Pressure-driven microbial and viral dynamics on individual sinking particles: implications for carbon cycling

Chloé M.J. Baumas, Danny Ionescu, Marc Garel, Hans-Peter Grossart, Christian Tamburini, Mina Bizic

The ocean’s biological carbon pump (BCP) regulates atmospheric CO2 by exporting organic carbon from the surface to the deep ocean. This process mainly depends on microbial communities associated with sinking particles which produce, degrade and transform organic matter. While many factors impact the efficiency of the BCP, here, we focus on particle heterogeneity and hydrostatic pressure, i.e. the relationships between microbial communities and heterogenous individual particles and the effect of increasing hydrostatic pressure on these relationships during particle descent in the upper mesopelagic. We accessed metagenomic and transcriptomic data at the level of individual particles exposed to increasing pressure mimicking gravitational particle sinking. Our results underscore the high variability among individual sinking particles in terms of community composition and metabolic activity. Individual-particle analyses revealed significant heterogeneity, even within particles of similar origin pointing to stochastic microbial colonization. These findings challenge traditional assumptions of similar responses by different microorganisms, revealing intricate and variable processes on individual particles (not captured by bulk measurements) that govern organic matter cycling. Under increased hydrostatic pressure, microbial diversity declined, with species-specific responses dominating on individual particles. We recognized piezosensitive microbes (not adapted to high pressure) that experienced broad transcriptional declines, and piezotolerant species that showed resilience and/or enhanced overall transcriptional activity. Metabolic pathways essential for carbon cycling, including organic matter degradation, were altered under hydrostatic pressure. At increasing pressure, viral dynamics shifted notably with lytic viral forms becoming dominant, potentially increasing microbial mortality and altering nutrient cycling on individual particles. Overall, our findings imply that accounting for particle heterogeneity and hydrostatic pressure driven changes allow to refine carbon flux models and improve predictions under changing ocean conditions.