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

Abstract

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.

Viral infection arrests coccolithophore calcification and nutrient consumption, and triggers shifts in organic stoichiometry

“…This can be attributed to viral-mediated cell lysis and release of cellular contents to the medium as dissolved forms. This agrees with recently reported important loss of dissolved carbon in E. huxleyi during infection (Vincent et al 2023). Nonetheless, differential loss of POC, PON and POP was detected, which led to a consistent relative enrichment of both C and P relative to N in organic matter during infections (Fig.…”

“…Given the rampant accumulation of free bacteria during the infection experiments (see Fig. 3), it is most likely that there was a concomitant accumulation of bacteria attached to particulate organic matter (Vincent et al 2023). POM-bound bacteria were not measured.…”

Biological sources and sinks of dimethylsulfide disentangled by an induced bloom experiment and a numerical model

“…Nanophytoplankton are divided into two types because their overall biomass increases during both blooms but the species involved in each bloom are different (see fig. 2 of Vincent et al (2023)). Eukaryotic picophytoplankton are grouped into a single type because their biomass increases only during the first bloom.…”

“…All observations presented in this article come from an induced phytoplankton bloom experiment carried out between the 23 May 2018 (day À1) and the 16 June 2018 (day 23) in Raunefjorden at the Marine Biological Station Espegrend (60 16 0 11N; 5 13 0 07E) in southern Norway (Kuhlisch et al 2021;Vincent et al 2023). On day À1, seven light-transparent 4-mdeep enclosure bags were filled with nonfiltered surrounding fjord water and continuously mixed by air bubbling (from day 0 onward).…”

“…Nutrient concentrations and plankton abundances from each bag (Supplementary Figs. S1, S2) were measured by Vincent et al (2023). In each bag, the phytoplankton community responded to nutrient addition (Supplementary Fig.…”