The sulfur cycle connects microbiomes and biogeochemistry in deep-sea hydrothermal plumes

Abstract

In globally distributed deep-sea hydrothermal vent plumes, microbiomes are shaped by the redox energy landscapes created by reduced hydrothermal vent fluids mixing with oxidized seawater. Plumes can disperse over thousands of kilometers and are complex. Their characteristics are determined by geochemical sources from hydrothermal vents, e.g., hydrothermal inputs, nutrients, and trace metals. However, the impacts of plume biogeochemistry on the oceans are poorly constrained due to a lack of integrated understanding of microbiomes, population genetics, and geochemistry. Here, we use microbial genomes to understand links between biogeography, evolution, and metabolic connectivity, and elucidate their impacts on biogeochemical cycling in the deep sea. Using data from 37 diverse plumes from 8 ocean basins, we show that sulfur metabolism defines the core microbiome of plumes and drives metabolic connectivity. Amongst all microbial metabolisms, sulfur transformations had the highest MW-score, a measure of metabolic connectivity in microbial communities. Our findings provide the ecological and evolutionary basis of change in sulfur-driven microbial communities and their population genetics in adaptation to changing geochemical gradients in the oceans.

Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

“…Given the importance of sulfur cycling in deep-sea hydrothermal systems [67][68][69], it is not surprising that genes associated with elemental sulfur, sulfide, and thiosulfate oxidation; sulfate reduction; and thiosulfate disproportionation were widely distributed in MAGs from different hydrothermal samples and were associated with diverse taxonomic guilds (Figs. 7 and 8).…”

Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota

“…Hydrothermal plumes are one of the major components of hydrothermal vent fields in the global midocean ridge system, and they have a profound influence on elemental cycles in the ocean ( 28 ). Hydrothermal plumes represent an extended mixed gradient between the venting fluid and the seawater, allowing for the settlement of luxuriant microbial and animal communities that derive their energy via chemosynthesis through oxidation-reduction reactions ( 29 , 30 ). The disproportionation of sulfur compounds in hydrothermal plumes has not been studied because the identification of sulfur-disproportionating bacteria relies on either cultural approaches or activity measurements.…”

Abundant and metabolically flexible lineages within the SAR324 and gammaproteobacteria dominate the potential for rubisco-mediated carbon fixation in the dark ocean

“…b) Schematic of phylogenetic relationships within the rubisco superfamily adapted from [24]. c) Pathway diagram for oxidative reactions involving sulfur, adapted from [93]. Abbreviations: prk, phosphoribulokinase; pgk, phosphoglycerate kinase; gapdh, glyceraldehyde 3-phosphate dehydrogenase; fba, fructose-1,6-bisphosphate aldolase, tim, triosephosphate isomerase; fbpase, fructose-1,6-bisphosphatase; tkl, transketolase; sbpase, sedoheptulose-1,7-bisphosphatase; rpi, ribose-5-phosphate isomerase; rpe, ribulose 5-phosphate 3-epimerase; ox., oxidation; prod., production, disp., disproportionation; org., organic; Hyd, hydrogen.…”