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.

The community of Marine Alveolate parasites in the Atlantic inflow to the Arctic Ocean is structured by season, depth and water mass

“…This cluster also had the highest number of unique ASVs (i.e., only detected in this cluster, Figure S5). A high number of unique MALV ASVs at depths 800 -1000 m has also been found in oligotrophic, tropical oceans (Anderson et al 2024). The most abundant clades in this cluster were DG-II Clades 6 and 7, and the most abundant ASVs were also assigned to these clades.…”

“…In the marine environment, parasitism by unicellular eukaryotes (protists) may regulate population sizes of both primary producers and consumers, and thus impact the food web structure and the carbon cycle (Berdjeb et al 2018;Skovgaard 2014). Consequently, new knowledge on the diversity and host preferences of marine protistan parasites ultimately has the potential to inform and improve models of trophic transfer and biogeochemical cycling (Anderson et al 2024).…”

“…The enigmatic Marine Alveolates (commonly referred to as MALVs) is a polyphyletic assemblage of parasitic dinoflagellates which are considered to be the dominating group of parasites in marine microbial food webs (Anderson et al 2024;Bjorbaekmo et al 2019;Holt et al 2023). In environmental sequencing studies, MALVs are generally reported to have high abundance and richness in marine pelagic environments (e.g.…”

“…Communities of microbial parasites and MALV in particular in a given layer of the water column may be shaped by biological factors such as access to hosts, and physical factors such as mixing or stratification of the water column, and sinking when attached to hosts or particles (Anderson et al 2024). Early meta-studies of environmental sequencing datasets suggested that MALV clade composition differs between the photic and aphotic zone (Guillou et al 2008).…”

“…Early meta-studies of environmental sequencing datasets suggested that MALV clade composition differs between the photic and aphotic zone (Guillou et al 2008). A recent metabarcoding study of MALV composition in the water column in the Sargasso sea found depth-structuring which was repeated over several years, and in this temperate region the MALV community was more strongly structured by depth than season (Anderson et al 2024). However, the seasonal variation of the pelagic MALV community composition is not well studied (Anderson and Harvey 2020), especially in polar regions and at mesopelagic depths, where sampling during the winter is challenging due to darkness and rough weather.…”