An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

Abstract

2Chapparvoviruses are a highly divergent group of parvoviruses (family 3 Parvoviridae) first identified in 2013. Interest in these poorly characterized 4 viruses has been raised by recent studies indicating that they are the cause of 5 chronic kidney disease that arises spontaneously in laboratory mice. In this 6 study, we investigate the biological and evolutionary characteristics of 7 chapparvoviruses via comparative analysis of genome sequence data. Our 8 analysis, which incorporates sequences derived from endogenous viral 9 elements (EVEs) as well as exogenous viruses, reveals that 10 chapparvoviruses are an ancient lineage within the family Parvoviridae, 11 clustering separately from members of both currently established parvoviral 12 subfamilies. Consistent with this, they exhibit a number of characteristic 13 genomic and structural features, i.e. a large number of putative auxiliary 14 protein-encoding genes, capsid protein genes non-homologous to any hitherto 15 parvoviral cap, as well as a putative capsid structure lacking the canonical fifth 16 strand of the ABIDG sheet comprising the luminal side of the jelly roll. Our 17 findings demonstrate that the chapparvovirus lineage infects an exceptionally 18 broad range of host species, including both vertebrates and invertebrates.19Furthermore, we observe that chapparvoviruses found in fish are more closely 20 related to those from invertebrates than they are to those that infect amniote 21 vertebrates. This suggests that transmission between distantly related host 22 species may have occurred in the past. Our study provides the first integrated 23 overview of the chapparvovirus group, and revises current views of parvovirus 24 evolution 25 26 AUTHOR SUMMARY 27 Chapparvoviruses are a recently identified group of viruses about 28 which relatively little is known. However, recent studies have shown that these 29 viruses cause disease in laboratory mice and are prevalent in the fecal virome 30 of pigs and poultry, raising interest in their potential impact as pathogens, and 31 utility as experimental tools. We examined the genomes of chapparvoviruses 32 and endogenous viral elements ('fossilized' virus sequences derived from 33 ancestral viruses) using a variety of bioinformatics-based approaches. We 3 1 show that the chapparvoviruses have an ancient origin and are evolutionarily 2 distinct from all other related viruses. Accordingly, their genomes and virions 3 exhibit a range of distinct characteristic features. We examine the distribution 4 of these features in the light of chapparvovirus evolutionary history (which we 5 can also infer from genomic data), revealing new insights into chapparvovirus 6 biology. 7 8

Comparative analysis reveals the long-term co-evolutionary history of parvoviruses and vertebrates

“…Orthologous copies of this element demonstrate that the association between hamaparvoviruses and vertebrates extends to the late Mesozoic Era >100 Mya, reinforces the view that this recently described subfamily is ancient and broadly distributed [46,47]. Among EPVs derived from subfamily Parvovirinae, the majority derived from two genera -Protoparvovirus and Dependoparvovirus.…”

Chapparvovirus DNA Found in 4% of Dogs with Diarrhea

“…A 210 amino acid ORF that is missing a start codon and is overlapping the NS1 ORF was also detected showing 57% identity to its homologue protein in mouse kidney parvovirus (AXX39021) [18] (Figure 1, panel A). This NP ORF is widely conserved among chapparvoviruses [19]. The 5’ UTR DNA sequence was 68% identical to that of the bat parvovirus sequence (MG693107.1)).…”

“…A close relative of murine chapparvovirus, initially reported in the feces of a wild Mus musculus from New York City [14], called murine kidney parvovirus (MH670588) was recently shown to cause nephropathy in immunocompromised laboratory mice [18]. A recent survey of eukaryotic genomes for chapparvovirus sequences has also shown the presence of a likely exogeneous chapparvovirus genome in a fish (Gulf pipefish or Syngnathus scovelli ) and of mostly defective germline sequences in another fish (Tiger tail seahorse or Hippocampus comes ) as well as in multiple invertebrates, indicating an ancient origin for chapparvoviruses [19]. A phylogenetic analysis of NS1 also indicated chapparvoviruses fall outside the traditional vertebrate-infecting Parvovirinae subfamily clade and closer to that of a subset of members of the subfamily Densovirinae [19].…”

Faecal Virome Analysis of Wild Animals from Brazil

“…Chapparvoviruses were also found in turkey, rat, Tasmanian devil, chicken, red-crowned crane, and mice faeces, rectal swab of pigs, in grey partridges, in Desmodus rotundus kidneys, and in faeces of animals of the present study [87,88,89,90,91,92,93,94]. Screening whole-genome shotgun (WGS) sequences assemblies, chapparvovirus endogenous viral elements (EVE) were identified in vertebrates and more recently in invertebrates [94,95]. This shows that Chapparvovirus has a wide range of host species and supports that vertebrate parvoviruses are not monophyletic as was commonly thought.…”