The mechanisms, key organisms, and geochemical significance of biological low pH Mn(II) oxidation are largely unexplored. Here we investigated the structure of indigenous Mn(II)-oxidizing microbial communities in a secondary subsurface Mn oxide deposit influenced by acidic (pH 4.8) metal-rich groundwater in a former uranium mining area. Microbial diversity was highest in the Mn deposit compared to the adjacent soil layers, and included the majority of known Mn(II)-oxidizing bacteria (MOB) and two genera of known Mn(II)-oxidizing fungi (MOF). Electron X-ray microanalysis showed that romanechite (Ba,H2O)2(Mn(4+),Mn(3+))5O10) was conspicuously enriched in the deposit. Canonical correspondence analysis (CCA) revealed that certain fungal, bacterial, and archaeal groups were firmly associated with the autochthonous Mn oxides. Eight MOB within the Proteobacteria, Actinobacteria, and Bacteroidetes and one MOF strain belonging to Ascomycota were isolated at pH 5.5 or 7.2 from the acidic Mn deposit. Soil-groundwater microcosms had 2.5 times faster Mn(II) depletion in the Mn deposit compared to adjacent soil layers. No depletion was observed in the abiotic controls suggesting that biological contribution is the main driver for Mn(II) oxidation at low pH. The composition and species specificity of the native low pH Mn(II) oxidizers were highly adapted to in situ conditions and these organisms may play a central role in the fundamental biogeochemical processes (e.g., metal natural attenuation), occurring in the acidic, oligotrophic, and metalliferous subsoil ecosystem.
This study provides multiple lines of evidence to show that microbes are the main drivers of Mn(II) oxidation even at acidic pH, offering new insights into Mn biogeochemical cycling. A distinct, highly adapted microbial community inhabits acidic, oligotrophic Mn deposits and mediates biological Mn oxidation. These data highlight the importance of biological processes for Mn biogeochemical cycling and show the potential for new bioremediation strategies aimed at enhancing biological Mn oxidation in low pH environments for contaminant mitigation.