Abstract
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.
Highlights
Supplementary information The online version of this article contains supplementary material, which is available to authorized users.Chemolithotrophy fuels primary production and nutrient cycling in dark environments (e.g., [1,2,3])
Metabolic predictions are largely based on isolate physiology studies [25, 26] and genomic potential [19, 20, 24] of the Zetaproteobacteria, while the functions of other, flanking members of the microbial community have largely been inferred from 16S rRNA gene taxonomy, which assumes metabolism is tied with taxonomic affiliation [8, 11, 18]
Our results reveal a fuller picture of the microbial ecology and geochemical cycling in iron microbial mats, including viral influences on dominant community members, nitrogen cycling by Zetaproteobacteria, and a role for a potential nitrate-reducing ironoxidizing Candidatus Ferristratum sp., from the uncharacterized DTB120 phylum
Summary
Metabolic predictions are largely based on isolate physiology studies [25, 26] and genomic potential [19, 20, 24] of the Zetaproteobacteria, while the functions of other, flanking members of the microbial community have largely been inferred from 16S rRNA gene taxonomy, which assumes metabolism is tied with taxonomic affiliation [8, 11, 18] This approach overlooks the roles of uncharacterized taxa such as the DTB120 phylum, found at Lōihi [11, 20], as well as viral communities that may moderate mat ecology and mediate nutrient fluxes [27]. Major questions remain about the metabolisms and biogeochemical roles of these iron oxidation-driven ecosystems
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