4 (w:v) aqueous slurry at 25 °C in the dark) (Reith and McPhail 2006). All these findings suggest that gold forming dicyanoaurate complex takes place through the solubilization of gold with amino acids.
In surficial and arid environments (at below 500 m of land surface), iron- and sulfur-oxidizing chemolithoautotrophic bacteria like Acidithiobacillus thiooxidans and Acidithiobacillus ferrooxidans and archaea. They can form biofilms on the surfaces of metal sulfides and obtain the required energy source by oxidizing the mineral through a number of metabolic pathways. For example, the sulfur oxidase pathway (Sox) and the reverse Dsr pathways are good examples (Nordstrom and Southam 1997; Friedrich et al. 2005; Southam and Saunders 2005). The biofilms altogether provide the reaction spaces for sulfide oxidation at interface, biogenic sulfuric acid for hydrolysis of proton ions and keep Fe3+ in its oxidized form and reactive state as well (Sand et al. 1995; Rawlings 2005; Mielke et al. 2003). Subsequently, a higher ferric and proton ions’ concentration actively attacks the valence bonds of sulfides to degrade through an intermediate product forming thiosulfate (Sand et al. 1995). Similarly, the oxidation of sulfidic minerals can also release the companion metals into the solution (Southam and Saunders 2005):
During that course, a few sulfur and iron oxidizers as Thiobacillus thioparus and A. ferrooxidans also excrete thiosulfate. Further, in the presence of oxygen, the oxidation of gold through complexation with thiosulfate takes place as follows (Aylmore and Muir 2001):
The metabolic production of thiosulfate can also be performed by some alternative procedures that involve different microbial groups which can stimulate gold dissolution. Sulfate reducing bacteria, commonly found in acid sulfate soils (in anoxic, metal-rich, sulfate-containing sites) can produce thiosulfate while sulfite is reduced by H2 and formate (Fitz and Cypionka 1990). The gold dissolution mechanism involving heterotrophic microorganisms (i.e., Pseudomonas fluorescens, Bacillus subtilis, Paenibacillus alvei, Serratia liquefaciens, and Brevibacillus nitrificans) have been underpinned by previous studies, where under an in vitro condition, approximately 35 ppm of gold was solubilized by forming the complexes with metabolic amino acid (Lyalikova and Mockeicheva 1969; Korobushkina et al. 1974, 1976; Boyle 1979; Korobushkina et al. 1983). An assessment of DNA fingerprinting and metabolic function of the microorganism community (during the incubation period) along with gold and amino acid analyses, a change in bacterial community has been observed by Reith and McPhail (2006). Some of the bacteria such as Streptomyces fradiae can produce thiosulfate in resultant to sulfur metabolization from cysteine and further assist to gold solubilization (Kunert and Stransky 1988).
2.2 Microbial Interaction with Gold in Aqueous Systems
The presence of gold in microbial system is very toxic to the microorganisms even at a lower concentration of gold. For example, the minimal inhibitory concentration (MIC) in Escherichia coli has been observed to be 20 μM gold (i.e., about 4.0 ppm). Notably, it is also analyzed that the adverse toxicity toward microbial growth starts at about 1/1000 of MIC (Nies 1999). This produces acute toxicity to the microorganism when the concentration of gold from auriferous soil leaching can be up to 100 ppb (Reith and McPhail 2006), which can be much higher in the leach solutions obtained by dissolution of gold nuggets. Hence, the bacterial community developed in these zones is supposed to adapt to the detoxification of cell environment. In this context, many microbes have grown with a direct genomic and biochemical responses that deal the gold toxicity from various aquatic environments.
