Transformation of Metals and Minerals by Microorganisms.
M. Fomina and Geoffrey M. Gadd. University of Dundee, Division of Environmental and Applied Biology, Biological Sciences Institute, Dundee, United Kingdom
Microorganisms are intimately involved in metal biogeochemistry with a variety of processes determining mobility, and bioavailability. The balance between mobilization and immobilization varies depending on the organisms involved, their environment and physico-chemical conditions. Metal mobilization can arise from leaching mechanisms, complexation by metabolites and siderophores, and methylation where this results in volatilization. Immobilization can result from sorption, transport and intracellular sequestration or precipitation as organic and inorganic compounds, e.g. oxalates (fungi) and sulfides. In addition, reduction of higher-valency species may effect mobilization, e.g Mn(IV) to Mn(II), or immobilization, e.g. Cr(VI) to Cr(III). Our work seeks to understand the mechanisms of microbial metal transformations and their environmental significance with particular reference to chemoorganotrophic transformations mediated by free-living and mycorrhizal fungi, and metal precipitation mediated by sulfate-reducing bacteria (SRB) under anaerobic conditions. In terrestrial environments, fungi serve as neglected but important geochemical agents. Fungi promote rock weathering and contribute to the dissolution of mineral aggregates in soil through excretion of H+, organic acids and other ligands, or through redox transformations of mineral constituents. We have found that the main mechanism of metal mobilization from insoluble metal minerals is a combination of acidification and ligand-promoted dissolution: if oxalic acid is produced the production of metal oxalates can occur. Fungi can therefore also play an active or passive role in mineral formation through precipitation of secondary minerals, e.g. oxalates, and through the nucleation of crystalline material onto cell walls that can result in the formation of biogenic micro-fabrics within mineral substrates. Such interactions between fungi and minerals are of importance to biogeochemical cycles including those of C, N, S and P. We have shown that fungi may play an important role in the transformation of micro-fabrics in limestone (CaCO3) and dolomite (CaMg(CO3)2) and have produced direct evidence of mineralized fungal filaments with secondary carbonates. Other experiments using laboratory microcosms showed that fungi can precipitate calcite (CaCO3) and whewellite (calcium oxalate monohydrate, CaC2O4.H2O). Other processes that can determine metal bioavailability are important microbially-catalyzed reactions of the natural sulfur cycle. Chemolithotrophic leaching by sulfur/sulfide-oxidizing bacteria can result in mobilization from polluted soil matrices, while sulfide production by SRB can result in precipitation of soluble metals as insoluble sulfides, with other redox transformations also being mediated by these organisms, e.g. Cr(VI) to Cr(III). We have found metals such as Cd, Co, Cr, Cu, Mn, Ni and Zn can be efficiently leached from contaminated soils, and removed from solution by SRB. In addition, SRB can reduce metalloid oxyanions such as selenite to elemental selenium. We have found that SRB, growing as a biofilm, can mediate formation of elemental sulfur in the presence of selenite. The indirect, enzymatically-mediated coprecipitation of sulfur and selenium is a generalised ability among SRB, arising from sulfide biogenesis, and can take place under low redox conditions and in the dark. This presentation will detail the above examples of metal-mineral transformations by microorganisms, and discuss their biogeochemical and applied relevance. For bioremediation, solubilization of metal contaminants provides a means of removal from soils, sediments, and solid industrial wastes. Alternatively, immobilization processes may enable metals to be transformed in situ and are particularly applicable to removing metals from aqueous solution.