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Expression profiling of host and virus during a coccolithophore bloom provides insights into the role of viral infection in promoting carbon export

The ISME Journalvolume 12pages704713 (2018) | Download Citation

Abstract

The cosmopolitan coccolithophore Emiliania huxleyi is a unicellular eukaryotic alga that forms vast blooms in the oceans impacting large biogeochemical cycles. These blooms are often terminated due to infection by the large dsDNA virus, E. huxleyi virus (EhV). It was recently established that EhV-induced modulation of E. huxleyi metabolism is a key factor for optimal viral infection cycle. Despite the huge ecological importance of this host–virus interaction, the ability to assess its spatial and temporal dynamics and its possible impact on nutrient fluxes is limited by current approaches that focus on quantification of viral abundance and biodiversity. Here, we applied a host and virus gene expression analysis as a sensitive tool to quantify the dynamics of this interaction during a natural E. huxleyi bloom in the North Atlantic. We used viral gene expression profiling as an index for the level of active infection and showed that the latter correlated with water column depth. Intriguingly, this suggests a possible sinking mechanism for removing infected cells as aggregates from the E. huxleyi population in the surface layer into deeper waters. Viral infection was also highly correlated with induction of host metabolic genes involved in host life cycle, sphingolipid, and antioxidant metabolism, providing evidence for modulation of host metabolism under natural conditions. The ability to track and quantify defined phases of infection by monitoring co-expression of viral and host genes, coupled with advance omics approaches, will enable a deeper understanding of the impact that viruses have on the environment.

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Acknowledgments

We thank the captain and crew of the R/V Knorr during the NAVICE cruise as well as the Marine Facilities and Operations at the Woods Hole Oceanographic Institution for assistance and cooperation at sea. We thank Shifra Ben-Dor for her contribution to the bioinformatics analysis. This research was supported by a European Research Council (ERC) StG (INFOTROPHIC grant # 280991) and CoG (VIROCELLSPHERE grant # 681715) as well as by the National Science Foundation (NSF) grant OCE-1061883 (to AV and KDB).

Author Contributions

US, SR, and AV conceived and design the experiments and analyses. US and SR analyzed the expression data. DS and NBG preformed and analyzed E. huxleyi and viral DNA qPCR enumeration. US analyzed all data including the cruise data. YL and IK analyzed satellite imagery. KDB was the chief scientist on the NAVICE cruise and implemented corresponding ship-based sampling strategies. RR preformed statistical analysis. US, AV, NBG, SR, and DS contributed to the writing of the manuscript. AV supervised the project.

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Affiliations

  1. Departments of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel

    • Uri Sheyn
    • , Shilo Rosenwasser
    • , Noa Barak-Gavish
    • , Daniella Schatz
    •  & Assaf Vardi
  2. The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University, Rehovot, 7610001, Israel

    • Shilo Rosenwasser
  3. Departments of Earth and Planetary Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel

    • Yoav Lehahn
    •  & Ilan Koren
  4. Department of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot, 7610001, Israel

    • Ron Rotkopf
  5. Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, 08901, USA

    • Kay D. Bidle

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The authors declare no conflict of interest.

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Correspondence to Assaf Vardi.

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DOI

https://doi.org/10.1038/s41396-017-0004-x