Temperature-Induced Viral Resistance in Emiliania huxleyi (Prymnesiophyceae)

Abstract

Annual Emiliania huxleyi blooms (along with other coccolithophorid species) play important roles in the global carbon and sulfur cycles. E. huxleyi blooms are routinely terminated by large, host-specific dsDNA viruses, (Emiliania huxleyi Viruses; EhVs), making these host-virus interactions a driving force behind their potential impact on global biogeochemical cycles. Given projected increases in sea surface temperature due to climate change, it is imperative to understand the effects of temperature on E. huxleyi’s susceptibility to viral infection and its production of climatically active dimethylated sulfur species (DSS). Here we demonstrate that a 3°C increase in temperature induces EhV-resistant phenotypes in three E. huxleyi strains and that successful virus infection impacts DSS pool sizes. We also examined cellular polar lipids, given their documented roles in regulating host-virus interactions in this system, and propose that alterations to membrane-bound surface receptors are responsible for the observed temperature-induced resistance. Our findings have potential implications for global biogeochemical cycles in a warming climate and for deciphering the particular mechanism(s) by which some E. huxleyi strains exhibit viral resistance.

Temperature is a key factor in Micromonas–virus interactions

“…Hence, the thermal environment of Micromonas determines the outcome of viral infection, leading to drastic changes in the lytic cycle and a possible switch in viral life strategy. Similar thermal responses to viral infection were reported for the raphidophyte Heterosigma akashiwo (Nagasaki and Yamaguchi, 1998) and the haptophyte Emiliania huxleyi (Kendrick et al, 2014). An alteration of the algicidal activity of viruses at high temperatures and a reduced intensity of viral lysis at low temperatures seem to represent a global pattern, which may have important consequences for the regulation of phytoplankton population in the ocean.…”

“…The observed loss of viral infectivity at this temperature suggests that viruses could become inactive during the period of the experiment. However, we cannot rule out that alterations of host phenotype modify their susceptibility to viral infection as demonstrated recently in Kendrick et al (2014). Hence, temperatures above T opt induced complex outcomes after viral infection in Mic-B.…”

“…the temperature that generates fast host lysis and/or high viral yield) generally matches the host optimal growth temperature, it is usually assumed that the impact of temperature on viral infection mostly arises from changes in host metabolism. Temperature-driven changes in host physiology were indeed shown to alter the kinetics of viral lysis, possibly inducing the development of viral resistance (Nagasaki and Yamaguchi, 1998;Kendrick et al, 2014;Tomaru et al, 2014) or switches from a lysogenic to lytic lifestyle (Wilson et al, 2001). Altogether, these studies point to important regulatory roles of temperature for viral infection.…”

The mutual interplay between calcification and coccolithovirus infection

“…). Both naked strains, CCMP374 and CCMP1516, were highly sensitive to EhV86 infection, consistent with previous observations (Schroeder et al ., ; Bidle et al ., ; Vardi et al ., ; Bidle and Kwityn, ; Fulton et al ., ; Kendrick et al ., ) with cell abundance declining within 48–72 h post infection (hpi) concomitant with high levels of virus production (~ 9 × 10 8 viruses ml −1 ). Consequently, these naked strains served as positive controls for sensitivity to infection.…”

“…Calcification of CCMP374 also significantly impacted infection dynamics. Naked CCMP374 has been shown in the lab to be highly susceptible to infection with lysis occurring with 48-72 hpi Bidle et al, 2007;Vardi et al, 2009;Bidle and Kwityn, 2012;Fulton et al, 2014;Kendrick et al, 2014). Calcified CCMP374 showed severely delayed infection dynamics with cells continuing to grow through 96 hpi (Supporting Information Fig.…”