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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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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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.
The authors declare no competing interests.
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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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