Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during coccolithophore blooms

Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global elemental cycling. Upon demise of the bloom, organic carbon is partly respired and partly transferred to either higher trophic levels, bacterial biomass production or sinking. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains largely unquantified. Here, we characterize the interplay between viral infection and the composition of a bloom-associated microbiome and consequently the evolving biogeochemical landscape, by conducting a large-scale mesocosm experiment where we monitor seven induced coccolithophore blooms. The blooms show different degrees of viral infection and reveal that only high levels of viral infection are followed by significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, upon viral infection the biomass of eukaryotic heterotrophs (thraustochytrids) rivals that of bacteria as potential recyclers of organic matter. By combining modeling and quantification of active viral infection at a single-cell resolution, we estimate that viral infection causes a 2-4 fold increase in per-cell rates of extracellular carbon release in the form of acidic polysaccharides and particulate inorganic carbon, two major contributors to carbon sinking into the deep ocean. These results reveal the impact of viral infection on the fate of carbon through microbial recyclers of organic matter in large-scale coccolithophore blooms. Algal blooms are hotspots of marine primary production that play central roles in microbial ecology and global elemental cycling. Here, the authors show how bloom termination by viral infection can shift the balance between eukaryotic and prokaryotic recyclers of phytoplankton biomass.

Automated summary

Algal blooms are important for marine primary production and play a central role in microbial ecology and global elemental cycling. This study investigates the effect of viral infection on the composition of a bloom-associated microbiome and the fate of carbon, and reveals that high levels of viral infection can result in significant shifts in bacterial and eukaryotic assemblages as well as increased carbon sinking into the deep ocean.