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  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 . 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 , 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 . Since then, 138 new smacovirus genome sequences have been made available in GenBank. Following the previously established demarcation criteria , 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).
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
Babosmacovirus (name derived from baboon – the host/source of the virus).
Bonzesmacovirus (name derived from bovine New Zealand – the host/source of the virus).
Bostasmacovirus (name derived from Bos taurus – the host/source of the virus).
Felismacovirus (name derived from feline – the host/source of the virus).
Inpeasmacovirus (name derived from Indian peaflowl – the host/source of the virus).
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 . 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.
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.
Altan E, Del Valle MJ, Deng X, Phan TG, Sadeghi M, Delwart EL (2017) Small circular rep-encoding single-stranded DNA genomes in Peruvian diarrhea virome. Genome Announc 5:e00822-e917
Altan E, Aiemjoy K, Phan TG, Deng X, Aragie S, Tadesse Z, Callahan KE, Keenan J, Delwart E (2018) Enteric virome of Ethiopian children participating in a clean water intervention trial. PLoS ONE 13:e0202054
Anindita PD, Sasaki M, Gonzalez G, Phongphaew W, Carr M, Hang’ombe BM, Mweene AS, Ito K, Orba Y, Sawa H (2019) Discovery and genetic characterization of diverse smacoviruses in Zambian non-human primates. Sci Rep 9:5045
Blinkova O, Victoria J, Li Y, Keele BF, Sanz C, Ndjango JB, Peeters M, Travis D, Lonsdorf EV, Wilson ML, Pusey AE, Hahn BH, Delwart EL (2010) Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 91:74–86
Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973
Cheung AK, Ng TF, Lager KM, Bayles DO, Alt DP, Delwart EL, Pogranichniy RM, Kehrli ME Jr (2013) A divergent clade of circular single-stranded DNA viruses from pig feces. Arch Virol 158:2157–2162
Cheung AK, Ng TF, Lager KM, Alt DP, Delwart E, Pogranichniy RM (2015) Identification of several clades of novel single-stranded circular DNA viruses with conserved stem-loop structures in pig feces. Arch Virol 160:353–358
Cheung AK, Ng TFF, Lager KM, Alt DP, Delwart E, Pogranichniy RM (2015) Identification of several clades of novel single-stranded circular DNA viruses with conserved stem-loop structures in pig feces. Adv Virol 160:353–358
Dayaram A, Potter KA, Pailes R, Marinov M, Rosenstein DD, Varsani A (2015) Identification of diverse circular single-stranded DNA viruses in adult dragonflies and damselflies (Insecta: Odonata) of Arizona and Oklahoma, USA. Infect Genet Evol 30:278–287
Diez-Villasenor C, Rodriguez-Valera F (2019) CRISPR analysis suggests that small circular single-stranded DNA smacoviruses infect Archaea instead of humans. Nat Commun 10:294
Duarte MA, Silva J, Brito CR, Teixeira DS, Melo FL, Ribeiro BM, Nagata T, Campos FS (2019) Faecal virome analysis of wild animals from Brazil. Viruses 11:803
Fontenele RS, Lacorte C, Lamas NS, Schmidlin K, Varsani A, Ribeiro SG (2019) Single stranded DNA viruses associated with capybara faeces sampled in Brazil. Viruses 11:710
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Kapusinszky B, Ardeshir A, Mulvaney U, Deng X, Delwart E (2017) Case-control comparison of enteric viromes in captive rhesus macaques with acute or idiopathic chronic diarrhea. J Virol 91:e00952-e1017
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166
Kazlauskas D, Dayaram A, Kraberger S, Goldstien S, Varsani A, Krupovic M (2017) Evolutionary history of ssDNA bacilladnaviruses features horizontal acquisition of the capsid gene from ssRNA nodaviruses. Virology 504:114–121
Kazlauskas D, Varsani A, Koonin EV, Krupovic M (2019) Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids. Nat Commun 10:3425
Kim AR, Chung HC, Kim HK, Kim EO, Nguyen VG, Choi MG, Yang HJ, Kim JA, Park BK (2014) Characterization of a complete genome of a circular single-stranded DNA virus from porcine stools in Korea. Virus Genes 48:81–88
Kim HK, Park SJ, Nguyen VG, Song DS, Moon HJ, Kang BK, Park BK (2012) Identification of a novel single-stranded, circular DNA virus from bovine stool. J Gen Virol 93:635–639
Kraberger S, Waits K, Ivan J, Newkirk E, VandeWoude S, Varsani A (2018) Identification of circular single-stranded DNA viruses in faecal samples of Canada lynx (Lynx canadensis), moose (Alces alces) and snowshoe hare (Lepus americanus) inhabiting the Colorado San Juan Mountains. Infect Genet Evol 64:1–8
Kraberger S, Serieys L, Fountain-Jones N, Packer C, Riley S, Varsani A (2019) Novel smacoviruses identified in the faeces of two wild felids: North American bobcat and African lion. Arch Virol 164:2395–2399
Krupovic M, Ghabrial SA, Jiang D, Varsani A (2016) Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol 161:2633–2643
