Four principles to establish a universal virus taxonomy.

A universal taxonomy of viruses is essential for a comprehensive view of the virus world and for communicating the complicated evolutionary relationships among viruses. However, there are major differences in the conceptualisation and approaches to virus classification and nomenclature among virologists, clinicians, agronomists, and other interested parties. Here, we provide recommendations to guide the construction of a coherent and comprehensive virus taxonomy, based on expert scientific consensus. Firstly, assignments of viruses should be congruent with the best attainable reconstruction of their evolutionary histories, i.e., taxa should be monophyletic. This fundamental principle for classification of viruses is currently included in the International Committee on Taxonomy of Viruses (ICTV) code only for the rank of species. Secondly, phenotypic and ecological properties of viruses may inform, but not override, evolutionary relatedness in the placement of ranks. Thirdly, alternative classifications that consider phenotypic attributes, such as being vector-borne (e.g., "arboviruses"), infecting a certain type of host (e.g., "mycoviruses," "bacteriophages") or displaying specific pathogenicity (e.g., "human immunodeficiency viruses"), may serve important clinical and regulatory purposes but often create polyphyletic categories that do not reflect evolutionary relationships. Nevertheless, such classifications ought to be maintained if they serve the needs of specific communities or play a practical clinical or regulatory role. However, they should not be considered or called taxonomies. Finally, while an evolution-based framework enables viruses discovered by metagenomics to be incorporated into the ICTV taxonomy, there are essential requirements for quality control of the sequence data used for these assignments. Combined, these four principles will enable future development and expansion of virus taxonomy as the true evolutionary diversity of viruses becomes apparent.

2024 Smacoviridae family update: 59 new species in seven genera.

Family Smacoviridae (order Cremevirales, class Arfiviricetes, phylum Cressdnaviricota) comprises viruses with small circular genomes of ~2300-3000 nt in length that encode at least two proteins, the rolling-circle replication associated protein (Rep) and the capsid protein (CP). Smacovirids have been discovered in fecal samples of various animals and display remarkable sequence diversity. Here, we provide an overview of the genomic properties of classified smacovirids and report on the latest taxonomy update in the family Smacoviridae. The family has been expanded by 59 new species in the genera Porprismacovirus (n = 25), Inpeasmacovirus (n = 1), Felismacovirus (n = 22), Drosmacovirus (n = 4), Dragsmacovirus (n = 2), Bovismacovirus (n = 4), and Bonzesmacovirus (n = 1) and currently includes 12 genera with 143 species officially recognized by the International Committee on Taxonomy of Viruses (ICTV).

New duck papillomavirus type identified in a mallard in Missouri, USA.

Papillomaviruses are small circular DNA viruses that infect epithelial and mucosal cells and have co-evolved with their hosts. Some papillomaviruses in mammals are well studied (especially those associated with disease). However, there is limited information on papillomaviruses associated with avian hosts. From a cloacal swab sample of a mallard (Anas platyrhynchos) sampled in Missouri, USA (6 Jan 2023), we identified a papillomavirus (7839 nt) that shares ~68% genome-wide nucleotide sequence identity with Anas platyrhynchos papillomavirus 1 (AplaPV1) from a mallard sampled in Newfoundland (Canada) and ~40% with AplaPV2 from a mallard sampled in Minnesota (USA) with mesenchymal dermal tumors. The papillomavirus we identified shares 73.6% nucleotide sequence identity in the L1 gene with that of AplaPV1 and thus represents a new AplaPV type (AplaPV3). The genome sequence of AplaPV3 shares >97% identity with three partial PV genome sequences (1316, 1997, and 4241 nt) identified in a mallard in India, indicating that that virus was also AplaPV3.

2024 taxonomy update for the family Circoviridae.

Circovirids have a circular single-stranded DNA genome packed into a small icosahedral capsid. They are classified within two genera, Circovirus and Cyclovirus, in the family Circoviridae (phylum Cressdnaviricota, class Arfiviricetes, order Cirlivirales). Over the last five years, a number of new circovirids have been identified, and, as a result, 54 new species have been created for their classification based on the previously established species demarcation criterion, namely, that viruses classified into different species share less than 80% genome-wide pairwise sequence identity. Of note, one of the newly created species includes a circovirus that was identified in human hepatocytes and suspected of causing liver damage. Furthermore, to comply with binomial species nomenclature, all new and previously recognized species have been (re)named in binomial format with a freeform epithet. Here, we provide a summary of the properties of circovirid genomes and their classification as of June 2024 (65 species in the genus Circovirus and 90 species in the genus Cyclovirus). Finally, we provide reference datasets of the nucleotide and amino acid sequences representing each of the officially recognized circovirid species to facilitate further classification of newly discovered members of the Circoviridae.

