Here, we introduce a new family of eukaryote-infecting single-stranded (ss) DNA viruses that was created recently by the International Committee on Taxonomy of Viruses (ICTV). The family, named Genomoviridae, contains a single genus, Gemycircularvirus, which currently has one recognized virus species, Sclerotinia gemycircularvirus 1. Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1 (SsHADV-1) is currently the sole representative isolate of the family; however, a great number of SsHADV-1-like ssDNA virus genomes has been sequenced from various environmental, plant- and animal-associated samples, indicating that members of family Genomoviridae are widespread and abundant in the environment.
Viruses with single-stranded DNA (ssDNA) genomes infect hosts in all three domains of life and include economically, medically, and environmentally important viral pathogens. Until recently, ssDNA viruses were classified into 10 different taxa—nine families and one genus not assigned to a family [14, 15]. In 2016, the International Committee on Taxonomy of Viruses (ICTV) created two new families for classification of ssDNA viruses, Pleolipoviridae and Genomoviridae . The family Pleolipoviridae includes viruses infecting hyperhalophilic archaea, and it has recently been described elsewhere . Here, we introduce the family Genomoviridae and provide a short overview of the properties of Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1 (SsHADV-1), the only cultivated member of the new family, and putative SsHADV-1-like viruses.
SsHADV-1 is the first—and thus far the only—ssDNA virus known to infect fungi (all other fungal viruses have RNA genomes) [10, 33]. SsHADV-1 was isolated from a plant-pathogenic fungus, Sclerotinia sclerotiorum . Another unique property of SsHADV-1 that has not been described for other fungal viruses is its ability to establish infection when applied extracellularly in the form of purified viral particles . Virions can infect the hyphae of virus-free S. sclerotiorum directly when applied to hyphae or sprayed on leaves of Arabidopsis thaliana and Brassica napus infected with S. sclerotiorum. When applied to S. sclerotiorum-infected leaves, the virus can suppress the development of S. sclerotiorum-induced lesions. SsHADV-1 has a narrow host range and, in addition to S. sclerotiorum, can infect the related species S. minor and S. nivalis, but not other relatively closely related fungi, such as Botrytis cinerea . Furthermore, SsHADV-1 has been identified in New Zealand and the USA in environmental samples and insects; however, this is not surprising given the near global distribution of S. sclerotiorum [6, 11].
SsHADV-1 virions are non-enveloped, isometric, 20-22 nm in diameter, and constructed from one capsid protein (CP) . The genome is a circular ssDNA molecule of 2,166 nucleotides and contains two genes – for CP and replication initiation protein (Rep) (Fig. 1). The prediction of the cp gene has been validated by N-terminal sequencing of the CP purified from the virions. The large intergenic region contains a potential stem-loop structure with a nonanucleotide (TAATATTAT) motif at its apex, which is likely to be important for rolling-circle replication. The CP of SsHADV-1 is not recognizably similar to the corresponding proteins from viruses in other taxa.
Although SsHADV-1 remains the only isolated member of the group, genomes of more than 100 SsHADV-1-like putative viruses have been reported (see Table 1). These genomes have been sequenced from different environmental samples, and many were identified associated with plant material as well as various animal-associated samples, including cerebrospinal fluid and blood of humans (Table 1 and references therein). Even though the hosts of these putative viruses remain unknown, their diversity suggests that SsHADV-1-like viruses are abundant and widespread in the environment.
All putative SsHADV-1-like viruses encode homologous Rep and CP, and in phylogenetic analyses form monophyletic clades with SsHADV-1 (Figures 2 and 3). Their genomes are of similar size, in the range of 2,089-2,290 nucleotides. Structural and genomic features of SsHADV-1 differ considerably from those of all other currently classified viruses. The Rep of SsHADV-1 is most closely related to the corresponding proteins of members of the family Geminiviridae. It shares with geminiviral proteins two conserved domains, namely geminivirus Rep catalytic domain (Gemini_AL1; PF00799) and geminivirus Rep protein central domain (Gemini_AL1_M; PF08283), with conserved motifs for rolling-circle replication. Notably, similar to some geminiviruses , certain SsHADV-1-like viruses also contain introns within their Rep-encoding genes [6, 7, 12, 13, 18, 19, 26–28, 30]. However, Rep-based phylogenetic analysis shows that SsHADV-1 and other related putative viruses form a well-supported, monophyletic clade, which branches as a sister group to geminiviruses (Fig. 2). Unlike the Rep, the CP of SsHADV-1 (and related viruses) does not display any recognizable sequence similarity to proteins of geminiviruses or any other group of known viruses. Furthermore, all geminiviruses possess distinctive geminate virions constructed from two incomplete T = 1 icosahedra [2, 36], whereas the virion of SsHADV-1 is isometric . Finally, the number of genes and size of the genome differ considerably between SsHADV-1-like viruses and geminiviruses. In particular, all putative SsHADV-1-like viruses lack the movement protein, which is essential for the plant geminiviruses.
In recognition of the unique features described above, SsHADV-1 has been classified into the species Sclerotinia gemycircularvirus 1 within the new genus Gemycircularvirus (Gemini-like myco-infecting circular virus)  within the new family Genomoviridae (sigil: Ge- for geminivirus-like, nomo- for no movement protein).
Although Genomoviridae currently includes only a single representative, new members, possibly including uncultivated viruses, are expected to be added to the family in the near future. Based on the available genetic data and phylogenetic analyses (Figures 2 and 3), it is already clear that many new genera will have to be introduced to adequately reflect the diversity of SsHADV-1-like viruses.
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The authors declare that no competing interests exist. This article does not contain any studies with human participants or animals performed by any of the authors.
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Krupovic, M., Ghabrial, S.A., Jiang, D. et al. Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol 161, 2633–2643 (2016). https://doi.org/10.1007/s00705-016-2943-3
- Capsid Protein
- Monophyletic Clade
- Fungal Virus
- Replication Initiation Protein
- ssDNA Virus