Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes

Abstract

The genomes of numerous circoviruses and distantly related circular DNA viruses encoding a rolling circle replication initiator protein (Rep) have been characterized from the tissues of mammals, fish, insects, and plants (geminivirus and nanovirus), human and animal feces, in an algae cell, and in diverse environmental samples. We review the genome organization, phylogenetic relationships and initial prevalence studies of cycloviruses, a proposed new genus in the Circoviridae family. Viral fossil rep sequences were also identified integrated on the chromosomes of mammals, frogs, lancelets, crustaceans, mites, gastropods, roundworms, placozoans, hydrozoans, protozoans, land plants, fungi, algae, and phytoplasma bacterias and their plasmids, reflecting their past host range. An ancient origin for viruses with rep-encoding single stranded small circular genomes, predating the diversification of eukaryotes, is discussed. The cellular hosts and pathogenicity of many recently described rep-containing circular genomes remain to be determined. Future studies of the virome of single cell and multi-cellular eukaryotes are likely to further extend the known diversity and host-range of small rep-containing circular viral genomes.

Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses

“…However, once the CP and the RC-Rep genes are sufficiently adapted to each other (that is, further 'sampling' decreases fitness) and/or viruses occupy a specific niche where 'sampling' is no longer possible, such high rate of gene exchange is expected to transit to a more conservative mode observed in other eukaryotic ssDNA viruses. Metagenomic studies have recently uncovered the unsuspected diversity of ssDNA viruses, many of which encode RC-Reps similar to those of geminiviruses, nanoviruses and, perhaps most commonly, circoviruses 17,18 . However, their CP genes are typically beyond recognition using sequence-based approaches, opening a possibility that these uncultured viruses represent highly divergent yet genuine members of the corresponding viral families.…”

“…A characteristic feature of RC-Reps of eukaryotic ssDNA viruses is the presence of the superfamily 3 helicase (S3H) domain 16,17 , which is fused carboxy-terminally to the catalytic nuclease domain encompassing three signature motifs found in all prokaryotic and eukaryotic virus and plasmid RC-Reps 14 . As opposed to CPs, RC-Reps of eukaryotic viruses display actual sequence similarity and RC-Rep-based phylogenies recapitulate the major taxonomic groups defined by the International Committee on Taxonomy of Viruses 1,18,19 . However, it should be noted that not all eukaryotic ssDNA viruses possess genes for canonical RC-Reps; for example, anelloviruses-even though believed to replicate via RC mechanism-do not encode a protein that would contain the entire set of motifs characteristic to RC-Reps 17 .…”

Potential role of viruses in white plague coral disease

“…The host for the coral-associated SCSDVs presented here is yet to be determined, but may include the algal endosymbiont (Symbiodinium spp., because nanovirus/geminiviruses infect plants), the coral host itself (because circoviruses infect animals), or another member of the coral holobiont (Yu et al, 2010;Delwart and Li, 2012;Rosario et al, 2012;). However, a previous study examining viruses associated with Montastraea cavernosa coral colonies searched Symbiodinium EST libraries and found few similarities to SCSDVs suggesting that the SCSDVs associated with diseased corals in this study are infecting the coral animal.…”

“…The Rep initiator protein was selected as a marker because of its evolutionary conservation in all SCSDVs and their associated satellite DNAs (Ilyina and Koonin, 1992;Gibbs and Weiller, 1999;Martin et al, 2011;Delwart and Li, 2012). METAVIR conducts the following steps to construct phylogenetic comparisons:…”

Plant paleopathology and the roles of pathogens and insects

“…For viruses, although experimental evidence indicates that silicification is possible (Ladier and Stedman, 2010;Orange et al, 2011), and molecular phylogenetic studies suggest deeptime origins (Delwart and Li, 2012), there is no indication of a fossil record until the Early Cretaceous. Interestingly, these Cretaceous virus fossils occur in association with insects preserved in amber (Poinar and Poinar, 2005).…”