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Published in: Archives of Virology 8/2018

Open Access 01-08-2018 | In honor of Marc van Regenmortel

Virus classification – where do you draw the line?

Authors: Peter Simmonds, Pakorn Aiewsakun

Published in: Archives of Virology | Issue 8/2018

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Abstract

High-throughput sequencing (HTS) and its use in recovering and assembling novel virus sequences from environmental, human clinical, veterinary and plant samples has unearthed a vast new catalogue of viruses. Their classification, known by their sequences alone, sets a major challenge to traditional virus taxonomy, especially at the family and species levels, which have been historically based largely on descriptive taxon definitions. These typically entail some knowledge of their phenotypic properties, including replication strategies, virion structure and clinical and epidemiological features, such as host range, geographical distribution and disease outcomes. Little to no information on these attributes is available, however, for viruses identified in metagenomic datasets. If such viruses are to be included in virus taxonomy, their assignments will have to be guided largely or entirely by metrics of genetic relatedness. The immediate problem here is that the International Committee on Taxonomy of Viruses (ICTV), an organisation that authorises the taxonomic classification of viruses, provides little or no guidance on how similar or how divergent viruses must be in order to be considered members of new species or new families. We have recently developed a method for scoring genomic (dis)similarity between viruses (Genome Relationships Applied to Virus Taxonomy – GRAViTy) among the eukaryotic and prokaryotic viruses currently classified by the ICTV. At the family and genus levels, we found large-scale consistency between genetic relationships and their taxonomic assignments for eukaryotic viruses of all genome configurations and genome sizes. Family assignments of prokaryotic viruses have, however, been made at a quite different genetic level, and groupings currently classified as sub-families are a much better match to the eukaryotic virus family level. These findings support the ongoing reorganisation of bacteriophage taxonomy by the ICTV Phage Study Group. A rapid and objective means to explore metagenomic viral diversity and make evidence-based assignments for such viruses at each taxonomic layer is essential. Analysis of sequences by GRAViTy provides evidence that family (and genus) assignments of currently classified viruses are largely underpinned by genomic relatedness, and these features could serve as a guide towards an evidence-based classification of metagenomic viruses in the future.
Literature
1.
go back to reference Abergel C, Legendre M, Claverie JM (2015) The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. FEMS Microbiol Rev 39:779–796CrossRefPubMed Abergel C, Legendre M, Claverie JM (2015) The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. FEMS Microbiol Rev 39:779–796CrossRefPubMed
2.
go back to reference Ackermann HW, Prangishvili D (2012) Prokaryote viruses studied by electron microscopy. Arch Virol 157:1843–1849CrossRefPubMed Ackermann HW, Prangishvili D (2012) Prokaryote viruses studied by electron microscopy. Arch Virol 157:1843–1849CrossRefPubMed
3.
go back to reference Adams MJ, Lefkowitz EJ, King AM, Harrach B, Harrison RL, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Mushegian AR, Nibert ML, Sabanadzovic S, Sanfacon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Orton RJ, Smith DB, Gorbalenya AE, Davison AJ (2017) 50 years of the International Committee on Taxonomy of Viruses: progress and prospects. Arch Virol 162:1441–1446CrossRefPubMed Adams MJ, Lefkowitz EJ, King AM, Harrach B, Harrison RL, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Mushegian AR, Nibert ML, Sabanadzovic S, Sanfacon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Orton RJ, Smith DB, Gorbalenya AE, Davison AJ (2017) 50 years of the International Committee on Taxonomy of Viruses: progress and prospects. Arch Virol 162:1441–1446CrossRefPubMed
5.
go back to reference Aiewsakun P, Simmonds P (2018) The genomic underpinnings of eukaryotic virus taxonomy: creating a sequence-based framework for family-level virus classification. Microbiome 6:38CrossRefPubMedPubMedCentral Aiewsakun P, Simmonds P (2018) The genomic underpinnings of eukaryotic virus taxonomy: creating a sequence-based framework for family-level virus classification. Microbiome 6:38CrossRefPubMedPubMedCentral
