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

Flora Vincent, Matti Gralka, Guy Schleyer, Daniella Schatz, Miguel Cabrera-Brufau, Constanze Kuhlisch, Andreas Sichert, Silvia Vidal-Melgosa, Kyle Mayers, Noa Barak-Gavish, J. Michel Flores, Marta Masdeu-Navarro, Jorun Karin Egge, Aud Larsen, Jan-Hendrik Hehemann, Celia Marrasé, Rafel Simó, Otto X. Cordero and Assaf Vardi ()
Additional contact information
Flora Vincent: Weizmann Institute of Science
Matti Gralka: Massachusetts Institute of Technology
Guy Schleyer: Weizmann Institute of Science
Daniella Schatz: Weizmann Institute of Science
Miguel Cabrera-Brufau: Institut de Ciències del Mar, CSIC
Constanze Kuhlisch: Weizmann Institute of Science
Andreas Sichert: Massachusetts Institute of Technology
Silvia Vidal-Melgosa: Max Planck Institute for Marine Microbiology
Kyle Mayers: NORCE Norwegian Research Centre
Noa Barak-Gavish: Weizmann Institute of Science
J. Michel Flores: Weizmann Institute of Science
Marta Masdeu-Navarro: Institut de Ciències del Mar, CSIC
Jorun Karin Egge: University of Bergen
Aud Larsen: NORCE Norwegian Research Centre
Jan-Hendrik Hehemann: Max Planck Institute for Marine Microbiology
Celia Marrasé: Institut de Ciències del Mar, CSIC
Rafel Simó: Institut de Ciències del Mar, CSIC
Otto X. Cordero: Massachusetts Institute of Technology
Assaf Vardi: Weizmann Institute of Science

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-36049-3

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