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Silicon limitation facilitates virus infection and mortality of marine diatoms

Nature Microbiology volume 4, pages 1790–1797 (2019)Cite this article

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Abstract

Diatoms are among the most globally distributed and ecologically successful organisms in the modern ocean, contributing upwards of 40% of total marine primary productivity1,2. By converting dissolved silicon into biogenic silica, and photosynthetically fixing carbon dioxide into particulate organic carbon, diatoms effectively couple the silicon (Si) and carbon cycles and ballast substantial vertical flux of carbon out of the euphotic zone into the mesopelagic and deep ocean3,4,5. Viruses are key players in ocean biogeochemical cycles6,7, yet little is known about how viral infection specifically impacts diatom populations. Here, we show that Si limitation facilitates virus infection and mortality in diatoms in the highly productive coastal waters of the California Current Ecosystem. Using metatranscriptomic analysis of cell-associated diatom viruses and targeted quantification of extracellular viruses, we found a link between Si stress and the early, active and lytic stages of viral infection. This relationship was also observed in cultures of the bloom-forming diatom Chaetoceros tenuissimus, where Si stress accelerated virus-induced mortality. Together, these findings contextualize viruses within the ecophysiological framework of Si availability and diatom-mediated biogeochemical cycling.

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Fig. 1: Station map, phytoplankton communities, Si stress and indicators of mortality during the DYEatom cruise in the California Current Ecosystem.
Fig. 2: Patterns of virus infection in diatom populations in the California Current Ecosystem.
Fig. 3: The impact of Si limitation on diatom host–virus dynamics in laboratory cultures of C. tenuissimus.
Fig. 4: Conceptual model of diatom host–virus dynamics and impacts on biogeochemical cycling.

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Data availability

All cruise-related data are available publicly at the Biological and Chemical Oceanography Data Management Office under the project number 550825 (https://www.bco-dmo.org/project/550825). The metatranscriptomic data reported in this paper have been deposited in the NCBI sequence read archive (BioProject accession no. PRJNA528986, BioSample accession nos SAMN11263616–SAMN11263639 and SAMN11258802–SAMN11258825). The assembled contigs used in this study can also be found at https://scripps.ucsd.edu/labs/aallen/data/ and BCO-DMO project number 558198 (https://www.bco-dmo.org/project/558198). All data generated or analysed during the current study are included in this published article and its supplementary information files.

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Acknowledgements

We would like to thank the captain and the crew of the RV Point Sur, J. Jones, H. McNair, E. Lachenmyer, I. Marquez and J. Ossolinski, for technical assistance during the cruise. Surface-tethered drogues used on the cruise were provided by R. Chant and E. Hunter. Thank you to Y. Tomaru for providing the laboratory diatom host–virus systems; J. Latham for technical support; B. Knowles, E. Zelzion and K. Bondoc for their useful discussions on statistical analysis; and B. Knowles and J. Nissimov for their helpful comments on the manuscript. This work was supported by grants from the National Science Foundation (grant nos OCE-13339329 and OCE-1559179 to K.T., OCE-1334387 to M.A.B., OCE-1155663 to J.W.K., and OCE-1637632 and OCE-1756884 to A.E.A.), the Gordon and Betty Moore Foundation (grant nos GBMF3301 to B.A.S.V.M. and K.D.B., GBMF3789 to K.D.B. and GBMF3828 to A.E.A.), the National Oceanic and Atmospheric Administration (grant no. NA15OAR4320071 to A.E.A.) and a postdoctoral fellowship from the Simons Foundation (grant no. 548156 to C.F.K.). Salary support for C.F.K. was also provided by the Institute of Earth, Ocean and Atmospheric Sciences at Rutgers University, the Rappaport Fund for Advanced Studies and Israel’s Council for Higher Education.

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Authors and Affiliations

  1. Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, USA

    Chana F. Kranzler, William P. Biggs, Kay D. Bidle & Kimberlee Thamatrakoln

  2. Dauphin Island Sea Lab, Dauphin Island, AL, USA

    Jeffrey W. Krause

  3. Department of Marine Sciences, University of South Alabama, Mobile, AL, USA

    Jeffrey W. Krause

  4. Marine Science Institute, University of California, Santa Barbara, CA, USA

    Mark A. Brzezinski & Michael Maniscalco

  5. Department of Earth and Planetary Science, University of California, Berkeley, CA, USA

    Bethanie R. Edwards

  6. Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, USA

    John P. McCrow & Andrew E. Allen

  7. Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    Benjamin A. S. Van Mooy

  8. Scripps Institution of Oceanography, University of California, San Diego, CA, USA

    Andrew E. Allen

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Contributions

C.F.K. and K.T. conceived the project, designed the experiments and wrote the paper. C.F.K. and W.P.B. conducted the laboratory culture-based experiments. C.F.K. performed the metatranscriptomic and statistical analyses. C.F.K. and K.T. processed and analysed the field samples for extracellular virus. M.M. assisted with the 18S rRNA and RdRP phylogenetic analyses. J.W.K. was the Chief Scientist of the DYEatom cruise. J.W.K., M.A.B., B.A.S.V.M., K.D.B. and K.T. were involved in the cruise planning. J.W.K. and M.A.B. collected and analysed the silica-production, nutrient and bulk particle data. B.R.E. and B.A.S.V.M. conducted and provided the on-ship protease activity data. K.D.B. and K.T. collected all other field samples. A.E.A. extracted the RNA and generated the metatranscriptome and 18S rRNA data. A.E.A. and J.P.M. performed the bioinformatic analyses. All authors provided comments on the manuscript.

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Correspondence to Kimberlee Thamatrakoln.

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Supplementary Information

Supplementary Figs. 1–7 and Supplementary Tables 1–3.

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Supplementary Dataset 1

Metatranscriptome and diatom virus analysis.

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Kranzler, C.F., Krause, J.W., Brzezinski, M.A. et al. Silicon limitation facilitates virus infection and mortality of marine diatoms. Nat Microbiol 4, 1790–1797 (2019). https://doi.org/10.1038/s41564-019-0502-x

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