In scenarios of genomic and biochemical responses of bacterial species, it was observed that cytoplasmic transcriptional regulators (metal ion responsive) were playing an important role to regulate genes’ expression involved in homeostasis and efflux systems of metal ions (Silver 1996; Nies 1999; Hobman 2007). The MerR family of transcriptional activators (which is a kind of metal-sensing regulators) were observed in several bacterial communities and found to recognize and respond to a variety of metal ions in various aqueous environments (Silver 1996; Nies 1999; Hobman 2007). The specific regulation of transcription exhibited by gold complexes with E. coli. Was demonstrated by Stoyanov and Brown (2003). Wherein, the MerR-like transcriptional activator (i.e., CueR usually responds to Cu+) was observed to be activated by gold complexes which were promoted by the specific binding of gold to the cysteine residues 112 and 120 (Cys 112 and 120). On the other hand, a newly characterized transcriptional regulator (i.e., GolS) in a bacterium Salmonella enterica was found to share Cys 112 and 120 with other MerR family regulators but retained exclusive specificity to gold chloride, AuCl4− (Checa et al. 2007). The occurrence of a minimum two open reading frames whose expression was activated by GolS was disclosed. Wherein, (i) predicted transmembrane efflux ATPase (GolT) and (ii) predicted metallochaperone (GolB) suggested the resistant mechanism to gold complexes along with the organization of other metal resistances. It was also observed that an MerR regulator not only controls the production of itself but also the production of a P-type ATPase and a chaperone protein as well (Checa et al. 2007; Hobman 2007).
In the case of using A. thiooxidans, gold accumulation inside cells as the fine-grained colloids (of size 5 to 10 nm in diameter) and in the aqueous solution as crystalline gold (of several micrometers) can be achieved (Lengke and Southam 2005). Gold deposition on cells occurs through the concentration build-up along the cytoplasmic membrane, indicating that gold precipitation improves via electron transportation in association with energy generation. When gold thiosulfate complex (Au+) enters into cells, thiosulfate is consumed in metabolic process within the periplasmic space while gold is transported into cytoplasmic membrane via the chemiosmotic gradient in association with ATP hydrolysis. As gold is nondegradable, Au+ presumably forms either a new complex or gets reduced to zero-valance gold (Au0). However, Au0 can further re-oxidized to form a new complex that can be transported outside the cytoplasm. On the other side, in the presence of [Au(S2O3)23−] as sole energy source, the exchange between sulfur species and gold is allowed through an outer membrane pore. In this case, the reactions of sulfur occur in the periplasmic space instead of the cytoplasmic membrane wherein gold gets reduced. Thereafter, both (reduced gold and oxidized sulfur) are released through the outer membrane pores (Lengke and Southam 2005). The entire schematic for gold thiosulfate complex mechanism exhibited by A. thiooxidans is depicted in Fig. 11.3.
Similarly, many bacterial species were observed to precipitate gold intra−/extracellularly, and in their metabolic products. Lengke et al. (2006) demonstrated that Leptolyngbya boryana cells release membrane vesicles after interacting with a higher [Au(S2O3)23−] concentration. These vesicles connected with cell envelopes prevent the uptake of [Au(S2O3)23−] and keep away from sensitive cellular components. Further, such an interaction between [Au(S2O3)23−] complex and the vesicle components resulting to precipitate gold in its elemental form, most probably via the interactions with phosphorus, sulfur, or nitrogen ligands of vesicle components (Lengke et al. 2006). Thus, the compatible microorganism (viz. S. enterica, Cupriavidus metallidurans, and Leptolyngbya boryana) evolves effective mechanisms to detect gold toxicity and detoxification as well, allowing microbes to thrive in gold-rich surroundings.
It is also believed that bioaccumulation of gold by diverse microbial communities may also lead to biomineralization of secondary gold grains of different shapes. Southam and Beveridge (1994) showed the formation of octahedral gold (as Au0) using biogenic organic phosphate and sulfur compounds at a pH value of about 2.6. The potential of C. metallidurans to accumulate gold from an aquatic environment revealed through molecular profiling was indicated by Reith et al. Lengke and Southam (2005) observed the formation of octahedral gold by Leptolyngbya boryana at pH 1.9–2.2. The cyanobacteria, which are killed during the process, could potentially immobilize (intracellularly) > 100 μg mg−1 gold grains. The ability of sulfur redox bacteria in transformation of gold complexes to octahedral elemental gold indicates the formation of gold platelets due to the bacterial contribution in the supergene environment.