Genome analysis of gyroviruses identified in waterfowl in Arizona (USA).

Gyroviruses are small single-stranded DNA (ssDNA) viruses that are largely associated with birds. Chicken anemia virus is the most extensively studied gyrovirus due to its disease impact on the poultry industry. However, we know much less about gyroviruses infecting other avian species. To investigate gyroviruses infecting waterfowl, we determined six complete genome sequences that fall into three gyrovirus groups, referred to as waterfowl gyrovirus 1 (n = 3), 2 (n = 2), and 3 (n = 1), in organs from hunter-harvested waterfowl from Arizona (USA). The waterfowl gyrovirus 1 variants were identified in multiple organs of a single American wigeon and represent a tentative new species. The waterfowl gyrovirus 2 variants were identified in the livers of two American wigeons and share >70% VP1 nucleotide sequence identity with gyrovirus 9, previously identified in the spleen of a Brazilian Pekin duck (MT318123) and a human fecal sample (KP742975). Waterfowl gyrovirus 3 was identified in a northern pintail spleen sample, and it shares >73% VP1 nucleotide sequence identity with two gyrovirus 13 sequences previously identified in Brazilian Pekin duck spleens (MT318125 and MT318127). These gyroviruses are the first to be identified in waterfowl in North America, as well as in American wigeons and northern pintails.

Detection and molecular characterization of a novel mitovirus associated with Passiflora edulis Sims.

Mitoviruses are cryptic capsidless viruses belonging to the family Mitoviridae that replicate and are maintained in the mitochondria of fungi. Complete mitovirus-like sequences were recently assembled from plant transcriptome data and plant leaf tissue samples. Passion fruit (Passiflora spp.) is an economically important crop for numerous tropical and subtropical countries worldwide, and many virus-induced diseases impact its production. From a large-scale genomic study targeting viruses infecting Passiflora spp. in Brazil, we detected a de novo-assembled contig with similarity to other plant-associated mitoviruses. The contig is ∼2.6 kb long, with a single open reading frame (ORF) encoding an RNA-dependent RNA polymerase (RdRP). This contig has been named "passion fruit mitovirus-like 1" (PfMv1). An alignment of the predicted amino acid sequence of the RdRP of PfMv1 and those of other plant-associated mitoviruses revealed the presence of the six conserved motifs of mitovirus RdRPs. PfMv1 has 79% coverage and 50.14% identity to Humulus lupulus mitovirus 1. Phylogenetic analysis showed that PfMV1 clustered with other plant-associated mitoviruses in the genus Duamitovirus. Using RT-PCR, we detected a PfMv1-derived fragment, but no corresponding DNA was identified, thus excluding the possibility that this is an endogenized viral-like sequence. This is the first evidence of a replicating mitovirus associated with Passiflora edulis, and it should be classified as a member of a new species, for which we propose the name "Duamitovirus passiflorae".

Virus taxonomy and the role of the International Committee on Taxonomy of Viruses (ICTV).

The taxonomy of viruses is developed and overseen by the International Committee on Taxonomy of Viruses (ICTV), which scrutinizes, approves and ratifies taxonomic proposals, and maintains a list of virus taxa with approved names (https://ictv.global). The ICTV has approximately 180 members who vote by simple majority. Taxon-specific Study Groups established by the ICTV have a combined membership of over 600 scientists from the wider virology community; they provide comprehensive expertise across the range of known viruses and are major contributors to the creation and evaluation of taxonomic proposals. Proposals can be submitted by anyone and will be considered by the ICTV irrespective of Study Group support. Thus, virus taxonomy is developed from within the virology community and realized by a democratic decision-making process. The ICTV upholds the distinction between a virus or replicating genetic element as a physical entity and the taxon category to which it is assigned. This is reflected by the nomenclature of the virus species taxon, which is now mandated by the ICTV to be in a binomial format (genus + species epithet) and is typographically distinct from the names of viruses. Classification of viruses below the rank of species (such as, genotypes or strains) is not within the remit of the ICTV. This article, authored by the ICTV Executive Committee, explains the principles of virus taxonomy and the organization, function, processes and resources of the ICTV, with the aim of encouraging greater understanding and interaction among the wider virology community.

Identification and characterization of a polyomavirus in the thornback skate (Raja clavata).

