In principle, iron oxidation can fuel significant primary productivity and nutrient cycling in dark environments such as the deep sea. However, we have an extremely limited understanding of the ecology of iron-based ecosystems, and thus the linkages between iron oxidation, carbon cycling, and nitrate reduction. Here we investigate iron microbial mats from hydrothermal vents at Lōʻihi Seamount, Hawaiʻi, using genome-resolved metagenomics and metatranscriptomics to reconstruct potential microbial roles and interactions. Our results show that the aerobic iron-oxidizing Zetaproteobacteria are the primary producers, concentrated at the oxic mat surface. Their fixed carbon supports heterotrophs deeper in the mat, notably the second most abundant organism, Candidatus Ferristratum sp. (uncultivated gen. nov.) from the uncharacterized DTB120 phylum. Candidatus Ferristratum sp., described using nine high-quality metagenome-assembled genomes with similar distributions of genes, expressed nitrate reduction genes narGH and the iron oxidation gene cyc2 in situ and in response to Fe(II) in a shipboard incubation, suggesting it is an anaerobic nitrate-reducing iron oxidizer. Candidatus Ferristratum sp. lacks a full denitrification pathway, relying on Zetaproteobacteria to remove intermediates like nitrite. Thus, at Lōʻihi, anaerobic iron oxidizers coexist with and are dependent on aerobic iron oxidizers. In total, our work shows how key community members work together to connect iron oxidation with carbon and nitrogen cycling, thus driving the biogeochemistry of exported fluids.

原则上，铁氧化可以在深海等黑暗环境中促进显着的初级生产力和养分循环。然而，我们对铁基生态系统的生态学以及铁氧化、碳循环和硝酸盐还原之间的联系知之甚少。在这里，我们使用基因组解析的宏基因组学和宏转录组学来重建潜在的微生物作用和相互作用，研究来自夏威夷洛伊希海山热液喷口的铁微生物垫。我们的研究结果表明，好氧铁氧化 Zetaproteobacteria 是主要生产者，集中在氧化垫表面。它们的固定碳支持垫子深处的异养生物，特别是第二丰富的生物，Candidatus Ferristratumsp。（uncultivated gen. nov.）来自未鉴定的 DTB120 门。Candidatus Ferristratum sp.，使用九个具有相似基因分布的高质量宏基因组组装基因组进行描述，在船上孵化中原位表达硝酸盐还原基因narGH和铁氧化基因cyc2并响应 Fe(II)，表明它是厌氧硝酸盐还原铁氧化剂。铁线莲sp。缺乏完整的反硝化途径，依靠 Zetaproteobacteria 去除亚硝酸盐等中间体。因此，在 Lōʻihi，厌氧铁氧化剂与需氧铁氧化剂共存并依赖于好氧铁氧化剂。总的来说，我们的工作展示了关键社区成员如何共同努力将铁氧化与碳和氮循环联系起来，从而推动输出流体的生物地球化学。