3 Microbial Interactions with Uranium
3.1 Microbial Interaction with Uranium in Solid Systems
Uranium exists as an admixture of U6+ and U4+ states in various natural uranium ores and mill tailings. U4+ is insoluble in sulfate-rich acidic solutions and usually requires to be oxidized to U4+ state to readily solubilize as uranyl ion (UO22+), commonly in a diluted solution of H2SO4. The dominant microbes commonly represented in these processes are Acidithiobacillus, Leptospirillum, Sulfobacillus, Alicyclobacillus, and Ferroplasma. Alicyclobacillus and Sulfobacillus spp. are observed in column leaching of the weathered low-grade uranium ore (Habashi 2020; Kaksonen et al. 2020). Mostly, microbes mobilize uranium either directly or indirectly depending on the valence of uranium, biogenic lixiviant, matrix composition, and contaminant solubility. The role of the microorganisms in terms of involving indirect mobilization is to oxidize zero-valance sulfur (S0) to sulfuric acid (H2SO4) and subsequently oxidize ferrous iron (Fe2+) to ferric species (Fe3+) after taking electrons (refer Eq. 11.2) as indicated in Fig. 11.4.
Biogenic ferric iron and sulfuric acid mobilize uranium as shown in Eqs. (11.6) and (11.7), respectively. These uranyl ions further interact with biogenic sulfate ions and form sulfate complexes.
This indicates a combined redoxolysis and acidolysis mechanism for metal mobilization. The bio-mobilization rate is majorly dependent on the initial conditions of solution pH, Fe2+ ions concentration, and its oxidation rate to forming Fe3+. For microbes, the bio-oxidation of ferrous iron (Fe2+) and regeneration of ferric iron (Fe3+) needs a sufficient availability of dissolved O2 and CO2. In addition to the ferric iron-mediated mobilization, direct oxidation of U4+ to U6+ by Acidithiobacillus ferrooxidans was also investigated by some researchers (DiSpirito et al. 1983) as shown in Eq.11.8.
Further, the hexavalent uranium species as uranyl ions dominate at a solution pH of 2.5 (refer Eq. 11.9); hence, the net oxidation reaction can be written as Eq. 11.10.
On the other side, the secondary mineral phase (like jarosite, MFe3(SO4)2.(OH)6) by precipitation of iron and sulfur species is inevitable. Wherein, a structural monovalent cation (usually Na+, K+, NH4+, H3O+) or a 0.5 equivalent of a divalent metal cation at ambient temperature and at a pH value below 3.5 reacts as Eq. (11.11).
Depending on the composition of monovalent cations in systems and concentration and in the absence of hydroxyl ions, the hydrolysis of Fe3+ ions at ambient temperature also leads to form ferric hydroxysulfate complexes, of which poorly crystallized schwertmannite is predominantly formed in a pH ranging between 2.0 and 3.5 (Bigham and Nordstrom 2000).
3.2 Microbial Interaction with Uranium in Aqueous Systems
Several key interactions of microbes-to-uranium ions that occur at low to neutral pH range facilitate metal binding with biogenic ligands onto the cell surfaces (Fowle et al. 2000; Fein et al. 1997), interaction with intracellular polyphosphates, chelation by extracellular polysaccharides (Merroun et al. 2006; Suzuki and Banfield 2004), binding to siderophores, and S-layer proteins (Merroun et al. 2005), precipitation of mineral phases (Jeong et al. 1997; Martinez et al. 2007) or, reduction to form insoluble tetra-valance U4+ (Lovley et al. 1991). A study performed by Cologgi et al. (2011) recently revealed that the conductive pili (anchored to cell envelope) of Geobacter sulfurreducens get involved to catalyze the extracellular reduction of U6+ to U4+. The expression of those pili improved the immobilization rate of uranium, preventing uranium permeation inside the periplasm, and also preserving the important functions of cell envelope and cell viability.
3.2.1 Microbial Interaction with Uranium by Redox Transformation; Bio-Reduction
Many physiologically active bacterial species can actively reduce soluble U6+ to insoluble U4+ to conserve energy for cellular growth or without any energy gain (Lovley and Phillips 1992; Lloyd and Renshaw 2005). In all these processes, the U6+ reduction was stimulated by injection of physiological electron donors such as acetate, lactate, or ethanol (Anderson et al. 2003; Haas et al. 2001; Volesky and Holan 1995).
