Top

Published in:

01-05-2020 | Escherichia Coli | Virology Division News:

Taxonomy of prokaryotic viruses: 2018-2019 update from the ICTV Bacterial and Archaeal Viruses Subcommittee

Authors: Evelien M. Adriaenssens, Matthew B. Sullivan, Petar Knezevic, Leonardo J. van Zyl, B. L. Sarkar, Bas E. Dutilh, Poliane Alfenas-Zerbini, Małgorzata Łobocka, Yigang Tong, James Rodney Brister, Andrea I. Moreno Switt, Jochen Klumpp, Ramy Karam Aziz, Jakub Barylski, Jumpei Uchiyama, Rob A. Edwards, Andrew M. Kropinski, Nicola K. Petty, Martha R. J. Clokie, Alla I. Kushkina, Vera V. Morozova, Siobain Duffy, Annika Gillis, Janis Rumnieks, İpek Kurtböke, Nina Chanishvili, Lawrence Goodridge, Johannes Wittmann, Rob Lavigne, Ho Bin Jang, David Prangishvili, Francois Enault, Dann Turner, Minna M. Poranen, Hanna M. Oksanen, Mart Krupovic

Published in: Archives of Virology | Issue 5/2020

Abstract

This article is a summary of the activities of the ICTV’s Bacterial and Archaeal Viruses Subcommittee for the years 2018 and 2019. Highlights include the creation of a new order, 10 families, 22 subfamilies, 424 genera and 964 species. Some of our concerns about the ICTV’s ability to adjust to and incorporate new DNA- and protein-based taxonomic tools are discussed.

Adriaenssens EM, Wittmann J, Kuhn JH, Turner D, Sullivan MB, Dutilh BE, Jang HB, van Zyl LJ, Klumpp J, Lobocka M, Moreno Switt AI, Rumnieks J, Edwards RA, Uchiyama J, Alfenas-Zerbini P, Petty NK, Kropinski AM, Barylski J, Gillis A, Clokie MRC, Prangishvili D, Lavigne R, Aziz RK, Duffy S, Krupovic M, Poranen MM, Knezevic P, Enault F, Tong Y, Oksanen HM, Rodney Brister J (2018) Taxonomy of prokaryotic viruses: 2017 update from the ICTV Bacterial and Archaeal Viruses Subcommittee. Arch Virol 163:1125–1129

Mochizuki T, Krupovic M, Pehau-Arnaudet G, Sako Y, Forterre P, Prangishvili D (2012) Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome. Proc Natl Acad Sci USA 109:13386–13391

Lavigne R, Seto D, Mahadevan P, Ackermann H-W, Kropinski AM (2008) Unifying classical and molecular taxonomic classification: analysis of thePodoviridae using BLASTP-based tools. Res Microbiol 159:406–414

Jamalludeen N, Johnson RP, Friendship R, Kropinski AM, Lingohr EJ, Gyles CL (2007) Isolation and characterization of nine bacteriophages that lyse O149 enterotoxigenic Escherichia coli. Vet Microbiol 124:47–57

Jamalludeen N, Kropinski AM, Johnson RP, Lingohr E, Harel J, Gyles CL (2008) Complete genomic sequence of bacteriophage phiEcoM-GJ1, a novel phage that has myovirus morphology and a podovirus-like RNA polymerase. Appl Environ Microbiol 74:516–525

Jang HB, Bolduc B, Zablocki O, Kuhn JH, Roux S, Adriaenssens EM, Brister JR, Kropinski AM, Krupovic M, Lavigne R, Turner D, Sullivan MB (2019) Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat Biotechnol 37:632–639

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:e3243

Krupovic M, Dutilh BE, Adriaenssens EM, Wittmann J, Vogensen FK, Sullivan MB, Rumnieks J, Prangishvili D, Lavigne R, Kropinski AM, Klumpp J, Gillis A, Enault F, Edwards RA, Duffy S, Clokie MR, Barylski J, Ackermann HW, Kuhn JH (2016) Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol 161:1095–1099

Laanto E, Mantynen S, De Colibus L, Marjakangas J, Gillum A, Stuart DI, Ravantti JJ, Huiskonen JT, Sundberg LR (2017) Virus found in a boreal lake links ssDNA and dsDNA viruses. Proc Natl Acad Sci USA 114:8378–8383

10.

Yutin N, Backstrom D, Ettema TJG, Krupovic M, Koonin EV (2018) Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis. Virol J 15:67

11.

Bath C, Cukalac T, Porter K, Dyall-Smith ML (2006) His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 350:228–239

12.

Bath C, Dyall-Smith ML (1998) His1, an archaeal virus of theFuselloviridae family that infectsHaloarcula hispanica. J Virol 72:9392–9395

13.

Krupovic M, Quemin ER, Bamford DH, Forterre P, Prangishvili D (2014) Unification of the globally distributed spindle-shaped viruses of the Archaea. J Virol 88:2354–2358

14.

