Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents

Abstract

Significance Heterotrophic protists are ubiquitous in all aquatic ecosystems and represent an important ecological link in food webs by transferring organic carbon from primary producers to higher trophic levels. Here, we quantify the predator–prey trophic interaction among protistan grazers and microbial prey within hydrothermal vent fluids from the Gorda Ridge spreading center in the northeast Pacific Ocean. Estimates of protistan grazing pressure were highest at sites of diffusely venting fluids, which are an oasis of biological activity in the deep sea. Our findings suggest that elevated grazing activity is attributed to a diverse assemblage of heterotrophic protistan species drawn to the hydrothermal vent habitat and demonstrates the important ecological roles that protists play in the deep-sea carbon cycle. 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.