The sulfate and iron-reducing bacterial species (Coates et al. 2001; Lloyd et al. 2005; Lovley and Phillips 1992; Suzuki et al. 2003), hyperthermophilic archaea (Kashefi and Lovley 2000), thermophiles (Kieft et al. 1999), fermentative bacteria (Francis et al. 1994; Suzuki and Suko 2006), acid-tolerant bacteria (Shelobolina et al. 2004), and myxobacteria (Wu et al. 2006) are well-known microorganisms applied to bio-reduction of uranium. In particular, Desulfovibrio spp., Geobacter spp., Shewanella spp., and Clostridium spp. are important microorganisms. Moreover, the responsible enzyme (tetraheme cytochrome c3) to bio-reduction of U6+ characterized in Desulfovibrio vulgaris exhibited in vitro U6+ reductase in combination with hydrogenase which served as its physiological electron donor (Payne et al. 2002). Similarly in another homologous system (triheme periplasmic cytochrome c7) of iron-reducing bacterium (G. sulfurreducens) eventually plays an important role in the reduction of U6+ to U4+ (Lloyd et al. 2003).
3.2.2 Microbial Interaction with Uranium by Redox Transformation; Bio-Oxidation
Microbially mediated bio-reduced U4+ can have probability of re-oxidation to U6+ by biotic or abiotic activities. Beller (2005) demonstrated the nitrate-dependent and anaerobic U4+ oxidation at neutral conditions by Thiobacillus denitrificans (the obligate chemolithoautotrophic bacterium). Senko et al. (2005) reported enzymatic oxidation of U4+ by nitrate-reducing Klebsiella sp. This enzymatic oxidation of U4+ was not linked to energy conservation which was imperative to the cell growth (Finneran et al. 2002; Beller 2005; Senko et al. 2002) albeit coupled with nitrate reduction which is a commonly existing contaminant at uranium sites (Riley et al. 1992). Similar was also observed by Finneran et al. (2002) with nitrate grown pure cultures of Geobacter metallireducens.
Furthermore, the presence of siderophores, humic substances, and biogenic (bi)-carbonates are suggested to stimulate uraninite oxidation by the formation of highly stable U4+ complexes (Frazier et al. 2005; Gorman-Lewis et al. 2005). Wan et al. (2005) reported that even under reducing conditions, the reduced uranium can be re-oxidized from U4+ to U6+ that too in the presence of microorganisms that can effectively reduce the uranium. They observed that the carbonate accumulations due to microbial respiration lead to stabilizing the carbonato-U6+ species, thus, increasing the thermodynamic feasibility of U4+ oxidation. The residual Fe3+ and possibly Mn4+, as co-existing species, act like terminal electron acceptors to re-oxidation of U4+.
3.2.3 Microbial Interaction with Uranium by Complexation; Biosorption
The metabolism independent sorption is termed biosorption that encompasses both adsorption and absorption. Most of the studies on this subject have indicated that uranium biosorption is species specific and is adversely affected by physiological condition of microbial cell, solution pH, nature of liquid media, other dissolved or coexisting species, and charged groups on the cell surface (Lloyd and Macaskie 2002). It is considered that microbial cell surface is a highly dynamic interface. On that cell surface, the new cell wall material and extracellular layers are added, signals are transduced, proteins are inserted, adherence to solid substrata occurs, nutrients and metabolites are exchanged and flocculation or mobility are controlled (Lalonde et al. 2008).
Since microbial cell surface along with cell wall remains in direct contact with a uranium-containing aqueous system, the charged functional groups within the surface layers can interact with charged molecules or ions present in the external milieu. Consequently, the metal cations become charged to bound with cell surfaces. The structural differences between cell walls of two microbial groups namely the Gram-positive and Gram-negative bacteria (as per their color behavior with Gram stain) exhibit a large potential to bind the cationic and anionic species as well (Frankel and Bazylinski 2003). The cell surface of both bacterial groups is shown in Fig. 11.5.