Members of the family Polyomaviridae have a circular double-stranded DNA genome that have been identified in various hosts ranging from mammals to arachnids. Here we report the identification and analysis of a complete genome sequence of a novel polyomavirus, Raja clavata polyomavirus (RcPyV1), from a cartilaginous fish, the thornback skate (Raja clavata). The genome sequence was determined using a metagenomics approach with an aim to provide baseline viral data in cartilaginous fish in different ecosystems. The RcPyV1 genome (4,195 nucleotides) had typical organization of polyomavirus, including early antigens (small T; Large T) encoded on one strand and late viral proteins (VP1; VP2) on the complementary strand. Maximum-likelihood phylogenetic analysis of the large T-antigen revealed that RcPyV1 clusters with a polyomavirus obtained from another cartilaginous fish, the guitarfish polyomavirus 1 (GfPyV1). These two share ~ 56% pairwise identity in LT and VP1 protein sequences. These analyses support the hypothesis that cartilaginous fishes have a specific lineage of polyomaviruses.

Anelloviridae taxonomy update 2023.

The family Anelloviridae comprises negative single-stranded circular DNA viruses. Within this family, there are 30 established genera. Anelloviruses in the genus Gyrovirus have been identified infecting various avian species, whereas those in the remaining 29 genera have been found primarily infecting various mammal species. We renamed the 146 anellovirus species with binomial species names, as required by the International Committee on Taxonomy of Viruses (ICTV) using a "genus + freeform epithet" format.

A circovirus and cycloviruses identified in feces of bobcats (Lynx rufus) in California.

Viruses in the family Circoviridae have small circular single-stranded DNA (ssDNA) genomes. Circoviruses are known to infect a wide variety of animals, with notable disease pathology in psittacine (psittacine beak and feather disease) and porcine (postweaning multisystemic wasting syndrome) species. There is still a dearth of research investigating circoviruses associated with felid species. In six fecal samples collected from bobcats (Lynx rufus) in California from 2010 to 2011, we identified six viruses belonging to the genera Circovirus (n = 1) and Cyclovirus (n = 5), using a high-throughput-sequencing-based approach. Of these, the virus in the genus Circovirus represents a new species, as it shares only 54-60% genome-wide sequence identity with the other members of this genus. The five viruses in the genus Cyclovirus represent three new species, sharing <73% genome-wide sequence identity with all other cycloviruses. Three of the cycloviruses belong to a single putative species and were obtained from the feces of three individual bobcats, sharing 95.7-99.9% sequence identity, whereas the other two unique cycloviruses were identified in a single fecal sample. At present, it is unknown whether the identified viruses infect bobcats, their prey, or their gut parasites.

Identification of small circular DNA viruses in coyote fecal samples from Arizona (USA).

Coyotes (Canis latrans) have a broad geographic distribution across North and Central America. Despite their widespread presence in urban environments in the USA, there is limited information regarding viruses associated with coyotes in the USA and in particular the state of Arizona. To explore viruses associated with coyotes, particularly small DNA viruses, 44 scat samples were collected (April-June 2021 and November 2021-January 2022) along the Salt River near Phoenix, Arizona (USA), along 43 transects (500 m). From these samples, we identified 11 viral genomes: two novel circoviruses, six unclassified cressdnaviruses, and two anelloviruses. One of the circoviruses is most closely related to a circovirus sequence identified from an aerosolized dust sample in Arizona, USA. The second circovirus is most closely related to a rodent-associated circovirus and canine circovirus. Of the unclassified cressdnaviruses, three encode replication-associated proteins that are similar to those found in protists (Histomonas meleagridis and Monocercomonoides exilis), implying an evolutionary relationship with or a connection to similar unidentified protist hosts. The two anelloviruses are most closely related to those found in rodents, and this suggests a diet-related identification.

Novel polyomaviruses identified in fecal samples from four carnivore species.

Polyomaviruses are oncogenic viruses that are generally thought to have co-evolved with their hosts. While primate and rodent polyomaviruses are increasingly well-studied, less is known about polyomaviruses that infect other mammals. In an effort to gain insight into polyomaviruses associated with carnivores, we surveyed fecal samples collected in the USA from bobcats (Lynx rufus), pumas (Puma concolor), Canada lynxes (Lynx canadensis), and grizzly bears (Ursus arctos). Using a viral metagenomic approach, we identified six novel polyomavirus genomes. Surprisingly, four of the six genomes showed a phylogenetic relationship to polyomaviruses found in prey animals. These included a putative rabbit polyomavirus from a bobcat fecal sample and two possible deer-trophic polyomaviruses from Canada lynx feces. One polyomavirus found in a grizzly bear sample was found to be phylogenetically distant from previously identified polyomaviruses. Further analysis of the grizzly bear fecal sample showed that it contained anelloviruses that are known to infect pigs, suggesting that the bear might have preyed on a wild or domestic pig. Interestingly, a polyomavirus genome identified in a puma fecal sample was found to be closely related both to raccoon polyomavirus 1 and to Lyon-IARC polyomavirus, the latter of which was originally identified in human saliva and skin swab specimens but has since been found in samples from domestic cats (Felis catus).

