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A 2021 taxonomy update for the family Smacoviridae

Abstract

The family Smacoviridae (order Cremevirales, class Arfiviricetes, phylum Cressdnaviricota) is comprised of viruses with small circular single-stranded DNA genomes of ~2.3-3 kb in length that have primarily been identified in fecal sample of various animals. Smacovirus genomes carry two genes in ambisense orientation encoding a capsid protein and a rolling-circle replication initiation protein, respectively. We have revised the taxonomy of the family by assigning 138 new genomic sequences deposited in GenBank to already established taxa as well as 41 new species and six new genera. Furthermore, we have adopted binomial species nomenclature, conforming to the “Genus + freeform epithet” format for all 84 species from 12 genera. The updated Smacoviridae taxonomy presented in this article has been ratified by the International Committee on Taxonomy of Viruses (ICTV).

Smacoviruses have small circular single-stranded DNA genomes (2.3 - 3.0 kb) with genes coding for a rolling-circle replication initiation protein (Rep) and a capsid protein (CP) in an ambience orientation. To date, all smacoviruses have been identified by metagenomic analysis in diverse animal fecal samples (both feces and rectal swabs) [1,2,3,4,5,6,7,8, 11, 12, 14, 15, 18,19,20,21,22, 24, 25, 27,28,29,30, 32, 34, 35, 37, 41]. However, a few have also been identified in domestic animal serum and tracheal swab samples [38, 40] and in insect samples [9, 31]. Smacoviruses appear to have a broad global distribution and have so far been identified in samples collected in Botswana, Brazil, Cameroon, China, the Dominican Republic, Ethiopia, France, Germany, Hungary, New Zealand, Peru, Saint Kitts and Nevis, South Korea, Tanzania, the United Arab Emirates, the United States of America, Viet Nam, and Zambia (Supplementary Table S1). Smacoviruses have not been cultured, and no definite host has been identified; however, a study by Díez-Villaseñor and Rodriguez-Valera [10] has suggested that gut-associated methanogenic archaea could be the actual hosts based on identification of CRISPR spacers matching regions of smacovirus genomes.

Smacoviruses are classified as members of the order Cremevirales, class Arfiviricetes, and phylum Cressdnaviricota [23]. The Rep proteins of smacoviruses are homologous to those of all other members of the phylum Cressdnaviricota and are phylogenetically most closely related to those of members of the order Mulpavirales [23], including the family Nanoviridae, with which smacovirid Reps share several unique sequence motifs, especially in the superfamily 3 helicase domain [16, 17]. During establishment of the family Smacoviridae, six genera (Bovismacovirus, Cosmacovirus, Dragsmacovirus, Drosmacovirus, Huchismacovirus, and Porprismacovirus) were originally created to accommodate the 83 full genome sequences available in public databases in 2017 [39]. Since then, 138 new smacovirus genome sequences have been made available in GenBank. Following the previously established demarcation criteria [39], we first used a Rep phylogeny based on amino acid sequences to determine the genus-level classification of these viral sequences (Fig. 1) and then used a genome-wide 77% pairwise sequence identity threshold to classify these into species (Fig. 2).

Fig. 1
figure1

Maximum-likelihood phylogenetic tree of the Rep amino acid sequences of 220 smacoviruses and a subset of nanoviruses [36], which were used as an outgroup. The Rep sequence alignment was constructed using MAFFT [15] and trimmed with TrimAL [5] using the gappyout option. The final alignment contained 202 amino acid sites and was used to construct a maximum-likelihood phylogenetic tree in PhyML [13] with the LG+F+I+G4 substitution model. Numbers at the nodes represent bootstrap support values (%). Accession numbers are provided for of the single members of the genera Babosmacovirus, Bonzesmacovirus, Bostasmacovirus, Cosmacovirus, Dragsmacovirus, and Felismacovirus

Fig. 2
figure2

Pairwise identity matrix of the genome sequences of representative members of each species of smacoviruses (n = 84) determined using SDT v1.2 [26], supporting the 77% nucleotide sequence identity between viruses proposed as a species demarcation criterion

Based on the Rep phylogeny, we established six new genera to accommodate some of the new divergent smacoviruses and to reclassify two viruses previously included in the genus Huchismacovirus (bovine faeces associated smacovirus 1 and bovine faeces associated smacovirus 2) into two distinct new genera.

The following names have been adopted for the six new genera

  1. 1.

    Babosmacovirus (name derived from baboon – the host/source of the virus).

  2. 2.

    Bonzesmacovirus (name derived from bovine New Zealand – the host/source of the virus).

  3. 3.

    Bostasmacovirus (name derived from Bos taurus – the host/source of the virus).

  4. 4.

    Felismacovirus (name derived from feline – the host/source of the virus).

  5. 5.

    Inpeasmacovirus (name derived from Indian peaflowl – the host/source of the virus).

  6. 6.

    Simismacovirus (name derived from Simian – the simian host/source of the virus).

We also adopted binomial species nomenclature for all smacovirid species (40 existing species, two that have been reassigned to new genera and 42 new species). We have changed the virus species names for this family to a manageable and easy-to-navigate form using a “Genus + freeform epithet” binomial system [33]. The name changes are summarized in Table 1. A detailed summary of all of the smacoviruses and their taxonomic assignments is provided in Supplementary Table S1, and a breakdown of the sources of classified smacoviruses is provided in Fig. 3.

Table 1 Taxonomic update of the family Smacoviridae, including nomenclatural changes and establishment of new species and genera
Fig. 3
figure3

Genus-based list of sources from which the smacovirus genome sequences were determined

Since the present taxonomy assessment, 22 genomic sequences of smacoviruses have been deposited in the GenBank database (15 May 2021), and of these, 15 are tagged as circular, and nine of them can be assigned to currently established species.

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Funding

M.K. was supported by l’Agence Nationale de la Recherche (grant ANR-20-CE20-0009-02).

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705_2021_5224_MOESM1_ESM.xlsx

Supplementary file1 Supplementary Table S1 Summary of the classification of smacoviruses with details of their sources, isolate IDs, and citations (XLSX 28 KB)

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Krupovic, M., Varsani, A. A 2021 taxonomy update for the family Smacoviridae. Arch Virol 166, 3245–3253 (2021). https://doi.org/10.1007/s00705-021-05224-6

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