Insights into circovirus host range from the genomic fossil record

Abstract

A diverse range of DNA sequences derived from circoviruses (family Circoviridae) have been identified in samples obtained from humans and domestic animals, often in association with pathological conditions. In the majority of cases, however, little is known about the natural biology of the viruses from which these sequences are derived.Endogenous circoviral elements (CVe) are DNA sequences derived from circoviruses that occur in animal genomes and provide a useful source of information about circovirus-host relationships. In this study we screened genome assemblies of 675 animal species and identified numerous circovirus-related sequences, including the first examples of CVe derived from cycloviruses. We confirmed the presence of these CVe in the germline of the elongate twig ant (Pseudomyrmex gracilis), thereby establishing that cycloviruses infect insects. We examined the evolutionary relationships between CVe and contemporary circoviruses, showing that CVe from ants and mites group relatively closely with cycloviruses in phylogenies. Furthermore, the relatively random interspersal of CVe from insect genomes with cyclovirus sequences recovered from vertebrate samples, suggested that contamination might be an important consideration in studies reporting these viruses. Our study demonstrates how endogenous viral sequences can inform metagenomics-based virus discovery. In addition, it raises doubts about the role of cycloviruses as pathogens of humans and other vertebrates. ImportanceAdvances DNA sequencing have dramatically increased the rate at which new viruses are being identified. However, the host species associations of most virus sequences identified in metagenomic samples are difficult to determine. Our analysis indicates that viruses proposed to infect vertebrates (in some cases being linked to human disease) may in fact be restricted to arthropod hosts. The detection of these sequences in vertebrate samples may reflect their widespread presence in the environment as viruses of parasitic arthropods.

Peer Review #2 of "Virus discovery in all three major lineages of terrestrial arthropods highlights the diversity of single-stranded DNA viruses associated with invertebrates (v0.1)"

“…We also note that there is a group of cycloviruses recovered from spiders and an insectivorous bat that seem intermediate between other cycloviruses and the circovirus clade ( Manuscript to be reviewed other invertebrates may help resolve phylogenetic relationships among members of the Circoviridae. Nevertheless, our phylogenetic analysis supports the idea that there are distinct groups of cycloviruses (Dennis et al 2018b).…”

“…All sequences outside of the established CRESS DNA families were grouped by organism (e.g., rodent associated sequences) and sequences within each group were clustered using a 70% amino acid identity cut off. In addition to sequences representing exogenous viruses and replicons, CRESS DNA-like endogenous viral sequences (CEVs) reported from various organisms were included (Dennis et al 2018a;Dennis et al 2018b;Liu et al 2011). Selected CEVs did not contain any early stop codons or frameshifts.…”

“…In addition, database searches using newly detected Reps led to the detection of an unreported endogenous cyclovirus-like element within a genome scaffold from a rodent-infecting nematode. Although cycloviruses have been mainly detected in feces from various mammals and homogenized tissues from insects (Rosario et al 2017), endogenous cyclovirus elements indicate that these viruses are able to infect both arthropod (mites) (Dennis et al 2018b;Liu et al 2011) and non-arthropod parasitic invertebrates.…”

Prevalence of a vertically transmitted single-stranded DNA virus in spinybacked orbweavers (Gasteracantha cancriformis) from Florida, USA

“…Although spiders harbor a diversity of viruses, there is scarce information regarding the prevalence and ecological impact of viral infection in spiders. Endogenous viral sequences within spider chromosomes indicate that these arachnids have been infected by both CRESS DNA viruses and double-stranded DNA polyomaviruses [19,20]. Studies within the past four years have also revealed a diversity of novel extant viruses in multiple spider species, including more than 20 CRESS DNA [2] and 100 RNA viruses [21][22][23][24] encompassing various viral families and unclassified species.…”

Conformational Dynamics of Nonenveloped Circovirus Capsid to the Host Cell Receptor

“…Circovirus is the smallest nonenveloped icosahedral virus, with a circular, single-stranded genomic DNA, which infects a variety of species ranging from animals to plants with different pathogenicities (20). PCV2, with an unique structural capsid protein, is a representative circovirus that causes significant morbidity and mortality in swine (21–23).…”