Krupovic M, Varsani A, Kazlauskas D, Breitbart M, Delwart E, Rosario K, Yutin N, Wolf YI, Harrach B, Zerbini FM, Dolja VV, Kuhn JH, Koonin EV (2020) Cressdnaviricota: a virus phylum unifying seven families of rep-encoding viruses with single-stranded, circular DNA genomes. J Virol 94:e00582-20
Lima DA, Cibulski SP, Finkler F, Teixeira TF, Varela APM, Cerva C, Loiko MR, Scheffer CM, Dos Santos HF, Mayer FQ, Roehe PM (2017) Faecal virome of healthy chickens reveals a large diversity of the eukaryote viral community, including novel circular ssDNA viruses. J Gen Virol 98:690–703
Lima DA, Cibulski SP, Tochetto C, Varela APM, Finkler F, Teixeira TF, Loiko MR, Cerva C, Junqueira DM, Mayer FQ, Roehe PM (2019) The intestinal virome of malabsorption syndrome-affected and unaffected broilers through shotgun metagenomics. Virus Res 261:9–20
Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9:e108277
Ng TF, Zhang W, Sachsenroder J, Kondov NO, da Costa AC, Vega E, Holtz LR, Wu G, Wang D, Stine CO, Antonio M, Mulvaney US, Muench MO, Deng X, Ambert-Balay K, Pothier P, Vinje J, Delwart E (2015) A diverse group of small circular ssDNA viral genomes in human and non-human primate stools. Virus Evol 1:vev017
Phan TG, da Costa AC, Del Valle MJ, Bucardo-Rivera F, Nordgren J, O’Ryan M, Deng X, Delwart E (2016) The fecal virome of South and Central American children with diarrhea includes small circular DNA viral genomes of unknown origin. Arch Virol 161:959–966
Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490
Reuter G, Boros A, Delwart E, Pankovics P (2014) Novel circular single-stranded DNA virus from turkey faeces. Arch Virol 159:2161–2164
Rosario K, Mettel KA, Benner BE, Johnson R, Scott C, Yusseff-Vanegas SZ, Baker CCM, Cassill DL, Storer C, Varsani A, Breitbart M (2018) Virus discovery in all three major lineages of terrestrial arthropods highlights the diversity of single-stranded DNA viruses associated with invertebrates. PeerJ 6:e5761
Sachsenroder J, Braun A, Machnowska P, Ng TFF, Deng X, Guenther S, Bernstein S, Ulrich RG, Delwart E, Johne R (2014) Metagenomic identification of novel enteric viruses in urban wild rats and genome characterization of a group A rotavirus. J Gen Virol 95:2734–2747
Siddell SG, Walker PJ, Lefkowitz EJ, Mushegian AR, Dutilh BE, Harrach B, Harrison RL, Junglen S, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Nibert ML, Rubino L, Sabanadzovic S, Simmonds P, Varsani A, Zerbini FM, Davison AJ (2020) Binomial nomenclature for virus species: a consultation. Arch Virol 165:519–525
Sikorski A, Arguello-Astorga GR, Dayaram A, Dobson RC, Varsani A (2013) Discovery of a novel circular single-stranded DNA virus from porcine faeces. Arch Virol 158:283–289
Steel O, Kraberger S, Sikorski A, Young LM, Catchpole RJ, Stevens AJ, Ladley JJ, Coray DS, Stainton D, Dayaram A, Julian L, van Bysterveldt K, Varsani A (2016) Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand. Infect Genet Evol 43:151–164
Thomas JE, Gronenborn B, Harding RM, Mandal B, Grigoras I, Randles JW, Sano Y, Timchenko T, Vetten HJ, Yeh HH, Ziebell H, Ictv Report C (2021) J Gen Virol 102:001544
Tisza MJ, Pastrana DV, Welch NL, Stewart B, Peretti A, Starrett GJ, Pang YS, Krishnamurthy SR, Pesavento PA, McDermott DH, Murphy PM, Whited JL, Miller B, Brenchley J, Rosshart SP, Rehermann B, Doorbar J, Ta’ala BA, Pletnikova O, Troncoso JC, Resnick SM, Bolduc B, Sullivan MB, Varsani A, Segall AM, Buck CB (2020) Discovery of several thousand highly diverse circular DNA viruses. Elife 9:e51971
Tochetto C, Muterle Varela AP, Alves de Lima D, Loiko MR, Mengue Scheffer C, Pinto Paim W, Cerva C, Schmidt C, Cibulski SP, Cano Ortiz L, Callegari Jacques SM, Franco AC, Quoos Mayer F, Roehe PM (2020) Viral DNA genomes in sera of farrowing sows with or without stillbirths. PLoS ONE 15:e0230714
Varsani A, Krupovic M (2018) Smacoviridae: a new family of animal-associated single-stranded DNA viruses. Arch Virol 163:2005–2015
Wang H, Li S, Mahmood A, Yang S, Wang X, Shen Q, Shan T, Deng X, Li J, Hua X, Cui L, Delwart E, Zhang W (2018) Plasma virome of cattle from forest region revealed diverse small circular ssDNA viral genomes. Virol J 15:11
Woo PC, Lau SK, Teng JL, Tsang AK, Joseph M, Wong EY, Tang Y, Sivakumar S, Bai R, Wernery R, Wernery U, Yuen KY (2014) Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virology 471–473:117–125
M.K. was supported by l’Agence Nationale de la Recherche (grant ANR-20-CE20-0009-02).
Conflict of interest
The authors declare no conflicts of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Sead Sabanadzovic.
Below is the link to the electronic supplementary material.
Supplementary file1 Supplementary Table S1 Summary of the classification of smacoviruses with details of their sources, isolate IDs, and citations (XLSX 28 KB)
About this article
Cite this article
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