Intragenus competition between coccolithoviruses: an insight on how a select few can come to dominate many

Abstract

Viruses are a major cause of coccolithophore bloom demise in both temperate and sub-temperate oceanic regions. Most infection studies on coccolithoviruses have been conducted with a single virus strain, and the effect of intragenus competition by closely related coccolithoviruses has been ignored. Here we conducted combined infection experiments, infecting Emiliania huxleyi CCMP 2090 with two coccolithoviruses: EhV-86 and EhV-207 both simultaneously and independently. EhV-207 displayed a shorter lytic cycle and increased production potential than EhV-86 and was remarkably superior under competitive conditions. Although the viruses displayed identical adsorption kinetics in the first 2 h post infection, EhV-207 gained a numerical advantage as early as 8 h post infection. Quantitative polymerase chain reaction (PCR) revealed that when infecting in combination, EhV-207 was not affected by the presence of EhV-86, whereas EhV-86 was quickly out-competed, and a significant reduction in free and cell-associated EhV-86 was seen as early as 2 days after the initial infection. The observation of such clear phenotypic differences between genetically distinct, yet similar, coccolithovirus strains, by flow cytometry and quantitative real-time PCR allowed tentative links to the burgeoning genomic, transcriptomic and metabolic data to be made and the factors driving their selection, in particular to the de novo coccolithovirus-encoded sphingolipid biosynthesis pathway. This work illustrates that, even within a family, not all viruses are created equally, and the potential exists for relatively small genetic changes to infer disproportionately large competitive advantages for one coccolithovirus over another, ultimately leading to a few viruses dominating the many.

Coccolithoviruses: A Review of Cross-Kingdom Genomic Thievery and Metabolic Thuggery

“…Interestingly, significant differences have been observed in the infection dynamics of representative EhVs belonging to each phylogenetic clade identified in this study (Figure 1), both in respect to their lytic period [13] and their ability to utilize their host for the production of virally encoded glycosphingolipids, which are crucial for the successful demise of host cells [67]. …”

“…Because of E. huxleyi ’s global impact on biogeochemical cycles, the study of this host-virus system is particularly relevant. Interactions between E. huxleyi and EhVs have been investigated both in vivo, through large-scale semi-natural mesocosm experiments and natural E. huxleyi blooms [7,8,9,10,11], and in vitro [12,13,14,15,16], in laboratory experiments designed to elucidate specific aspects of the infection cycle, the infection dynamics and the host cellular response to infection [17]. …”

Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton

“…In the case of the Phycodnaviridae EhV, a virus of the coccolithophore Emiliania, it was noted that viral genomes were being overproduced during the infection cycle, relative to the number of capsids being produced by the infected phytoplankton (73). Such a discrepancy between genome and capsid productions may be linked to a shortage in amino acids and/or lipids, a constituent of EhV lipid membrane, limiting viral production (73,74).…”

“…Such a discrepancy between genome and capsid productions may be linked to a shortage in amino acids and/or lipids, a constituent of EhV lipid membrane, limiting viral production (73,74). This is predictable for Phycodnaviridae given the N requirements of PBCV1 capsid, which is composed of ∼5,050 major capsid proteins (MCPs) (75).…”

Change in Emiliania huxleyi Virus Assemblage Diversity but Not in Host Genetic Composition during an Ocean Acidification Mesocosm Experiment

“…Nissimov et al [41] investigated competition between the two EhVs, finding that EhV-207 had a competitive advantage over EhV-86. It would thus be of value to determine how external factors, such as elevated CO 2 , would affect relative competitive ability of EhVs; would EhV-207 still outcompete EhV-86?…”