Identification of a novel polyomavirus in wild Sonoran Desert rodents of the family Heteromyidae.

Rodents are the largest and most diverse group of mammals. Covering a wide range of structural and functional adaptations, rodents successfully occupy virtually every terrestrial habitat, and they are often found in close association with humans, domestic animals, and wildlife. Although a significant amount of research has focused on rodents' prominence as known reservoirs of zoonotic viruses, there has been less emphasis on the viral ecology of rodents in general. Here, we utilized a viral metagenomics approach to investigate polyomaviruses in wild rodents from the Baja California peninsula, Mexico, using fecal samples. We identified a novel polyomavirus in fecal samples from two rodent species, a spiny pocket mouse (Chaetodipus spinatus) and a Dulzura kangaroo rat (Dipodomys simulans). These two polyomaviruses represent a new species in the genus Betapolyomavirus. Sequences of this polyomavirus cluster phylogenetically with those of other rodent polyomaviruses and two other non-rodent polyomaviruses (WU and KI) that have been identified in the human respiratory tract. Through our continued work on seven species of rodents, we endeavor to explore the viral diversity associated with wild rodents on the Baja California peninsula and expand on current knowledge of rodent viral ecology and evolution.

Changes to virus taxonomy and the ICTV Statutes ratified by the International Committee on Taxonomy of Viruses (2023).

This article reports changes to virus taxonomy and taxon nomenclature that were approved and ratified by the International Committee on Taxonomy of Viruses (ICTV) in April 2023. The entire ICTV membership was invited to vote on 174 taxonomic proposals that had been approved by the ICTV Executive Committee in July 2022, as well as a proposed revision of the ICTV Statutes. All proposals and the revised ICTV Statutes were approved by a majority of the voting membership. Of note, the ICTV continued the process of renaming existing species in accordance with the recently mandated binomial format and included gene transfer agents (GTAs) in the classification framework by classifying them as viriforms. In total, one class, seven orders, 31 families, 214 genera, and 858 species were created.

Guidance for creating individual and batch latinized binomial virus species names.

The International Committee on Taxonomy of Viruses recently adopted, and is gradually implementing, a binomial naming format for virus species. Although full Latinization of these names remains optional, a standardized nomenclature based on Latinized binomials has the advantage of comparability with all other biological taxonomies. As a language without living native speakers, Latin is more culturally neutral than many contemporary languages, and words built from Latin roots are already widely used in the language of science across the world. Conversion of established species names to Latinized binomials or creation of Latinized binomials de novo may seem daunting, but the rules for name creation are straightforward and can be implemented in a formulaic manner. Here, we describe approaches, strategies and steps for creating Latinized binomials for virus species without prior knowledge of Latin. We also discuss a novel approach to the automated generation of large batches of novel genus and species names. Importantly, conversion to a binomial format does not affect virus names, many of which are created from local languages.

Naryaviridae, Nenyaviridae, and Vilyaviridae: three new families of single-stranded DNA viruses in the phylum Cressdnaviricota.

The phylum Cressdnaviricota includes viruses with circular single-stranded DNA (ssDNA) genomes and icosahedral capsids. These viruses display global environmental distribution and infect diverse eukaryotic hosts, including animals, plants, and fungi. Here, we report on the formal creation of two new orders, Rivendellvirales and Rohanvirales, and three new families, Naryaviridae, Nenyaviridae, and Vilyaviridae, of ssDNA viruses associated with protozoan parasites belonging to the genera Entamoeba and Giardia. We describe a sequence-based taxonomic framework, which was used to classify 60 ssDNA viruses into 12 genera (with 18 species) within the family Vilyaviridae; four genera (with five species) within the family Naryaviridae; and five genera (with six species) within the family Nenyaviridae. We also highlight the challenges associated with the classification of chimeric virus genomes, such as those in the families Naryaviridae and Nenyaviridae, where the replication initiation and capsid protein genes have undergone several independent non-orthologous replacements. The described taxonomic changes have been ratified by the International Committee on Taxonomy of Viruses (ICTV) and expand the phylum Cressdnaviricota to eight orders and 11 families.

