A new perspective on the evolution and diversity of the genus Amdoparvovirus (family Parvoviridae) through genetic characterization, structural homology modeling, and phylogenetics

Abstract

Amdoparvoviruses (genus Amdoparvovirus, family Parvoviridae) are primarily viruses of carnivorans, but recent studies have indicated that their host range might also extend to rodents and chiropterans. While their classification is based on the full sequence of the major non-structural protein (NS1), several studies investigating amdoparvoviral diversity have been focused on partial sequences, leading to difficulties in accurately determining species demarcations and leaving several viruses unclassified. In this study, while reporting the complete genomic sequence of a novel amdoparvovirus identified in an American mink (British Columbia amdoparvovirus, BCAV), we studied the phylogenetic relationships of all amdoparvovirus-related sequences and provide a comprehensive reevaluation of their diversity and evolution. After excluding recombinant sequences, phylogenetic and pairwise sequence identity analyses allowed us to define 14 different viruses, including the five currently classified species, BCAV, and four additional viruses that fulfill the International Committee on Taxonomy of Viruses (ICTV) criteria to be classified as species. We show that the group of viruses historically known as Aleutian mink disease virus (AMDV, species Carnivore amdoparvovirus 1) should be considered as a cluster of at least four separate viral species that have been co-circulating in mink farms, facilitating the occurrence of inter-species recombination. Genome organization, splicing donor and acceptor sites, and protein sequence motifs were surprisingly conserved within the genus. The sequence of the major capsid protein (VP2) was significantly more conserved between and within species compared to NS1, a phenomenon possibly linked to antibody-dependent enhancement (ADE). Homology models suggest a remarkably high degree of conservation of the spikes located near the icosahedral threefold axis of the capsid, comprising the surface region associated with ADE. A surprisingly high number of divergent amino acid positions were found in the luminal threefold and twofold axes of the capsid, regions of hitherto unknown function. We emphasize the importance of complete genome analyses and, given the marked phylogenetic inconsistencies across the genome, advise to obtain the complete coding sequences of divergent strains. Further studies on amdoparvovirus biology and structure as well as epidemiological and virus discovery investigations are required to better characterize the ecology and evolution of this important group of viruses.

First Report of Skunk Amdoparvovirus (Species Carnivore amdoparvovirus 4) in Europe in a Captive Striped Skunk (Mephitis mephitis)

“…Knowledge of the diversity of amdoparvoviruses has been greatly expanded in recent years, with several new species reported and the host range being possibly extended to bats and rodents [ 38 ]. This highlights the necessity for increased surveillance of potential reservoir species and further investigations into the diversity of amdoparvoviruses.…”

Capsid Structure of Aleutian Mink Disease Virus and Human Parvovirus 4: New Faces in the Parvovirus Family Portrait

“…Aleutian mink disease virus (AMDV) is a member of the genus Amdoparvovirus . Viruses of this genus primarily infect carnivores, as well as some rodents and bats [ 19 ]. AMDV is known to cause Aleutian disease, which results in the enlargement of the kidneys, the spleen, and the lymph nodes and manifests in deadly plasmacytosis and hyperglobulinemia [ 20 ].…”

Amdoparvovirus-associated disease in striped skunks (Mephitis mephitis)

“…Unique APV species have been identified from 5 carnivore species in the past 12 years, and among those studied, infection is highly prevalent and is associated with disease in a subset of animals. 2,4,5,12,18 AMDV has been detected in hosts other than mink, but we have no idea whether or how co-infections and/or host-switching influence clinical outcome. Comparisons of disease expression among hosts would benefit from pathogenesis studies that consider viral evolution and potential for viral spillover.…”

“…Specific PCR detection for SKAV species has been performed in a few studies, but given that we have only recently uncovered the high prevalence of SKAV, any unchallenged declaration of disease association based on PCR alone is precarious. 2,5 Molecular detection of SKAV from diseased tissue coupled with viral distribution by in situ hybridization (ISH) both establishes disease association and reveals mechanisms of pathogenesis such as tissue targets of infection and pathways for SKAV shedding and transmission.…”

“…Recent data demonstrates that this species harbors a phylogenetically distinct species called skunk amdoparvovirus (SKAV). 2,5 SKAV prevalence, estimated by detection in blood is remarkably high in all areas that have been tested (Canada, 86%, US 82%), but potential disease association, including the type and impact of disease, is unknown. 1,3,8,11 Most APVs, including SKAV, were discovered in the last decade, so disease association is further complicated by any literature prior to 2011 that could not distinguish among multiple potential viral species.…”