For a Gram-positive bacterium, the cell wall consists of highly cross-linked polymer that forms a peptidoglycan layer (or say, murein sacculus) of 25 nm thickness with enriched carboxylic groups. The secondary polymeric chains (like teichoic acid) of 8–50 glycerol/ribitol molecules that are closely etherified by phosphate bridges, or teichuronic acid, extend the arsenal of negatively charged compounds like the PO43− and RCOO− groups (Frankel and Bazylinski 2003). Kelly et al. (2002) further showed that these two metal-binding groups are implicated in radionuclide coordination. On the other side, the Gram-negative bacterium cell wall consists of a thin peptidoglycan layer (of thickness 4 nm) that remains isolated from the external environment by the bi-layeric lipoprotein of the outer membrane. The outward extended lipopolysaccharides are holding in place to the outer membrane with lipophilic ends with the preferred centers to bind cationic species with the counter anionic groups of PO43− and RCOO− (Beveridge and Koval 1981). Ferris and Beveridge reported that in Escherichia coli K-12 the residual phosphoryl of the polar head of phospholipids and lipopolysaccharides in the outer membrane exhibited the most possible binding sites for the cationic metal species. Further investigations indicated that the phosphoryl groups in the core-lipid A region of the lipopolysaccharides are primarily involved in metal binding in Pseudomonas aeruginosa. The studies conducted by Haas et al. (2001) and Fein et al. (1997) revealed that the uranyl ion sorption is progressed through two separate adsorptions to form the surface adsorbed complexes as > COO–UO2+ and > PO4H–UO2(OH)2. Therefore, the PO43− containing surface sites (pKa ≈ 7.0), RCOO− containing surface sites (pKa < 4.27–4.37), OH− containing surface sites, and amine groups (pKa > 8) are supposed to do binding of radionuclide metal species.
Various surface structures of cell wall interact with metal cations. Their composition is majorly proteinaceous layers (e.g., S-layers) or polymeric carbohydrate (e.g., capsules) (Douglas and Beveridge 1998). The crystalline S-layer belongs to the outermost cell envelope components of numerous bacteria and archaea (Sára and Sleytr 2000). Mostly, their thickness of 5–15 nm is comprised of protein (or glycoprotein subunits) and their ability to provide a complete cover cell surface, during all stages of bacterial multiplication has been identified. S-layers may also possess pores of identical morphology and size ranging between 2 and 6 nm (Beveridge 1994). These proteins may act like molecular sieving to trap ions or protect the cells against environmental adversities of metal toxicity of radionuclides metal (Sleytr et al. 1996; Sleytr 1997). Saturation of the S-layer with radionuclides like uranium or toxic metals may lead to denaturation of its surface lattice by replacing it with the freshly synthesized proteins (Merroun et al. 2005). These proteins possess a large number of carboxyl and phosphate groups, which can be involved in uranium complexation (Merroun et al. 2005; Sleytr 1997; Pietzsch et al. 1999).
Microbial cells able to generate macromolecules that become positioned outside the cell walls are known as extracellular polymeric substances (EPS). An EPS is a metabolic product albeit it may be a resultant from organic matter of the effluents by hydrolysis or other cell activities (Wingender et al. 1999) that actively serves to protect the cells from the external adversities (Comte et al. 2008). Although they have complex composition but majorly consist of polysaccharides, humic substances, proteins, nucleic acids, uronic acids, and lipids containing ionizable functional groups like PO43−, RCOO−, and OH− to provide the potential binding sites for metals’ sequestration (Wingender et al. 1999; Lawson et al. 1984).
The EPS of some isolated microbial species of diverse streams (like uranium mill tailings, uranium mining wastes, and groundwater repositories), exhibited high ability for uranium accumulation. The structural observations of uranium-complexed bacterial EPS exhibited similarity with U/fructose phosphate complexes (Koban et al. 2004) indicating the importance of organic phosphate present in EPS to coordination with metal species.