6.
go back to reference Barylski J, Enault F, Dutilh BE, Schuller MB, Edwards RA, Gillis A, Klumpp J, Knezevic P, Krupovic M, Kuhn JH, Lavigne R, Oksanen HM, Sullivan MB, Wittmann J, Tolstoy I, Brister JR, Kropinski AM, Adriaenssens EM (2018) Analysis of spounaviruses as a case study for the overdue reclassification of tailed bacteriophages. bioRxiv. https://doi.org/10.1101/220434 CrossRef Barylski J, Enault F, Dutilh BE, Schuller MB, Edwards RA, Gillis A, Klumpp J, Knezevic P, Krupovic M, Kuhn JH, Lavigne R, Oksanen HM, Sullivan MB, Wittmann J, Tolstoy I, Brister JR, Kropinski AM, Adriaenssens EM (2018) Analysis of spounaviruses as a case study for the overdue reclassification of tailed bacteriophages. bioRxiv. https://​doi.​org/​10.​1101/​220434 CrossRef
7.
go back to reference Blitvich BJ, Beaty BJ, Blair CD, Brault AC, Dobler G, Drebot MA, Haddow AD, Kramer LD, LaBeaud AD, Monath TP, Mossel EC, Plante K, Powers AM, Tesh RB, Turell MJ, Vasilakis N, Weaver SC (2018) Bunyavirus taxonomy: limitations and misconceptions associated with the current ICTV criteria used for species demarcation. Am J Trop Med Hyg 99(1):11–16CrossRefPubMed Blitvich BJ, Beaty BJ, Blair CD, Brault AC, Dobler G, Drebot MA, Haddow AD, Kramer LD, LaBeaud AD, Monath TP, Mossel EC, Plante K, Powers AM, Tesh RB, Turell MJ, Vasilakis N, Weaver SC (2018) Bunyavirus taxonomy: limitations and misconceptions associated with the current ICTV criteria used for species demarcation. Am J Trop Med Hyg 99(1):11–16CrossRefPubMed
8.
go back to reference Bolduc B, Jang HB, Doulcier G, You ZQ, Roux S, Sullivan MB (2017) vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria. PeerJ 5:e3243CrossRefPubMedPubMedCentral Bolduc B, Jang HB, Doulcier G, You ZQ, Roux S, Sullivan MB (2017) vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria. PeerJ 5:e3243CrossRefPubMedPubMedCentral
9.
go back to reference Brussow H (2009) The not so universal tree of life or the place of viruses in the living world. Philos Trans R Soc Lond Ser B Biol Sci 364:2263–2274CrossRef Brussow H (2009) The not so universal tree of life or the place of viruses in the living world. Philos Trans R Soc Lond Ser B Biol Sci 364:2263–2274CrossRef
13.
go back to reference Forterre P (2006) The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 117:5–16CrossRefPubMed Forterre P (2006) The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 117:5–16CrossRefPubMed
14.
go back to reference Gibbs AJ, Gibbs MJ (2006) A broader definition of ‘the virus species’. Arch Virol 151:1419–1422CrossRefPubMed Gibbs AJ, Gibbs MJ (2006) A broader definition of ‘the virus species’. Arch Virol 151:1419–1422CrossRefPubMed
15.
go back to reference Grose JH, Casjens SR (2014) Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae. Virology 468–470:421–443CrossRefPubMed Grose JH, Casjens SR (2014) Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae. Virology 468–470:421–443CrossRefPubMed
16.
go back to reference Hulo C, Masson P, Le Mercier P, Toussaint A (2015) A structured annotation frame for the transposable phages: a new proposed family “Saltoviridae” within the Caudovirales. Virology 477:155–163CrossRefPubMed Hulo C, Masson P, Le Mercier P, Toussaint A (2015) A structured annotation frame for the transposable phages: a new proposed family “Saltoviridae” within the Caudovirales. Virology 477:155–163CrossRefPubMed
18.
go back to reference King AMQ, Lefkowitz EJ, Mushegian AR, Adams MJ, Dutilh BE, Gorbalenya AE, Harrach B, Harrison RL, Junglen S, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Nibert ML, Rubino L, Sabanadzovic S, Sanfacon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Davison AJ (2018) Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2018). Arch Virol. https://doi.org/10.1007/s00705-018-3847-1 PubMedCrossRef King AMQ, Lefkowitz EJ, Mushegian AR, Adams MJ, Dutilh BE, Gorbalenya AE, Harrach B, Harrison RL, Junglen S, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Nibert ML, Rubino L, Sabanadzovic S, Sanfacon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Davison AJ (2018) Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2018). Arch Virol. https://​doi.​org/​10.​1007/​s00705-018-3847-1 PubMedCrossRef
20.
go back to reference Krupovic M, Ghabrial SA, Jiang D, Varsani A (2016) Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol 161(9):2633–2643CrossRefPubMed Krupovic M, Ghabrial SA, Jiang D, Varsani A (2016) Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol 161(9):2633–2643CrossRefPubMed
