Archives of Virology

, Volume 162, Issue 4, pp 1153–1157

Taxonomy of prokaryotic viruses: 2016 update from the ICTV bacterial and archaeal viruses subcommittee

  • Evelien M. Adriaenssens
  • Mart Krupovic
  • Petar Knezevic
  • Hans-Wolfgang Ackermann
  • Jakub Barylski
  • J. Rodney Brister
  • Martha R. C. Clokie
  • Siobain Duffy
  • Bas E. Dutilh
  • Robert A. Edwards
  • Francois Enault
  • Ho Bin Jang
  • Jochen Klumpp
  • Andrew M. Kropinski
  • Rob Lavigne
  • Minna M. Poranen
  • David Prangishvili
  • Janis Rumnieks
  • Matthew B. Sullivan
  • Johannes Wittmann
  • Hanna M. Oksanen
  • Annika Gillis
  • Jens H. Kuhn
Virology Division News
The prokaryotic virus community is represented at the International Committee on Taxonomy of Viruses (ICTV) by the Bacterial and Archaeal Viruses Subcommittee. Since our last report [8], the committee composition has changed, and a large number of taxonomic proposals (TaxoProps) were submitted to the ICTV Executive Committee (EC) for approval.
  1. 1.

    New appointments. The committee has been enlarged through the additions of Drs. J. Rodney Brister (Chair—Molecular Typing), Ho Bin Jang (Member), Petar Knezevic (Chair—ICTV Inoviridae Study Group), Hanna M. Oksanen (Chair—ICTV Corticoviridae Study Group), and Minna M. Poranen (Chair—ICTV Cystoviridae Study Group). In addition, Dr. Mart Krupovic has taken over the Chairmanship of the ICTV Plasmaviridae Study Group.

     
  2. 2.

    Future of the orderCaudovirales. With the dramatic increase in the number of characterized tailed bacterial and archaeal viruses, it is becoming increasingly clear that the order Caudovirales (and the three included families Myoviridae, Siphoviridae and Podoviridae) can no longer sustain the huge genetic diversity within this virus group [5] and has to be adequately reorganized. Indeed, taxonomic hurdles with this and some other expansive groups of viruses, prompted ICTV to explore the possibility of introducing additional taxonomic levels. Initial ideas and plans were presented to the microbial viruses community at the 2016 EMBO conference “Viruses of Microbes IV” (Liverpool, UK). Currently, the Bacterial and Archaeal Viruses Subcommittee is examining the consistency of the order Caudovirales on the example of a diverse group of phages currently classified in the subfamily Spounavirinae [2, 6, 7, 9, 12]. We applied a range of complementary DNA and protein sequence analysis tools as well as phylogenetic methods to the analysis of 93 Bacillus, Enterococcus, Listeria, and Staphylococcus phages with large genomes (≈110–160 kb). A manuscript describing our findings is in preparation, and the appropriate TaxoProps will be submitted.

     
  3. 3.
    Taxonomy of prokaryotic viruses found in GenBank. Genome sequences of prokaryotic viruses are accumulating in public sequence databases, such as GenBank, at an increasing rate. Oftentimes, these sequences are being deposited without or with only minimal taxonomy descriptions. To appropriately classify these viruses, the Subcommittee adopted a holistic approach with the first-line discriminator being DNA sequence identity (calculated using NCBI BLASTN [3, 10] or Gegenees BLASTN [1]) of the genome in question to those of previously classified viruses. Next, overall protein identity was calculated using Gegenees TBLASTX for large datasets and CoreGenes 3.5 [11] for smaller sets. Lastly, phylogenetic analyses of one to three conserved phage proteins, often including the large subunit of the terminase and major capsid proteins or DNA-replication-associated proteins, were carried out using maximum-likelihood method as implemented at Phylogeny.fr [4]. The changes described here were formalized and submitted in more than 80 ICTV TaxoProps for consideration by the ICTV EC (http://www.ictvonline.org). One new archaeal virus family (Tristromaviridae), six new bacteriophage subfamilies (Ounavirinae [Salmonella phage FelixO1], Sepvirinae [Escherichia phage 933 W], Arquatrovirinae [Streptomyces phage R4], Bclasvirinae [Mycobacterium phage Acadian], Mclasvirinae [Mycobacterium phage Pipefish] and Pclasvirinae [Mycobacterium phage Fishburne]), and 88 new genera including 249 species are covered in these proposals (Table 1). These proposals were submitted to the ICTV EC in 2016 for approval. In addition, another 70 phages and one archaeal virus belonging to existing genera were classified. Of particular note is a fundamental reorganization of the family Inoviridae by Petar Knezevic, Chair of the Inoviridae Study Group, who has rearranged the two existing genera (Inovirus and Plectovirus), created five new genera and 17 new species, reassigned 12 previously approved species, and deleted 29 species.
    Table 1

    Taxonomy proposals (TaxoProps) describing new taxa (families, subfamilies, genera) submitted to the ICTV Executive Committee in 2016

    Family

    Subfamily

    New genus

    Type species

    Number of new species in genus (total number of species in genus)

    Inoviridae

     

    Fibrovirus

    Vibrio virus fs1

    1 (2)

    Inoviridae

     

    Habenivirus

    Ralstonia virus RSM1

    3

    Inoviridae

     

    Lineavirus

    Salmonella virus Ike

    0 (2)

    Inoviridae

     

    Saetivirus

    Vibrio virus fs2

    1 (2)

    Inoviridae

     

    Vespertiliovirus

    Spiroplasma virus R8A2B

    1 (3)

    Myoviridae

    Ounavirinae

    Ea214virus

    Erwinia virus Ea214

    1 (2)

