The mutual interplay between calcification and coccolithovirus infection

Abstract

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Johns, C. T., Grubb, A. R., Nissimov, J. I., Natale, F., Knapp, V., Mui, A., Fredricks, H. F., Van Mooy, B. A. S., & Bidle, K. D. The mutual interplay between calcification and coccolithovirus infection. Environmental Microbiology, 21(6), (2019): 1896-1915, doi:10.1111/1462-2920.14362.Two prominent characteristics of marine coccolithophores are their secretion of coccoliths and their susceptibility to infection by coccolithoviruses (EhVs), both of which display variation among cells in culture and in natural populations. We examined the impact of calcification on infection by challenging a variety of Emiliania huxleyi strains at different calcification states with EhVs of different virulence. Reduced cellular calcification was associated with increased infection and EhV production, even though calcified cells and associated coccoliths had significantly higher adsorption coefficients than non‐calcified (naked) cells. Sialic acid glycosphingolipids, molecules thought to mediate EhV infection, were generally more abundant in calcified cells and enriched in purified, sorted coccoliths, suggesting a biochemical link between calcification and adsorption rates. In turn, viable EhVs impacted cellular calcification absent of lysis by inducing dramatic shifts in optical side scatter signals and a massive release of detached coccoliths in a subpopulation of cells, which could be triggered by resuspension of healthy, calcified host cells in an EhV‐free, ‘induced media’. Our findings show that calcification is a key component of the E. huxleyi‐EhV arms race and an aspect that is critical both to the modelling of these host–virus interactions in the ocean and interpreting their impact on the global carbon cycle.We thank Liti Haramaty for her guidance and assistance in culturing and infection experiments. This research was funded by the Gordon and Betty Moore Foundation (GBMF3301 to BVM and KDB and GBMF3789 to KDB) and the National Science Foundation (OCE‐1537951 and OCE‐1559179 to KDB)