Iron-oxidizing Zetaproteobacteria are well known to colonize deep-sea hydrothermal vent fields around the world where iron-rich fluids are discharged into oxic seawater. How inter-field and intra-field differences in geochemistry influence the diversity of Zetaproteobacteria, however, remains largely unknown. Here, we characterize Zetaproteobacteria phylogenomic diversity, metabolic potential, and morphologies of the iron oxides they form, with a focus on the recently discovered Fåvne vent field. Located along the Mohns ridge in the Arctic, this vent field is a unique study site with vent fluids containing both iron and hydrogen with thick iron microbial mats (Fe mats) covering porously venting high-temperature (227–267°C) black smoker chimneys. Through genome-resolved metagenomics, we demonstrate that Zetaproteobacteria, Ghiorsea spp., likely produce tubular iron oxide sheaths dominating the Fe mats at Fåvne, as observed via microscopy. With these structures, Ghiorsea may provide a surface area for members of other abundant taxa such as Campylobacterota, Gammaproteobacteria, and Alphaproteobacteria. Furthermore, Ghiorsea likely oxidizes both iron and hydrogen present in the fluids, with several Ghiorsea populations co-existing in the same niche. Homologs of Zetaproteobacteria Ni,Fe hydrogenases and iron oxidation gene cyc2 were found in genomes of other community members, suggesting exchange of these genes could have happened in similar environments. Our study provides new insights into Zetaproteobacteria in hydrothermal vents, their diversity, energy metabolism and niche formation. IMPORTANCE: Knowledge on microbial iron oxidation is important for understanding the cycling of iron, carbon, nitrogen, nutrients, and metals. The current study yields important insights into the niche sharing, diversification, and Fe(III) oxyhydroxide morphology of Ghiorsea , an iron- and hydrogen-oxidizing Zetaproteobacteria representative belonging to Zetaproteobacteria operational taxonomic unit 9. The study proposes that Ghiorsea exhibits a more extensive morphology of Fe(III) oxyhydroxide than previously observed. Overall, the results increase our knowledge on potential drivers of Zetaproteobacteria diversity in iron microbial mats and can eventually be used to develop strategies for the cultivation of sheath-forming Zetaproteobacteria.

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