3.2.4 Microbial Interaction with Uranium by Complexation; Precipitation
The microbial activities can potentially lead to precipitation of metal ions including the radionuclides as their salts in carbonate, phosphate, and hydroxide form at different pH of solutions (Van Roy et al. 1997). Additionally, metals can be precipitated by contacting with biogenic ligands like phosphate, sulfide, and oxalate (Lovley et al. 1991, Xu et al. 1999). Microbial catalyzed biomineralization process forming the rock-carbonates is an important one particular to capture the atmospheric CO2 (Braissant et al. 2002; Ehrlich 2002; Riding 2000). The processes have further a vital role in ornamental stone conservation (Rodriguez-Navarro et al. 2003), bio-geo-chemical cycling of elements (Banfield 1997, Ehrlich 2002), and metal-contaminated groundwater bioremediation (Mitchell and Ferris 2005).
The microbial-induced precipitation of uranium as phosphate salt forming the mineral phases of H-autunite and autunite/meta-autunite at the pH range between 4.5 and 7.0 is reported. The process exhibits passive adsorption of uranium cations by the negatively charged extracellular polymeric substances of the cell walls and active secretion of PO43− groups through the phosphatase process (Renninger et al. 2004; Macaskie et al. 2000). Notably, the biomineralization process of uranium has been found to be independent of any geographic origin of the microorganisms rather strongly dependent on cell wall structure (i.e., Gram-positive and Gram-negative bacteria) at acidic and neutral conditions (Nedelkova et al. 2005; Jeong et al. 1997; Merroun et al. 2006). At physiological conditions of a pH value 6.9, HUO2PO4 and NaUO2PO4 phases are precipitated surrounding the cells of Citrobacter sp. (Lovley et al. 1991, Macaskie et al. 2000). At acidic conditions of pH 4 ~ 5, enzymatically assisted uranium precipitation by strains belonging to genera Bacillus and Rahnella are also revealed by Martinez et al. (2007) and Beazley et al. (2007). These bacteria precipitate uranium at a pH of about 4.5 by forming phosphate mineral phase of meta-autunite group. At a pH value of 2.0, adsorption of uranium on cell surface organic phosphate occurs instead of exhibiting the precipitation phenomenon. A similar pH-dependent speciation has been observed in bacterial strains of B. sphaericus JG-7B, Sphingomonas sp. SW366–3, etc.
3.2.5 Microbial Interaction with Uranium by Complexation; Intracellular Accumulation
Uranium does not exhibit essential biological functions. Hence, its transportation to microbial cells also differing the metabolism mainly because of an increased membrane permeability due to uranium toxicity (Suzuki and Banfield 2004). The microbial cells have numerous mechanistic routes to immobilize uranium after its intracellular accumulation (e.g., uranium chelation by polyphosphate bodies). Polyphosphate’s role in ATP substitution for sugar and adenylate kinases (as source energy) and metal chelation are established. TEM analysis indicated uranium accumulated in the cytoplasm that remains closer to the plasma membrane in Pseudomonas migulae CIP 105470. This uptake of uranium indicated the properties of bacterial outer cell membrane that allowed an inner cell diffusion of metal and their immobilization through the localized polyphosphate (Merroun and Selenska-Pobell 2008). Additionally, the U/polyphosphate accumulation in the form of needle-shape fibrils of various sizes alike the cytoplasm of natural isolates of Arthrobacter sp., Sphingomonas sp. S15–S1, and others are observed by Merroun et al. (2006). In the cells of Stenotrophomonas maltophilia JG-2, a strain isolated from mining waste, intracellular accumulated uranium, and its transport from the cell membranes to the cytoplasm was observed albeit the mechanistic route is yet to be disclosed.
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Acknowledgments
This work was supported by the Brain Pool Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (Grant No. 2021H1D3A2A01100016) and the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (Project No. 2020R1I1A1A01074249). The author, S. Ilyas would like to convey thanks to Prof. Christon J. Hurst for his valuable suggestions to shape this chapter.
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Ilyas, S., Kim, H., Srivastava, R.R. (2022). Microbial Interactions with Gold and Uranium. In: Hurst, C.J. (eds) Microbial Metabolism of Metals and Metalloids. Advances in Environmental Microbiology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-030-97185-4_11
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