Endogenous parvoviral elements in the pit viper (Protobothrops mucrosuamatus) and in three members of three mammalian orders: implications for ecology and evolution of genera Amdoparvovirus and Protoparvovirus.

Abstract

Amdoparvoviruses (family Parvoviridae: genus Amdoparvovirus) infect carnivores, and are a major cause of morbidity and mortality in farmed mink. Relatively little is known about amdoparvovirus evolution, partly because so few endogenous parvoviral elements (PVe) derived from amdoparvovirus-like viruses have been identified. In this study, we systematically screened animal genomes to identify PVe disclosing a high degree of similarity to amdoparvoviruses, and investigated their genomic, phylogenetic and protein structural features. We report the first full-length, amdoparvovirus-derived PVe in the genome of the Transcaucasian mole vole (Ellobius lutescens). Furthermore, we identify four further PVe in mammal and reptile genomes that are intermediate between amdoparvoviruses and protoparvoviruses (genus Protoparvovirus) in terms of their phylogenetic placement and genomic features. In particular, we identified a genome-length PVe in the genome of a pit viper (Protobothrops mucrosquamatus) that is protoparvovirus-like in terms of its phylogenetic placement and the structural features of its capsid protein (as revealed by homology modeling), but exhibits characteristically amdoparvovirus-like features including (i) a putative middle ORF gene, and (ii) the lack of the phospholipase A2 (PLA2) domain as well as (iii) the putative transcription of VP1. These findings indicate that either: (i) amdoparvoviruses evolved from protoparvoviruses via a series of transitional forms, or; (ii) there are as yet uncharacterised parvovirus lineages that possess a mixture of proto- and amdoparvovirus-like characteristics. Our investigation also provides evidence that amdoparvovirus host range has extended to rodents in the past, and that reptilian parvoviruses exist outside of genus Dependoparvovirus. Finally, we show that PVe in the mole vole and pit viper encode intact, expressible replicase genes, adding to a growing body of evidence that these genes have repeatedly been co-opted or exapted in vertebrate genomes.