Aerobic and anaerobic iron oxidizers together drive denitrification and carbon cycling at marine iron-rich hydrothermal vents

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.

Iron Oxidation by a Fused Cytochrome-Porin Common to Diverse Iron-Oxidizing Bacteria

“…The expression of cyc2 and the nitrate reduction gene narG from “ Ca. Ferristratum” increased concurrently in response to Fe(II) addition, suggesting this group of organisms couples iron oxidation to nitrate reduction ( 10 ). This approach can guide the exploration of the diversity, distribution, and roles of iron-oxidizing bacteria in environmental systems.…”

“…Environmental metatranscriptomics of marine iron-oxidizing microbial mats dominated by Zetaproteobacteria , including Mariprofundus spp. found high expression of cyc2 , along with evidence that cyc2 expression may be regulated in response to Fe(II), suggesting utility for cyc2 in an iron-oxidizing environment ( 7 , 10 ). Proteomics of M. ferrooxydans PV-1 showed that Cyc2 was expressed, and a membrane complex containing Cyc2 possessed ferrocyanide oxidation activity ( 39 ).…”

“…Neutrophilic iron oxidizers thrive at anoxic-oxic interfaces where they can outcompete abiotic iron oxidation rates at low oxygen concentrations ( 8 ). Iron-oxidizing microbes can grow by coupling iron oxidation to the reduction of oxygen or nitrate, using this energy to fuel carbon fixation and biomass production ( 2 , 9 , 10 ), but in many iron-replete environments, we lack a clear understanding of the extent of microbial iron oxidation. To address this, we need to confidently identify iron oxidation mechanisms.…”

Metagenomic Insights Into the Microbial Iron Cycle of Subseafloor Habitats

“…Iron is the dominant redox-active element in the Earth's crust and an important nutrient for almost all known life. In many environments, iron cycling is intimately linked to biogeochemical cycling of other elements, including carbon (e.g., CO 2 , CH 4 , and organic carbon), nitrogen (Laufer et al, 2016b;McAllister et al, 2020b), and heavy metals (Cooper et al, 2006). Thus, even though biologically available iron is comparatively rare/transient in many ecosystems, its speciation and flux considerably impacts the overall activities and productivity of diverse ecosystems.…”

“…While there have been studies, largely in ecosystems where iron-oxidizing and -reducing bacteria are conspicuously present (Riedinger et al, 2014;Laufer et al, 2016a,b;Beam et al, 2018;Bryce et al, 2018;Aromokeye et al, 2020;McAllister et al, 2020b), the extent of microbial iron cycling in other environments, including marine sediment and sediment-buried crustal aquifers, remains comparatively underexplored. Even though microbes capable of iron redox can form only a small proportion of the community in the latter habitats (e.g., rare biosphere), their influence on iron-cycling has potential to significantly impact the surrounding geochemistry.…”