Fermentative iron reduction by a psychrotolerant Clostridium-dominant consortium enriched from Antarctic penguin-impacted soils

Microbial iron cycling regulates nutrient availability and redox balance in global ecosystems, yet its pathways remain underexplored in ice-free Antarctic terrestrial ecosystems. This study reports the enrichment of a psychrotolerant microbial consortium from penguin-impacted soils on Beaufort Island, Antarctica, capable of reducing Fe(III) to Fe(II) at 4 °C via an anaerobic (likely fermentative) iron-reducing pathway. The consortium was dominated by Clostridium sensu stricto 13 and completely reduced 230 mg L-1 Fe(III) citrate within three months and drove the biogenic formation of magnetite (Fe3O4). Metagenomic binning yielded four high-quality Clostridium genomes harboring multiple hydrogenases and cold-shock proteins (csp), revealing genomic strategies for energy conservation and psychrotolerance. Hydrogen production was strongly suppressed in the presence of Fe(III) citrate, indicating an intimate coupling of fermentation-derived electron flow to Fe(III) reduction. Our findings reveal a previously unrecognized low-temperature iron reduction mechanism and highlight the ecological significance of anaerobic (likely fermentative) iron reducers in ornithogenic soils—microhabitats enriched in organic matter and metals by penguin guano. This work expands the known diversity of Fe(III)-reducing microorganisms, demonstrates their role in magnetite biomineralization under extreme conditions, and provides insights into microbial modulation of iron speciation in Antarctic ornithogenic soils. A psychrotolerant Clostridium-dominated consortium mediates fermentative Fe(III) reduction and magnetite formation at 4 °C in Antarctic ornithogenic soils, revealing a previously overlooked pathway in polar iron cycling.