Genome and Environmental Activity of a Chrysochromulina parva Virus and Its Virophages

Abstract

Some giant viruses are ecological agents that are predicted to be involved in the top-down control of single-celled eukaryotic algae populations in aquatic ecosystems. Despite an increased interest in giant viruses since the discovery and characterization of Mimivirus and other viral giants, little is known about their physiology and ecology. In this study, we characterized the genome and functional potential of a giant virus that infects the freshwater haptophyte Chrysochromulina parva , originally isolated from Lake Ontario. This virus, CpV-BQ2, is a member of the nucleo-cytoplasmic large DNA virus (NCLDV) group and possesses a 437 kb genome encoding 503 ORFs with a GC content of 25%. Phylogenetic analyses of core NCLDV genes place CpV-BQ2 amongst the emerging group of algae-infecting Mimiviruses informally referred to as the “extended Mimiviridae ,” making it the first virus of this group to be isolated from a freshwater ecosystem. During genome analyses, we also captured and described the genomes of three distinct virophages that co-occurred with CpV-BQ2 and likely exploit CpV for their own replication. These virophages belong to the polinton-like viruses (PLV) group and encompass 19–23 predicted genes, including all of the core PLV genes as well as several genes implicated in genome modifications. We used the CpV-BQ2 and virophage reference sequences to recruit reads from available environmental metatranscriptomic data to estimate their activity in fresh waters. We observed moderate recruitment of both virus and virophage transcripts in samples obtained during Microcystis aeruginosa blooms in Lake Erie and Lake Tai, China in 2013, with a spike in activity in one sample. Virophage transcript abundance for two of the three isolates strongly correlated with that of the CpV-BQ2. Together, the results highlight the importance of giant viruses in the environment and establish a foundation for future research on the physiology and ecology CpV-BQ2 as a model system for algal Mimivirus dynamics in freshwaters.

Metagenomic analysis of virus diversity and relative abundance in a eutrophic freshwater harbour

“…Further exploration and sequencing of virophage, polinton, PLV and transpoviron diversity is required to expand databases and improve accuracy of identification of these entities in metagenomic datasets. As a final comment on virophages, recent genome sequencing of a giant virus isolated from Lake Ontario revealed the presence of three putative virophages [67]. This giant virus and associated virophages infect the freshwater haptophyte Chrysochromulina parva ; the C. parva virus is a close relative to the Hamilton Harbour mimivirus contigs annotated as Chrysochromulina ericinia virus.…”

The “Neglected Viruses” of Taihu: Abundant Transcripts for Viruses Infecting Eukaryotes and Their Potential Role in Phytoplankton Succession

“…All reference proteins used to reconstruct phylogenies came from viruses that have been isolated in labs and sequenced, with the exception of some virophage sequences. Mavirus, Sputnik, and Zamilon remain the only virophage that have been isolated, purified and sequenced to date (La Scola et al, 2008;Fischer and Suttle, 2011;Gaia et al, 2014), while three Chrysochromulina parva Virus Virophages (CpVVs denoted Curly, Larry, and Moe) have been isolated but not purified beyond unialgal lysates (Stough et al, 2019). Several intact virophage have been assembled from metagenomic analyses and were employed here to make our phylogenetics more robust (Zhou et al, 2013(Zhou et al, , 2015.…”

Polinton-like viruses and virophages are widespread in aquatic ecosystems

“…Additionally, 78% of viruses from the CHI group (n=32) also contained a chitinase gene (Table S5). In terms of the known PLVs, network analysis confirmed the PgVV group which included PgVV and the C. parva virus virophages 11 (Table 1), all of which share the same MCP protein cluster (PC_0089) and are associated with giant viruses infecting haptophytes ( Table 1). No Gossenköllesee viruses fell into the PgVV cluster, however several viruses from global metagenomes were included.…”

“…Similarly, 61 viruses in our dataset, across all virus groups (apart from the S. Punctatus and CHI groups) contained a predicted E3 ubiquitin-protein ligase. E3 ligases are known to counter host immune defenses in vertebrate viruses 27 , they have previously been detected in one other PLV 11 . Interestingly, there was a further group of 12 virophages from VC_34 which encoded a Cas4-like nuclease (Figure 2).…”

“…The recent discovery of ca. 25 Polinton-Like Virus (PLV) genomes 3,10,11 has revealed a further group of related and presumed algal viruses, with several being associated with, or even integrated into, giant virus genomes which infect algae 10,11 . Only one PLV, Tetraselmis striata virus (originally named Tetraselmis viridis virus) 12 has been observed as a virus particle, the remainder were discovered in sequencing projects or database searches based on the novel capsid gene of an unusual giant virus associated element, Phaeocystis globosa virus virophage (PgVV) 3 .…”