Metatranscriptomics reveals protistan and viral metabolic reprogramming of sinking particle microbiomes in Oyashio waters.

Protists and viruses play a crucial role in the biological carbon pump by aggregating and degrading organic carbon. However, the identities of active lineages and their metabolic activities within sinking particles remain poorly characterized. Here, we examined the transcriptional dynamics of protists and viruses in sinking and suspended particles collected by a marine snow catcher in the Oyashio region. We found taxon-specific metabolic variations, with sinking particles showing high abundance of upregulated transcripts from ciliates, dinoflagellates, and viruses, while suspended particles exhibited those from haptophytes and chlorophytes. Diatoms exhibited species-specific responses to particle types: Minidiscus variabilis upregulated more genes in suspended particles, whereas the large chain-forming Thalassiosira rotula overexpressed genes in sinking particles. Gene co-expression network analysis revealed that the diatom Thalassiosira and Chaetoceros, which include chain-forming species, constitute a co-expression module positively correlated with POC and PON fluxes, while modules enriched in small phytoplankton (e.g. Minidiscus, haptophytes, and chlorophytes) were negatively correlated with these fluxes. A module dominated by ciliates, dinoflagellates, and viruses associated with sinking particles was negatively correlated with POC and PON fluxes, implying that their consumption and lysis of the sinking organisms could reduce the vertical export. Consistently, dinoflagellate species such as Karlodinium veneficum and Karenia brevis exhibited enrichment of functional genes involved in carbon degradation pathways. Overall, our findings underscore the importance of specific plankton and viral lineages and their functions in aggregation and degradation processes of sinking particles.