A hydrogenotrophic Sulfurimonas is globally abundant in deep-sea oxygen-saturated hydrothermal plumes

Abstract

Members of the bacterial genus Sulfurimonas (phylum Campylobacterota) dominate microbial communities in marine redoxclines and are important for sulfur and nitrogen cycling. Here we used metagenomics and metabolic analyses to characterize a Sulfurimonas from the Gakkel Ridge in the Central Arctic Ocean and Southwest Indian Ridge, showing that this species is ubiquitous in non-buoyant hydrothermal plumes at Mid Ocean Ridges across the global ocean. One Sulfurimonas species, USulfurimonas pluma, was found to be globally abundant and active in cold (<0−4 °C), oxygen-saturated and hydrogen-rich hydrothermal plumes. Compared with other Sulfurimonas species, US. pluma has a reduced genome (>17%) and genomic signatures of an aerobic chemolithotrophic metabolism using hydrogen as an energy source, including acquisition of A2-type oxidase and loss of nitrate and nitrite reductases. The dominance and unique niche of US. pluma in hydrothermal plumes suggest an unappreciated biogeochemical role for Sulfurimonas in the deep ocean.

A pan‐genomic approach reveals novel Sulfurimonas clade in the ferruginous meromictic Lake Pavin

“…Comparative analysis of the 17 Sulfurimonas reference genomes revealed a pan‐genome composed of 9021 gene clusters (GCs) among which 915 core GCs, 3508 shell GCs and 4598 cloud GCs (Figure 7a), which is consistent with previous studies (Molari et al., 2023; Wang, Jiang, et al., 2021). With regards to the LP genomes (SAG 733‐F2, Bin58 and Bin76), they contained 272–842 core GCs, 460–1152 shell GCs, and 57–192 cloud GCs (Figure 7b).…”

“…All components required for the denitrification pathway were detected in LP strains (Figure 5b, Table S11), with a periplasmic nitrate reductase catalytic subunit (NapA) organised in a well conserved operon. Only S. pluma is currently known to lack this operon (Molari et al., 2023). Moreover, as previously shown, NapA from hydrothermal vent strains represent a monophyletic group distinct from genomes obtained from other ecosystems (Figure S7).…”

“…Like other Sulfurimonas genomes (Molari et al., 2023), LP strains carry various systems for uptake and intracellular availability control of iron and manganese. Among them, a gene encodes a DNA‐binding protein belonging to the ferritin‐like diiron‐carboxylate protein superfamily (known as Dps).…”

“…NO 3 − , O 2 , MnO 2 ) and by their adaptative abilities (e.g. aerobic to anoxic growth conditions, osmotic stress, etc) (Götz et al., 2018; Molari et al., 2023; Rogge et al., 2017; Taylor et al., 2018; Zeng et al., 2021). In addition to chemolithoautotrophic oxidation of sulfur compounds, they also perform chemolithoautotrophic disproportionation of thiosulphate and elemental sulphur that may represent a previously unrecognised primary production process (Wang et al., 2023).…”

Reduced chemosymbiont genome in the methane seep thyasirid and the cooperated metabolisms in the holobiont under anaerobic sediment

“…The different structure in the redox-driven pumping mechanism from mitochondria-like caa 3 -type enables cbb 3 -type to keep catalytic activity at low oxygen concentrations (Buschmann et al, 2010). By contrast, the acquisition of caa 3 -types cytochrome c oxidase in Sulfurimonas pluma was proposed as one of the adaptive strategies in the aerobic chemolithotrophic metabolism (Molari et al, 2023). Therefore, the loss of caa 3 -type might be a signature of the thyasirid holobionts from Haima hydrocarbon seep undergoing an anaerobic metabolism for an extended period.…”