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Microbial eukaryotes (or protists) in marine ecosystems are a link between primary producers and all higher trophic levels, and the rate at which heterotrophic protistan grazers consume microbial prey is a key mechanism for carbon transport and recycling in microbial food webs. At deep-sea hydrothermal vents, chemosynthetic bacteria and archaea form the base of a food web that functions in the absence of sunlight, but the role of protistan grazers in these highly productive ecosystems is largely unexplored. Here, we pair grazing experiments with a molecular survey to quantify protistan grazing and to characterize the composition of vent-associated protists in low-temperature diffuse venting fluids from Gorda Ridge in the northeast Pacific Ocean. Results reveal protists exert higher predation pressure at vents compared to the surrounding deep seawater environment and may account for consuming 28 to 62% of the daily stock of prokaryotic biomass within discharging hydrothermal vent fluids. The vent-associated protistan community was more species rich relative to the background deep sea, and patterns in the distribution and co-occurrence of vent microbes provide additional insights into potential predator–prey interactions. Ciliates, followed by dinoflagellates, Syndiniales, rhizaria, and stramenopiles, dominated the vent protistan community and included bacterivorous species, species known to host symbionts, and parasites. Our findings provide an estimate of protistan grazing pressure within hydrothermal vent food webs, highlighting the important role that diverse protistan communities play in deep-sea carbon cycling.

Little is known about viruses in oxygen-deficient water columns (ODWCs). In surface ocean waters, viruses are known to act as gene vectors among susceptible hosts. Some of these genes may have metabolic functions and are thus termed auxiliary metabolic genes (AMGs). AMGs introduced to new hosts by viruses can enhance viral replication and/or potentially affect biogeochemical cycles by modulating key microbial pathways. Here we identify 748 viral populations that cluster into 94 genera along a vertical geochemical gradient in the Cariaco Basin, a permanently stratified and euxinic ocean basin. The viral communities in this ODWC appear to be relatively novel as 80 of these viral genera contained no reference viral sequences, likely due to the isolation and unique features of this system. We identify viral elements that encode AMGs implicated in distinctive processes, such as sulfur cycling, acetate fermentation, signal transduction, [Fe–S] formation, and N-glycosylation. These AMG-encoding viruses include two putative Mu-like viruses, and viral-like regions that may constitute degraded prophages that have been modified by transposable elements. Our results provide an insight into the ecological and biogeochemical impact of viruses oxygen-depleted and euxinic habitats.

Genetic markers and geochemical assays of microbial nitrogen cycling processes, including autotrophic and heterotrophic denitrification, anammox, ammonia oxidation, and nitrite oxidation, were examined across the oxycline, suboxic, and anoxic zones of the Cariaco Basin, Venezuela. Ammonia and nitrite oxidation genes were expressed through the entire gradient. Transcripts associated with autotrophic and heterotrophic denitrifiers were mostly confined to the suboxic zone and below but were also present in particles in the oxycline. Anammox genes and transcripts were detected over a narrow depth range near the bottom of the suboxic zone and coincided with secondary NO₂⁻maxima and available NH₄⁺. Dissolved inorganic nitrogen (DIN) amendment incubations and comparisons between our sampling campaigns suggested that denitrifier activity may be closely coupled with NO₃⁻availability. Expression of denitrification genes at depths of high rates of chemoautotrophic carbon fixation and phylogenetic analyses of nitrogen cycling genes and transcripts indicated a diverse array of denitrifiers, including chemoautotrophs capable of using NO₃⁻to oxidize reduced sulfur species. Thus, results suggest that the Cariaco Basin nitrogen cycle is influenced by autotrophic carbon cycling in addition to organic matter oxidation and anammox.

A chemoautotrophy maximum is present in many anoxic basins at the sulfidic layer's upper boundary, but the factors controlling this feature are poorly understood. In 13 of 31 cruises to the Cariaco Basin, particulate organic carbon (POC) was enriched in¹³C (δ¹³C_POCas high as −16‰) within the oxic/sulfidic transition compared to photic zone values (−23 to −26‰). During “heavy” cruises, fluxes of O₂and [NO₃⁻+ NO₂⁻] to the oxic/sulfidic interface were significantly lower than during “light” cruises. Cruises with isotopically heavy POC were more common between 2013 and 2015 when suspended particles below the photic zone tended to be nitrogen rich compared to later cruises. Within the chemoautotrophic layer, nitrogen‐rich particles (molar ratio C/N< 10) were more likely to be¹³C‐enriched than nitrogen‐poor particles, implying that these inventories were dominated by living cells and fresh detritus rather than laterally transported or extensively decomposed detritus. During heavy cruises,¹³C enrichments persisted to 1,300 m, providing the first evidence of downward transport of chemoautotrophically produced POC. Dissolved inorganic carbon assimilation during heavy cruises (n= 3) was faster and occurred deeper than during light cruises (n= 2). Metagenomics data from the chemoautotrophic layer during two cruises support prevalence of microorganisms carrying RuBisCO form II genes, which encode a carbon fixation enzyme that discriminates less against heavy isotopes than most other carbon fixation enzymes, and metatranscriptomics data indicate that higher expression of form II RuBisCO genes during the heavy cruises at depths where essential reactants coexist are responsible for the isotopically heavier POC.