Molecular identification and phylogenetic characterization of A-strain isolates of maize streak virus from western Ethiopia.

The A-strain of maize streak virus (MSV) causes maize streak disease (MSD), which is a major biotic threat to maize production in sub-Saharan Africa. Previous studies have described different MSV strains of economic importance from southern and eastern African countries and how eastern African regions are hubs for MSV diversification. Despite these efforts, due to a lack of extensive sampling, there is limited knowledge about the MSV-A diversity in Ethiopia. Here, field sampling of maize plants and wild grasses with visible MSD symptoms was carried out in the western Ethiopian regions of Gambela, Oromia, and Benishangul-Gumuz during the maize-growing season of 2019. The complete genomes of MSV isolates (n = 60) were cloned and sequenced by the Sanger method. We used a model-based phylogenetic approach to analyse 725 full MSV genome sequences available in the GenBank database together with newly determined genome sequences from Ethiopia to determine their subtypes and identify recombinant lineages. Of the 127 fields accessed, MSD prevalence was highest, at 96%, in the Gambela region and lowest in Oromia, at 66%. The highest mean symptom severity of 4/5 (where 5 is the highest and 1 the lowest) was observed in Gambela and Benishangul-Gumuz. Our results show that these newly determined MSV isolates belong to recombinant lineage V of the A1 subtype, with the widest dissemination and greatest economic significance in sub-Saharan Africa and the adjacent Indian Ocean islands.

Establishment of five new genera in the family Geminiviridae: Citlodavirus, Maldovirus, Mulcrilevirus, Opunvirus, and Topilevirus.

Geminiviruses are plant-infecting, circular single-stranded DNA viruses that have a geminate virion morphology. These viruses infect both cultivated and non-cultivated monocotyledonous and dicotyledonous plants and have a wide geographical distribution. Nine genera had been established within the family Geminiviridae (Becurtovirus, Begomovirus, Capulavirus, Curtovirus, Eragrovirus, Grablovirus, Mastrevirus, Topocuvirus, and Turncurtovirus) as of 2020. In the last decade, metagenomics approaches have facilitated the discovery and identification of many novel viruses, among them numerous highly divergent geminiviruses. Here, we report the establishment of five new genera in the family Geminiviridae (Citlodavirus, Maldovirus, Mulcrilevirus, Opunvirus, and Topilevirus) to formally classify twelve new, divergent geminiviruses.

Novel adenovirus associated with common tern (Sterna hirundo) chicks.

Adenoviruses have been identified in a wide variety of avian species, and in some species, they have been shown to cause disease and increase mortality. As part of an endeavor to investigate viruses associated with common terns (Sterna hirundo), a novel adenovirus was identified in fecal samples from two common terns on Gull Island, Lake Ontario, Canada. The coding-complete genome sequence of the new adenovirus is 31,094 bp, containing 28 putative genes, and this is the first adenovirus to be associated with terns. The virus was identified in two out of 13 fecal samples from tern chicks, and it was found to be most closely related to duck adenovirus 1, with the DNA polymerase sharing 58% amino acid sequence identity. Phylogenetic analysis based on DNA polymerase protein sequences showed that the new virus forms a distinct sub-branch within the atadenovirus clade and likely represents a new species in this genus.

Identification of diverse papillomaviruses in captive black-and-white ruffed lemurs (Varecia variegata).

Papillomaviruses (PVs) are host-species-specific and tissue-specific viruses that infect a diverse array of vertebrate hosts, including humans and non-human primates, with varying pathogenic outcomes. Although primate PVs have been studied extensively, no complete genome sequences of PVs from lemurs have been determined to date. Saliva samples from three critically endangered, captive black-and-white ruffed lemurs (Varecia variegata variegata) at the Duke Lemur Center (USA) were analyzed, using high-throughput sequencing, for the presence of oral papillomaviruses. We identified three PVs from two individuals, one of which had a coinfection with two different PVs. Two of the three PVs share 99.6% nucleotide sequence identity, and we have named these isolates "Varecia variegata papillomavirus 1" (VavPV1). The third PV shares ~63% nucleotide sequence identity with VavPV1, and thus, we have named it "Varecia variegata papillomavirus 2" (VavPV2). Based on their E1 + E2 + L1 protein sequence phylogeny, the VavPVs form a distinct clade. This clade likely represents a novel genus, with VavPV1 and VavPV2 belonging to two distinct species. Our findings represent the first complete genome sequences of PVs found in lemuriform primates, with their presence suggesting the potential existence of diverse PVs across the over 100 species of lemurs.