Collaborative microbial Fe-redox cycling by pelagic floc bacteria across wide ranging oxygenated aquatic systems

• Discovery of a floc-hosted Fe-redox wheel mediated by IRB-IOB-aerobe consortia
• Identify a cooperative strategy where Fe-bacteria collaborate with O2-consuming species
• Experimentally demonstrate Fe-redox cycling under varying oxygen concentrations
• Fe-redox cycling consortia generate unexpected Fe-biomineral assemblages.
• Reframes the environmental range of microbial Fe biogeochemical impact

Fe(III)-reducing bacteria (IRB) and Fe(II)-oxidizing bacteria (IOB) significantly impact the transformations and geochemical cycling of Fe. As these bacteria are thought to be differentially segregated to specific environments reflecting oxygen and pH restrictions on their respective metabolisms, their impact on Fe biogeochemistry in pelagic environments has not been well investigated. Here we report the discovery of cooperative Fe-redox cycling bacterial consortia within flocs found in circumneutral freshwaters with a wide range of oxygenated conditions (O2Sat. = 1–103%). Favorable low-oxygen microscale conditions are engineered through consortial aggregate formation, enabling both IRB and IOB metabolisms within floc and thus the macroscale expansion of aero-intolerant IRB and IOB activity into presumed inhospitable oxic waters. Floc-associated IOB and IRB identified here (16S rDNA) differ from those commonly identified within sediment/groundwater (IRB) and seep (IOB) habitats, indicating a likely wider habitat distribution and genetic diversity of Fe-bacteria than currently considered. Further, both in situ floc communities and experimentally enriched floc consortial communities constitute aero-intolerant IRB and microaerobic IOB together with oxygen-consuming organotrophic species (i.e. aerobes). These results identify a collaborative Fe-cycling strategy through aggregate formation and cooperation with aerobic species that substantively extends the potential environmental range of IRB-IOB impact on Fe geochemical cycling. Supporting this hypothesis, experimental microcosm IRB-IOB-aerobe consortial aggregates generated unusual assemblages of co-occurring reduced and oxidized Fe minerals, not predicted by treatment oxygen levels, but also observed in environmental pelagic aggregate samples from systems with similar O2 levels. These findings have large implications for the use of Fe minerals as geochemical proxies to constrain the chemistry and infer the history of atmospheric O2 on early Earth, and question the utility of theoretical thermodynamic constraints alone as a guide to investigating and interpreting microbe–geosphere interactions.