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

Abstract

Coccolithoviruses (Phycodnaviridae) infect and lyse the most ubiquitous and successful coccolithophorid in modern oceans, Emiliania huxleyi. So far, the genomes of 13 of these giant lytic viruses (i.e., Emiliania huxleyi viruses—EhVs) have been sequenced, assembled, and annotated. Here, we performed an in-depth comparison of their genomes to try and contextualize the ecological and evolutionary traits of these viruses. The genomes of these EhVs have from 444 to 548 coding sequences (CDSs). Presence/absence analysis of CDSs identified putative genes with particular ecological significance, namely sialidase, phosphate permease, and sphingolipid biosynthesis. The viruses clustered into distinct clades, based on their DNA polymerase gene as well as full genome comparisons. We discuss the use of such clustering and suggest that a gene-by-gene investigation approach may be more useful when the goal is to reveal differences related to functionally important genes. A multi domain “Best BLAST hit” analysis revealed that 84% of the EhV genes have closer similarities to the domain Eukarya. However, 16% of the EhV CDSs were very similar to bacterial genes, contributing to the idea that a significant portion of the gene flow in the planktonic world inter-crosses the domains of life.

Biochemical diversity of glycosphingolipid biosynthesis as a driver of Coccolithovirus competitive ecology

“…Taken together with field data showing entrainment of fast viruses at depth (Fig. S10), the 'differential removal' model supports enhanced removal of virulent strains from the upper ocean and implicates them in the enhanced production of TEP, particle aggregation and sinking flux (Laber et al, 2018;Nissimov et al, 2018).…”

“…The more rapid, virulent infection dynamics of EhV207 supports previous findings in which it outcompeted EhV86 in simultaneous laboratory infection experiments (Nissimov et al ., ) and are consistent with early (2–4 hpi) upregulation of SPT gene transcripts in E. huxleyi cells infected with EhV201 (Ziv et al ., ), the closest phylogenetic relative to EhV207 (Fig. B) (Nissimov et al ., ).…”

“…The rationale for this approach was several fold. First, EhV infection induces the production of sticky transparent exopolymeric particles (TEP), enhancing aggregate formation of infected cells and facilitating downward flux in natural populations in the North Atlantic (Vardi et al, 2012;Laber et al, 2018;Nissimov et al, 2018); this phenomenon is accentuated in fastinfecting EhV207 and occurs early in infection, absent of lysis (Nissimov et al, 2018). Second, we observed an enrichment of EhV207-like SPT linker amplicons in sinking biomass collected at 150 m at 5 of seven CTD cast stations ( Fig.…”

“…1B). All sequenced EhV genomes to date encode genes for sphingolipid biosynthesis with 11 of the 13 containing the linker sequence (Nissimov et al, 2017). Oligonucleotide primers targeting this region successfully amplify natural EhV populations in the North Atlantic and South Atlantic oceans (Nissimov et al, 2013) and do not amplify host-derived SPTs (Fig.…”

Dynamics of transparent exopolymer particle production and aggregation during viral infection of the coccolithophore, Emiliania huxleyi

“…Likewise, EhVs range in their relative virulence and infectivity dynamics (Nissimov et al ., ). There are currently at least 13 sequenced EhV genomes in the public domain that provide a glimpse into the genomic potential of coccolithoviruses and into their evolutionary relationship with other members of the NCLDV family of algal viruses (Wilson et al ., 2005; 2009; Allen et al ., ; Dunigan et al ., ; Nissimov et al ., 2011a,b; 2012a,b; 2014; 2017; Pagarete et al ., ). This makes E. huxleyi and its EhVs an ideal platform for investigating some of the ecological interactions that drive biogeochemical processes.…”