Major contribution of particle-associated microbes to deep-sea organic carbon degradation

The biological carbon pump mediates the export of particulate organic carbon from the euphotic zone to the deep ocean, where it provides the base of the food web. Although deep-sea microbial metabolism is considered to be largely associated with macroscopic particles, such as marine snow, the specific contribution of particle-associated microorganisms to the utilization of bulk organic matter has rarely been directly quantified. We used in situ pumps to collect particles larger than 3 μm from mesopelagic and bathypelagic waters along a latitudinal transect in the North Atlantic. Prokaryotic abundance, respiration, heterotrophic biomass production, and community composition were determined and compared to the bulk prokaryotic community collected by Niskin bottles. Although particle-associated prokaryotes represented less than 1% of bulk prokaryotic abundance, they contributed on average 28% to bulk prokaryotic respiration and 12% to biomass production. The organic carbon turnover time of particles mediated by prokaryotes was 0.5–1.5 months, while it was up to 3 yr for the total organic carbon fraction. Thus, particles represent hotspots of organic carbon remineralization in the mesopelagic and bathypelagic ocean. Furthermore, metagenomic analyses revealed clear differences in taxonomy and diversity between the free-living (0.2–0.8 μm) and particle-associated (> 3 μm) prokaryotic communities. Our results emphasize the significant role of particle-associated prokaryotes in driving organic matter utilization in the dark ocean.