Light regulation of coccolithophore host-virus interactions.

Kimberlee Thamatrakoln,Liti Haramaty,Ben Knowles,Christopher Maniscalco,Michael J Follows,Kay D Bidle,David Talmy,Frank Natale,Jason R Latham,Marco J L Coolen

doi:10.1111/nph.15459

Abstract

Viruses that infect photoautotrophs have a fundamental relationship with light, given the need for host resources. We investigated the role of light on Coccolithovirus (EhV) infection of the globally distributed coccolithophore, Emiliania huxleyi. Light was required for EhV adsorption, and viral production was highest when host cultures were maintained in continuous light or at irradiance levels of 150-300μmolm-2 s-1 . During the early stages of infection, photosynthetic electron transport remained high, while RuBisCO expression decreased concomitant with an induction of the pentose phosphate pathway, the primary source of de novo nucleotides. A mathematical model developed and fitted to the laboratory data supported the hypothesis that EhV replication was controlled by a trade-off between host nucleotide recycling and de novo synthesis, and that photoperiod and photon flux could toggle this switch. Laboratory results supported field observations that light was the most robust driver of EhV replication within E.huxleyi populations collected across a 2000 nautical mile transect in the North Atlantic. Collectively, these findings demonstrate that light can drive host-virus interactions through a mechanistic interplay between host metabolic processes, which serve to structure infection and phytoplankton mortality in the upper ocean.

Highlights

Virus infection is a primary mechanism of high lysis rates of phytoplankton populations (van Boekel et al, 1992; Bratbak et al, 1993; Brussaard et al, 1995; Valiela, 1995; Agustı et al, 1998)
Genes associated with de novo nucleotide synthesis, namely those involved in the phosphate pathway (PPP), were found to be upregulated during infection of E. huxleyi (Rosenwasser et al, 2014)
To determine whether these observed increases in transcript abundance translated into higher rates of nucleotide synthesis, we measured the enzymatic activity of key enzymes of the PPP during the early stages (< 24 hpi) of Emiliania huxleyi and its associated Coccolithovirus (EhV) infection

Summary

Introduction

Virus infection is a primary mechanism of high lysis rates of phytoplankton populations (van Boekel et al, 1992; Bratbak et al, 1993; Brussaard et al, 1995; Valiela, 1995; Agustı et al, 1998). Despite the impact on phytoplankton communities, viralinduced mortality is not routinely accounted for in models of ecosystem processes and carbon export, due to inadequate mechanistic and quantitative understanding of the environmental factors that regulate host–virus interactions. Emiliania huxleyi and its associated Coccolithovirus (EhV) is a highly studied marine eukaryotic algal host–virus model system due to its ecological relevance and the availability of genetically diverse hosts and EhV strains in culture (Schroeder et al, 2002; Bidle & Vardi, 2011).

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