The mutual interplay between calcification and coccolithovirus infection

Christopher T Johns,Helen F Fredricks,Benjamin A S Van Mooy,Jozef I Nissimov,Austin R Grubb,Alwin Mui,Kay D Bidle,Frank Natale,Viki Knapp

doi:10.1111/1462-2920.14362

Abstract

SummaryTwo 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.

Highlights

Distributed, unicellular coccolithophores have existed in the oceans for at least 209–220 million years (Falkowski et al, 2004; Monteiro et al, 2016), playing prominent roles in the oceanic carbon cycle due to their ability to both photosynthetically fix CO2 into particulate organic carbon (POC) and biomineralize particulate inorganic carbon (PIC) as calcium carbonate (CaCO3) (Iglesias-Rodriguez et al, 2002)
The E. huxleyi strains used in this study span a range of calcification states, side-scatter and CaCO3:POC ratios relevant to carbon flux (Fig. 1)
Our results demonstrate that calcification is another important factor influencing the dynamic arms race between E. huxleyi and coccolithoviruses

Summary

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. 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. 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’. Virus interactions in the ocean and interpreting their impact on the global carbon cycle

Introduction

Results and discussion

Conclusion

Experimental procedures Culture growth and maintenance