21.
go back to reference Mokili JL, Rohwer F, Dutilh BE (2012) Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2:63–77CrossRefPubMed Mokili JL, Rohwer F, Dutilh BE (2012) Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2:63–77CrossRefPubMed
22.
go back to reference Rosario K, Breitbart M (2011) Exploring the viral world through metagenomics. Curr Opin Virol 1:289–297CrossRefPubMed Rosario K, Breitbart M (2011) Exploring the viral world through metagenomics. Curr Opin Virol 1:289–297CrossRefPubMed
23.
go back to reference Shi M, Lin XD, Vasilakis N, Tian JH, Li CX, Chen LJ, Eastwood G, Diao XN, Chen MH, Chen X, Qin XC, Widen SG, Wood TG, Tesh RB, Xu J, Holmes EC, Zhang YZ (2015) Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J Virol 90:659–669CrossRefPubMedPubMedCentral Shi M, Lin XD, Vasilakis N, Tian JH, Li CX, Chen LJ, Eastwood G, Diao XN, Chen MH, Chen X, Qin XC, Widen SG, Wood TG, Tesh RB, Xu J, Holmes EC, Zhang YZ (2015) Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J Virol 90:659–669CrossRefPubMedPubMedCentral
24.
go back to reference Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu J, Holmes EC, Zhang YZ (2016) Redefining the invertebrate RNA virosphere. Nature 540:539–543CrossRef Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu J, Holmes EC, Zhang YZ (2016) Redefining the invertebrate RNA virosphere. Nature 540:539–543CrossRef
25.
go back to reference Simmonds P, Adams MJ, Benko M, Breitbart M, Brister JR, Carstens EB, Davison AJ, Delwart E, Gorbalenya AE, Harrach B, Hull R, King AM, Koonin EV, Krupovic M, Kuhn JH, Lefkowitz EJ, Nibert ML, Orton R, Roossinck MJ, Sabanadzovic S, Sullivan MB, Suttle CA, Tesh RB, van der Vlugt RA, Varsani A, Zerbini FM (2017) Consensus statement: Virus taxonomy in the age of metagenomics. Nat Rev Microbiol 15:161–168CrossRefPubMed Simmonds P, Adams MJ, Benko M, Breitbart M, Brister JR, Carstens EB, Davison AJ, Delwart E, Gorbalenya AE, Harrach B, Hull R, King AM, Koonin EV, Krupovic M, Kuhn JH, Lefkowitz EJ, Nibert ML, Orton R, Roossinck MJ, Sabanadzovic S, Sullivan MB, Suttle CA, Tesh RB, van der Vlugt RA, Varsani A, Zerbini FM (2017) Consensus statement: Virus taxonomy in the age of metagenomics. Nat Rev Microbiol 15:161–168CrossRefPubMed
26.
go back to reference Simmonds P (2018) A clash of ideas—the varying uses of the ‘species’ term in virology and their utility for classifying viruses in metagenomic datasets. J Gen Virol 99:277–287CrossRef Simmonds P (2018) A clash of ideas—the varying uses of the ‘species’ term in virology and their utility for classifying viruses in metagenomic datasets. J Gen Virol 99:277–287CrossRef
27.
go back to reference Van Regenmortel MH, Maniloff J, Calisher C (1991) The concept of virus species. Arch Virol 120:313–314CrossRefPubMed Van Regenmortel MH, Maniloff J, Calisher C (1991) The concept of virus species. Arch Virol 120:313–314CrossRefPubMed
28.
go back to reference Van Regenmortel MH (2003) Viruses are real, virus species are man-made, taxonomic constructions. Arch Virol 148:2481–2488CrossRefPubMed Van Regenmortel MH (2003) Viruses are real, virus species are man-made, taxonomic constructions. Arch Virol 148:2481–2488CrossRefPubMed
29.
go back to reference Van Regenmortel MHV (2016) Classes, taxa and categories in a heirarchical virus classification: a review of current debates of definitions and names of species. Bionomia 10(1):1–21CrossRef Van Regenmortel MHV (2016) Classes, taxa and categories in a heirarchical virus classification: a review of current debates of definitions and names of species. Bionomia 10(1):1–21CrossRef
31.
go back to reference Wigington CH, Sonderegger D, Brussaard CPD, Buchan A, Finke JF, Fuhrman JA, Lennon JT, Middelboe M, Suttle CA, Stock C, Wilson WH, Wommack KE, Wilhelm SW, Weitz JS (2016) Re-examination of the relationship between marine virus and microbial cell abundances. Nat Microbiol 1:15024CrossRefPubMed Wigington CH, Sonderegger D, Brussaard CPD, Buchan A, Finke JF, Fuhrman JA, Lennon JT, Middelboe M, Suttle CA, Stock C, Wilson WH, Wommack KE, Wilhelm SW, Weitz JS (2016) Re-examination of the relationship between marine virus and microbial cell abundances. Nat Microbiol 1:15024CrossRefPubMed
Metadata
Title
Virus classification – where do you draw the line?
Authors
Peter Simmonds
Pakorn Aiewsakun
Publication date
01-08-2018
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 8/2018
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-018-3938-z

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