Syndiniales parasites drive species networks and are a biomarker for carbon export in the oligotrophic ocean

Abstract

Microbial associations that result in phytoplankton mortality are important for carbon transport in the ocean. This includes parasitism, which in microbial food webs, is dominated by the marine alveolate group, Syndiniales. Parasites are expected to contribute to carbon recycling via host lysis; however, knowledge on host dynamics and correlation to carbon export remain unclear and limit the inclusion of parasitism in biogeochemical models. We analyzed a 4-year 18S rRNA metabarcoding dataset (2016-2019), performing network analysis for twelve discrete depths (1- 1000 m) to determine Syndiniales-host associations in the seasonally oligotrophic Sargasso Sea. Analogous water column and sediment trap data were included to define environmental drivers of Syndiniales and their correlation with particulate carbon flux (150 m). Syndiniales accounted for 48-74% of network edges, most often associated with Dinophyceae and Arthropoda (mainly copepods) at the surface and Rhizaria (Polycystinea, Acantharea, and RAD-B) in the aphotic zone. Unlike other major groups, Syndiniales were significantly (and negatively) correlated with particulate carbon flux, suggesting parasites may drive flux attenuation through remineralization. Examination of Syndiniales amplicons revealed a range of depth patterns, including specific ecological niches and vertical connection among a subset (19%) of the community, the latter implying sinking of parasites (infected hosts or spores) on particles. Our findings point to the use of Syndiniales as biomarkers of carbon export, highlighting their importance for marine food webs and biogeochemistry. Significance StatementSyndiniales parasites are widespread in the ocean and represent a potentially important, albeit poorly resolved, source of carbon recycling. Here, we assess Syndiniales population dynamics, trophic relationships, and links to carbon export in the Sargasso Sea. Species networks at all depths were driven by Syndiniales, with parasite-host relationships varying with depth based on shifts in host composition. Syndiniales were the only eukaryote group to be significantly (and negatively) correlated with particulate carbon flux, indicating their contribution to flux attenuation via remineralization. Yet, a subset of parasites was vertically connected between photic and aphotic zones, suggesting continued export. Our findings elevate the critical role of Syndiniales in marine microbial systems and reveal their potential use as biomarkers for carbon export.