Pietilä MK, Atanasova NS, Oksanen HM, Bamford DH (2013) Modified coat protein forms the flexible spindle-shaped virion of haloarchaeal virus His1. Environ Microbiol 15:1674–1686

15.

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, Jang HB, Simmonds P, Aiewsakun P, Wittmann J, Tolstoy I, Brister JR, Kropinski AM, Adriaenssens EM (2020) Analysis of spounaviruses as a case study for the overdue reclassification of tailed phages. Syst Biol 69:110–123

16.

Klumpp J, Lavigne R, Loessner MJ, Ackermann HW (2010) The SPO1-related bacteriophages. Arch Virol 155:1547–1561

17.

Aiewsakun P, Simmonds P (2018) The genomic underpinnings of eukaryotic virus taxonomy: creating a sequence-based framework for family-level virus classification. Microbiome 6:38

18.

Rohwer F, Edwards R (2002) The phage proteomic tree: a genome-based taxonomy for phage. J Bacteriol 184:4529–4535

19.

Wang H, Guo Z, Feng H, Chen Y, Chen X, Li Z, Hernandez-Ascencio W, Dai X, Zhang Z, Zheng X, Mora-Lopez M, Fu Y, Zhang C, Zhu P, Huang L (2018) Novel Sulfolobus virus with an exceptional capsid architecture. J Virol 92:e01717–e01727

20.

Kim JG, Kim SJ, Cvirkaite-Krupovic V, Yu WJ, Gwak JH, Lopez-Perez M, Rodriguez-Valera F, Krupovic M, Cho JC, Rhee SK (2019) Spindle-shaped viruses infect marine ammonia-oxidizing thaumarchaea. Proc Natl Acad Sci USA 116:15645–15650

21.

Prangishvili D, Krupovic M, ICTV Report Consortium (2018) ICTV virus taxonomy profile: Ampullaviridae. J Gen Virol 99:288–289

22.

Prangishvili D, Krupovic M, ICTV Report Consortium (2018) ICTV virus taxonomy profile: Bicaudaviridae. J Gen Virol 99:864–865

23.

Prangishvili D, Krupovic M, ICTV Report Consortium (2018) ICTV Virus Taxonomy Profile: Globuloviridae. J Gen Virol 99:1357–1358

24.

Prangishvili D, Mochizuki T, Krupovic M, ICTV Report Consortium (2018) ICTV virus taxonomy profile: Guttaviridae. J Gen Virol 99:290–291

25.

Prangishvili D, Mochizuki T, Krupovic M, ICTV Report Consortium (2020) ICTV virus taxonomy profile: Spiraviridae. J Gen Virol. https://doi.org/10.1099/jgv.0.001385CrossRef

26.

Prangishvili D, Rensen E, Mochizuki T, Krupovic M, ICTV Report Consortium (2019) ICTV virus taxonomy profile: Tristromaviridae. J Gen Virol 100:135–136

27.

Krupovic M, ICTV Report Consortium (2018) ICTV virus taxonomy profile: Plasmaviridae. J Gen Virol 99:617–618

28.

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 (2019) Binomial nomenclature for virus species: a consultation. Arch Virol. https://doi.org/10.1007/s00705-019-04477-6CrossRef

29.

Bao Y, Amarasinghe GK, Basler CF, Bavari S, Bukreyev A, Chandran K, Dolnik O, Dye JM, Ebihara H, Formenty P, Hewson R, Kobinger GP, Leroy EM, Muhlberger E, Netesov SV, Patterson JL, Paweska JT, Smither SJ, Takada A, Towner JS, Volchkov VE, Wahl-Jensen V, Kuhn JH (2017) Implementation of objective PASC-derived taxon demarcation criteria for official classification of filoviruses. Viruses 9:106

30.

Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277

31.

Randhawa GS, Hill KA, Kari L (2019) ML-DSP: machine learning with digital signal processing for ultrafast, accurate, and scalable genome classification at all taxonomic levels. BMC Genom 20:267

32.

Meier-Kolthoff JP, Goker M (2017) VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics 33:3396–3404

33.

Chibani CM, Farr A, Klama S, Dietrich S, Liesegang H (2019) Classifying the unclassified: a phage classification method. Viruses 11:195

34.

Nishimura Y, Yoshida T, Kuronishi M, Uehara H, Ogata H, Goto S (2017) ViPTree: the viral proteomic tree server. Bioinformatics 33:2379–2380

35.

Low SJ, Dzunkova M, Chaumeil PA, Parks DH, Hugenholtz P (2019) Evaluation of a concatenated protein phylogeny for classification of tailed double-stranded DNA viruses belonging to the order Caudovirales. Nat Microbiol 4:1306–1315

36.

Kristensen DM, Kannan L, Coleman MK, Wolf YI, Sorokin A, Koonin EV, Mushegian A (2010) A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches. Bioinformatics 26:1481–1487

37.

Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, Rubin E, Ivanova NN, Kyrpides NC (2016) Uncovering Earth’s virome. Nature 536:425–430

38.

Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, Poulos BT, Solonenko N, Lara E, Poulain J, Pesant S, Kandels-Lewis S, Dimier C, Picheral M, Searson S, Cruaud C, Alberti A, Duarte CM, Gasol JM, Vaque D, Bork P, Acinas SG, Wincker P, Sullivan MB (2016) Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537:689–693

39.

Shkoporov AN, Clooney AG, Sutton TDS, Ryan FJ, Daly KM, Nolan JA, McDonnell SA, Khokhlova EV, Draper LA, Forde A, Guerin E, Velayudhan V, Ross RP, Hill C (2019) The human gut virome is highly diverse, stable, and individual specific. Cell Host Microbe 26:527–541 (e525)

40.

Callanan J, Stockdale SR, Shkoporov A, Draper LA, Ross RP, Hill C (2018) RNA phage biology in a metagenomic era. Viruses 10:386

41.

Creasy A, Rosario K, Leigh BA, Dishaw LJ, Breitbart M (2018) Unprecedented Diversity of ssDNA phages from the family Microviridae detected within the gut of a protochordate model organism (Ciona robusta). Viruses 10:404

42.

Gong Z, Liang Y, Wang M, Jiang Y, Yang Q, Xia J, Zhou X, You S, Gao C, Wang J, He J, Shao H, McMinn A (2018) Viral diversity and its relationship with environmental factors at the surface and deep sea of Prydz Bay, Antarctica. Front Microbiol 9:2981

43.

Krishnamurthy SR, Janowski AB, Zhao G, Barouch D, Wang D (2016) Hyperexpansion of RNA bacteriophage diversity. PLoS Biol 14:e1002409

44.

Quaiser A, Dufresne A, Ballaud F, Roux S, Zivanovic Y, Colombet J, Sime-Ngando T, Francez AJ (2015) Diversity and comparative genomics of Microviridae in Sphagnum-dominated peatlands. Front Microbiol 6:375

45.

Sommers P, Fontenele RS, Kringen T, Kraberger S, Porazinska DL, Darcy JL, Schmidt SK, Varsani A (2019) Single-stranded DNA viruses in antarctic cryoconite holes. Viruses 11:1022

46.

Wang H, Ling Y, Shan T, Yang S, Xu H, Deng X, Delwart E, Zhang W (2019) Gut virome of mammals and birds reveals high genetic diversity of the family Microviridae. Virus Evol 5:vez013

47.

Zhong X, Guidoni B, Jacas L, Jacquet S (2015) Structure and diversity of ssDNA Microviridae viruses in two peri-alpine lakes (Annecy and Bourget, France). Res Microbiol 166:644–654

48.

Callanan J, Stockdale SR, Shkoporov A, Draper LA, Ross RP (2020) Hill C (2020) Expansion of known ssRNA phage genomes: from tens to over a thousand. Sci Adv 6(6):eaay5981. https://doi.org/10.1126/sciadv.aay5981CrossRef

Title: Taxonomy of prokaryotic viruses: 2018-2019 update from the ICTV Bacterial and Archaeal Viruses Subcommittee
Authors: Evelien M. Adriaenssens
Matthew B. Sullivan
Petar Knezevic
Leonardo J. van Zyl
B. L. Sarkar
Bas E. Dutilh
Poliane Alfenas-Zerbini
Małgorzata Łobocka
Yigang Tong
James Rodney Brister
Andrea I. Moreno Switt
Jochen Klumpp
Ramy Karam Aziz
Jakub Barylski
Jumpei Uchiyama
Rob A. Edwards
Andrew M. Kropinski
Nicola K. Petty
Martha R. J. Clokie
Alla I. Kushkina
Vera V. Morozova
Siobain Duffy
Annika Gillis
Janis Rumnieks
İpek Kurtböke
Nina Chanishvili
Lawrence Goodridge
Johannes Wittmann
Rob Lavigne
Ho Bin Jang
David Prangishvili
Francois Enault
Dann Turner
Minna M. Poranen
Hanna M. Oksanen
Mart Krupovic
Publication date: 01-05-2020
Publisher: Springer Vienna
Keyword: Escherichia Coli
Published in: Archives of Virology / Issue 5/2020
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-020-04577-8

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Taxonomy of prokaryotic viruses: 2018-2019 update from the ICTV Bacterial and Archaeal Viruses Subcommittee

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2020

Development of a rapid and sensitive europium (III) chelate microparticle-based lateral flow test strip for the detection and epidemiological surveillance of porcine epidemic diarrhea virus

Metaviromic analysis reveals coinfection of papaya in western Kenya with a unique strain of Moroccan watermelon mosaic virus and a novel member of the family Alphaflexiviridae

Correction to: Binomial nomenclature for virus species: a consultation

Higher virulence of swine H1N2 influenza viruses containing avian-origin HA and 2009 pandemic PA and NP in pigs and mice

Complete genome analysis of the novel Edwardsiella tarda phage vB_EtaM_ET-ABTNL-9

Human respiratory syncytial virus F protein expressed in Pichia pastoris or Escherichia coli induces protective immunity without inducing enhanced respiratory disease in mice

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page