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

Abstract

Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global nutrient cycling. When blooms collapse, organic carbon is transferred to higher trophic levels, microbial respiration or sinking in proportions that depend on the dominant mortality agent. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains an open question. Here, we characterized the consequences of viral infection on the microbiome composition and biogeochemical landscape of marine ecosystems by conducting a large-scale mesocosm experiment. Moniroting of seven induced coccolithophore blooms, which showed different degrees of viral infection, revealed that only high levels of viral infection caused significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, viral infection favored the growth of eukaryotic heterotrophs (thraustochytrids) over 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 can increase per-cell rates of extracellular carbon release by 2-4.5 fold. This happened via production 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.

Novel lipid biomarkers for algal resistance to viral infection in the ocean

“…Therefore, we sought to gain a detailed temporal resolution for our suite of biomarkers in order to assess the various phenotypes the occur during E. huxleyi bloom succession. Therefore, we conducted an in situ mesocosm experiment in the coastal waters of southern Norway 51, 52 , where annual blooms and viral infection of E. huxleyi occur naturally 27 . Briefly, the experiment included seven mesocosm bags that were filled with natural marine microbial communities and monitored daily over 24 days.…”

“…6a, b and Fig. S24a, b), which were isolated during the bloom phase of E. huxleyi 51 . However, we also isolated a few resistant E. huxleyi strains, among them isolate RCC6961 (Fig.…”

“…S24c). This isolate, along with additional resistant isolates, was isolated during the virus-induced demise phase of the E. huxleyi bloom 51 . Interestingly, some of the isolated susceptible strains showed rapid recovery 1-2 weeks after viral infection (RCC6918 and RCC6912, Fig.…”

“…E. huxleyi RCC6936 was isolated from bag 4 at day 13 of the experiment (June 6, 2018), also during the bloom phase of E. huxleyi . The resistant isolate RCC6961 was isolated from bag 7 at day 16 of the experiment (June 9, 2018), during the virus-induced demise of E. huxleyi 51 .…”

Complete Genome Sequence of Emiliania huxleyi Virus Strain M1, Isolated from an Induced E. huxleyi Bloom in Bergen, Norway

“…EhV is a large, double-stranded DNA virus from the family Phycodnaviridae ( 2 ). Here, we report the complete genome sequence of EhV strain M1 (EhVM1), which was isolated from an E. huxleyi bloom during a mesocosm experiment in Bergen, Norway ( 3 , 4 ). To isolate EhV strains from the natural environment, water from the induced blooms in mesocosm bags ( 3 ) was filtered through a GF/C filter and stored at 4°C.…”