Metallophilicity in hot acid: microbial-mineral interface of extreme thermoacidophile Metallosphaera sedula

Rare microbial-mineral interactions in extreme environments are a focus of our investigations. Metal oxidizing thermophiles represent a unique group of microorganisms, which can prosper in many different kinds of extreme environments using a broad range of energy sources inaccessible to other forms of life. The nature of the mineral–microbe interface, where electron and mass transfer processes arise, is a key element to understand how the transition of geochemistry to biochemistry occurs in extreme hot habitats.
The extreme thermoacidophile Metallosphaera sedula is a versatile energy scavenger that flourishes in hot acid conditions utilizing various metal-bearing minerals to run its respiratory electron transport chain. Here we report the extracellular and intracellular biomineralization of M. sedula, grown on tungsten ores and Martian regolith analogues as a result of biogeochemical interactions in between microbe and mineral phase. When given an access to these mineral materials, M. sedula releases metal ions into the solution due to its metal oxidizing metabolic activity. Relieved inorganic ions tend to accumulate on the surface of microbial cell, forming mineral phase precipitates on the S-layer. Employing high-resolution transmission electron microscopy and a comprehensive set of spectroscopy tools, we have achieved ultrastructural analysis of M. sedula and resolved metal-microbial interface down to the nanometre scale. When grown on tungsten minerals, M. sedula is characterized by tungsten-encrusted S-layer and intracellular tungsten-filled storage inclusions. The observed cellular accumulation of tungsten crystallites leads to the formation of lager deposits, which results in a metal encrusted cell surface of M. sedula. M. sedula mediated bioprocessing of tungsten ores provides a low energy and reagents-requiring alternative to hydrometallurgical or pyrometallurgical processes to break the tungsten-oxygen bond. In this connection, the further thorough molecular analysis of tungsten mineral-microbial interactions will enable this approach to be utilized in commercial operations.
M. sedula actively colonizes synthetic Martian regolith simulants as suggested by multi-labeled fluorescence in situ hybridization (MiL-FISH) analysis and performs biotransformation of these Mn- and Fe- bearing minerals. Our results show that M. sedula mediates oxidation of Mn(II)-bearing synthetic Martian soils and subsequent formation of Mn(IV) oxide minerals. By applying electron paramagnetic resonance (EPR) spectroscopy we further show specific biogenic spectral signatures on Martian regolith simulants left upon M. sedula that are distinct from abiogenic Mn oxides. These studies have potential astrobiological implications for the detection of extinct or/and extant life and especially emphasize the role of chemolithotrophs as geobiological and bioleaching agents, which promote biomineralization and metal solubilisation.