COLLABORATIVE MICROBIAL FE REDOX CYCLING – AN ANCIENT ECOLOGICAL STRATEGY TO COLONIZE AN OXYGENATING WORLD?

Iron, the 4^th most abundant planetary element, is critically implicated in environmental contaminant behaviour and is a key interpretative marker for Earth’s geologic and atmospheric record. Fe^(III)-reducing bacteria (IRB) and Fe^(II)-oxidizing bacteria (IOB) significantly impact the transformations and geochemical cycling of Fe. However, these bacteria are thought to be differentially segregated to highly restricted oxygen and pH conditions, as O₂ inhibits IRB and, while metabolically required by many IOB, rapidly oxidizes Fe^(II) at pH>3. Thus, their collective impacts on Fe cycling have not been typically considered. We have identified the occurrence of cooperative Fe redox-cycling bacterial consortia from diverse oxygenated (O₂^Sat.=1-103%), circumneutral freshwaters associated with floc. Favourable microscale habitats are engineered through pelagic aggregate formation, enabling the macroscale expansion of aero-intolerant IRB and Fe^(II) requiring IOB into inhospitable open waters. Both environmental and experimental aggregate consortia constitute aero-intolerant IRB and IOB together with oxygen-consuming organotrophic species. Further, identified aggregate IOB and IRB here differ from those commonly identified from classical sediment/groundwater (IRB) and seep (IOB) habitats, indicating far greater environmental occurrence and diversity of Fe-metabolizing bacteria than currently considered. Further, experimental microcosm IRB-IOB aggregates generated assemblages of co-occurring reduced and oxidized Fe biominerals, not predicted by treatment oxygen levels, but also observed in environmental pelagic aggregate samples from freshwater systems with similar bulk O₂ levels. This discovery of a floc-hosted, microbial Fe redox wheel in oxygenated waters identifies an ancient cooperative strategy to colonize inhospitable environments; reframing the environmental range of microbial Fe biogeochemical impact and revealing unexpected Fe biominerals that may affect interpretation of Earth’s oxygen record.