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, Assaf Vardi*

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

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.

Original languageEnglish
Article number510
Pages (from-to)1-17
Number of pages17
JournalNature Communications
Volume14
DOIs
Publication statusPublished - 31 Jan 2023

Bibliographical note

Funding Information:
We thank all team members of the AQUACOSM VIMS-Ehux project for setting up and conducting the mesocosm experiment. We further thank the team members and crew of the NA-VICE cruise for assistance at sea, as well as the Marine Facilities and Operations at the Woods Hole Oceanographic Institution for logistical support. We thank Miri Shnayder for help on ddPCR, Tina Trautmann for help on microarrays and Jackie Collier for discussion on Thraustochytrids. This research was supported by the European Research Council CoG (VIROCELLSPHERE grant no. 681715, A.V.), the European Research Council AdV (VIBES, grant no. 101053543, A.V.) and the Simons foundation grant (no. 735079, A.V.) “Untangling the infection outcome of host-virus dynamics in algal blooms in the ocean” and the Dean of Faculty Fellowship of the Weizmann Institute of Science and Israeli Academy of Science and Humanities awarded to F.V. The mesocosm experiment VIMS-Ehux was supported by EU Horizon2020-INFRAIA project AQUACOSM (grant no. 731065, A.V.). The NA-VICE cruise was supported by the NSF (grant no. OCE-1059884). J.-H.H. was supported by the Max Planck Society and by the Deutsche Forschungsgemeinschaft (DFG) Emmy Noether grant HE 7217/1-1, and through the Cluster of Excellence “The Ocean Floor—Earth’s Uncharted Interface” project 390741603. O.X.C. was supported by the Simons Collaboration: Principles of Microbial Ecosystems (PriME) award no. 542395. M.G. was supported by Simons Foundation Postdoctoral Fellowship Award 599207. The ICM-CSIC group acknowledges funding from Spanish Ministry of Science and Innovation (MCIN/AEI, doi: 10.13039/501100011033) through the BIOGAPS grant (CTM2016–81008–R) and the “Severo Ochoa Centre of Excellence” accreditation (CEX2019-000298-S), and from the European Research Council under the EU’s Horizon 2020 research and innovation programme through the SUMMIT grant (ERC-2018-AdG#834162).

Funding Information:
We thank all team members of the AQUACOSM VIMS-Ehux project for setting up and conducting the mesocosm experiment. We further thank the team members and crew of the NA-VICE cruise for assistance at sea, as well as the Marine Facilities and Operations at the Woods Hole Oceanographic Institution for logistical support. We thank Miri Shnayder for help on ddPCR, Tina Trautmann for help on microarrays and Jackie Collier for discussion on Thraustochytrids. This research was supported by the European Research Council CoG (VIROCELLSPHERE grant no. 681715, A.V.), the European Research Council AdV (VIBES, grant no. 101053543, A.V.) and the Simons foundation grant (no. 735079, A.V.) “Untangling the infection outcome of host-virus dynamics in algal blooms in the ocean” and the Dean of Faculty Fellowship of the Weizmann Institute of Science and Israeli Academy of Science and Humanities awarded to F.V. The mesocosm experiment VIMS-Ehux was supported by EU Horizon2020-INFRAIA project AQUACOSM (grant no. 731065, A.V.). The NA-VICE cruise was supported by the NSF (grant no. OCE-1059884). J.-H.H. was supported by the Max Planck Society and by the Deutsche Forschungsgemeinschaft (DFG) Emmy Noether grant HE 7217/1-1, and through the Cluster of Excellence “The Ocean Floor—Earth’s Uncharted Interface” project 390741603. O.X.C. was supported by the Simons Collaboration: Principles of Microbial Ecosystems (PriME) award no. 542395. M.G. was supported by Simons Foundation Postdoctoral Fellowship Award 599207. The ICM-CSIC group acknowledges funding from Spanish Ministry of Science and Innovation (MCIN/AEI, doi: 10.13039/501100011033) through the BIOGAPS grant (CTM2016–81008–R) and the “Severo Ochoa Centre of Excellence” accreditation (CEX2019-000298-S), and from the European Research Council under the EU’s Horizon 2020 research and innovation programme through the SUMMIT grant (ERC-2018-AdG#834162).

Publisher Copyright:
© 2023, The Author(s).

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