Novel Antarctic chemolithotroph drives iron biomineralization.

Abstract

Background: Iron, the most abundant redox-active metal in the Earth's crust, is coupled to numerous biogeochemical cycles. However, the mechanisms of iron oxidation and the organisms involved remain incompletely understood. Banded iron formations (BIFs) are a major reservoir of iron ore in the Precambrian sedimentary record, yet the biological contribution to their genesis remains a subject of unresolved debate. While large-scale BIF deposition largely ceased after the Proterozoic, microbial activity in modern Holocene sediments under fluctuating redox conditions provides a unique opportunity to examine mechanisms reminiscent of ancient iron cycling. Here, we report the stratigraphic sequence of microbiome profiles recorded in laminated facies with iron-containing crystalline illite in the embayment sediments beneath the Larsen C Ice Shelf (LCIS) in Antarctica during the Holocene.

Results: LCIS sediments record microbial community shifts tightly coupled to environmental changes throughout the Holocene. Metagenomic analyses revealed three dominant microbial phases corresponding to geological facies boundaries. The open marine setting (phase A) showed higher taxonomic richness, whereas the sub-ice shelf sediments (phases B and C) were largely anoxic and characterized by diverse chemolithoautotrophic metabolisms. Keystone taxa including uncultured members of Thermodesulfovibrionia, as well as unique microbial communities and metabolisms, were evident in the aphotic, anoxic seawater; metagenomic analyses further revealed chemolithotrophy. The Thermodesulfovibrionia bacterium, visualized using fluorescence in situ hybridization and designated as "Candidatus Mariimomonas ferrooxydans", formed a novel clade in the phylum Nitrospirota. Metagenome-assembled genome analysis identified a putative outer-membrane Fe(II) oxidase, Cyc2, whose Fe(II)-oxidation activity was experimentally confirmed.

Conclusion: Our findings document the interaction between microbiome and environment, illustrating how LCIS sediments preserve a dynamic record of microbial community responses to environmental transitions. These results provide critical insights into microbial iron mineralization, echoing the biogeochemistry of the geologic past, particularly synglacial iron formation during the Neoproterozoic Snowball Earth. Video Abstract.