    Myoviridae

    Ounavirinae

    Mooglevirus

    Citrobacter virus Moogle

    2

    Myoviridae

    Ounavirinae

    Suspvirus

    Escherichia virus SUSP1

    2

    Myoviridae

    Spounavirinae

    Tsarbombavirus

    Bacillus virus TsarBomba

    2

    Myoviridae

    Tevenvirinae

    Jd18virus

    Klebsiella virus JD18

    2

    Myoviridae

    Tevenvirinae

    Kp15virus

    Klebsiella virus KP15

    5

    Myoviridae

    Tevenvirinae

    Moonvirus

    Citrobacter virus Moon

    2

    Myoviridae

     

    Abouovirus

    Brevibacillus virus Abouo

    2

    Myoviridae

     

    Agrican357virus

    Erwinia virus Ea35-70

    5

    Myoviridae

     

    Arv1virus

    Arthobacter virus ArV1

    2

    Myoviridae

     

    Elvirus

    Pseudomonas virus EL

    0 (1)

    Myoviridae

     

    Jimmervirus

    Brevibacillus virus Jimmer

    2

    Myoviridae

     

    M12virus

    Sinorhizobium virus M12

    3

    Myoviridae

     

    Marthavirus

    Arthrobacter virus Martha

    4

    Myoviridae

     

    Msw3virus

    Edwardsiella virus MSW3

    2

    Myoviridae

     

    Rsl2virus

    Ralstonia virus RSL2

    2

    Myoviridae

     

    Rslunavirus

    Ralstonia virus RSL1

    1

    Myoviridae

     

    Sep1virus

    Staphylococcus virus SEP1

    2

    Myoviridae

     

    Spn3virus

    Salmonella virus SPN3US

    1

    Podoviridae

    Autographivirinae

    Fri1virus

    Acinetobacter virus Fri1

    7

    Podoviridae

    Autographivirinae

    Kp32virus

    Klebsiella virus KP32

    6

    Podoviridae

    Autographivirinae

    Pradovirus

    Xylella virus Prado

    3

    Podoviridae

    Picovirinae

    Cp1virus

    Streptococcus virus Cp1

    1

    Podoviridae

    Sepvirinae

    Nona33virus

    Escherichia virus 933 W

    5

    Podoviridae

    Sepvirinae

    Pocjvirus

    Shigella virus POCJ13

    2

    Podoviridae

    Sepvirinae

    Tl2011virus

    Escherichia virus TL2011

    4

    Podoviridae

     

    Ea92virus

    Erwinia virus Ea9-2

    2

    Podoviridae

     

    Kf1virus

    Edwardsiella virus KF1

    1

    Podoviridae

     

    Kpp25virus

    Pseudomonas virus KPP25

    2

    Podoviridae

     

    Luz7virus

    Pseudomonas virus LUZ7

    2

    Podoviridae

     

    Prtbvirus

    Brucella virus Pr

    2

    Podoviridae

     

    Una961virus

    Helicobacter virus 1961P

    3

    Siphoviridae

    Arquatrovirinae

    Camvirus

    Streptomyces virus phiCam

     2

    Siphoviridae

    Arquatrovirinae

    Likavirus

    Streptomyces virus Lika

    9

    Siphoviridae

    Arquatrovirinae

    R4virus

    Streptomyces virus R4

    2

    Siphoviridae

    Bclasvirinae

    Acadianvirus

    Mycobacterium virus Acadian

    2 (3)

    Siphoviridae

    Bclasvirinae

    Coopervirus

    Mycobacterium virus Cooper

    5 (10)

    Siphoviridae

    Bclasvirinae

    Pipefishvirus

    Mycobacterium virus Pipefish

    1 (4)

    Siphoviridae

    Bclasvirinae

    Rosebushvirus

    Mycobacterium virus Rosebush

    1 (2)

    Siphoviridae

    Mclasvirinae

    Bongovirus

    Mycobacterium virus Bongo

    0 (1)

    Siphoviridae

    Pclasvirinae

    Fishburnevirus

    Mycobacterium virus Fishburne

    4 (5)

    Siphoviridae

    Pclasvirinae

    Phayoncevirus

    Mycobacterium virus Phayonce

    1

    Siphoviridae

     

    Ab18virus

    Pseudomonas virus Ab18

    3

    Siphoviridae

     

    Amigovirus

    Arthrobacter virus Amigo

    1

    Siphoviridae

     

    Bennievirus

    Arthrobacter virus Bennie

    9

    Siphoviridae

     

    Bernal13virus

    Mycobacterium virus Bernal13

    1

    Siphoviridae

     

    Cronusvirus

    Rhodobacter virus RcCronus

    1

    Siphoviridae

     

    Decurrovirus

    Arthrobacter virus Decurro

    1

    Siphoviridae

     

    Demosthenesvirus

    Gordonia virus Demosthenes

    3

    Siphoviridae

     

    Eiauvirus

    Edwardsiella virus eiAU

    1

    Siphoviridae

     

    Gaiavirus

    Mycobacterium virus Gaia

    1

    Siphoviridae

     

    Gilesvirus

    Mycobacterium virus Giles

    1

    Siphoviridae

     

    Gordonvirus

    Arthrobacter virus Gordon

    2

    Siphoviridae

     

    Gordtnkvirus

    Gordonia virus GordTnk2

    1

    Siphoviridae

     

    Harrisonvirus

    Paenibacillus virus Harrison

    1

    Siphoviridae

     

    Jenstvirus

    Brevibacillus virus Jenst

    1

    Siphoviridae

     

    Jwxvirus

    Achromobacter virus JWX

    2

    Siphoviridae

     

    Kelleziovirus

    Arthrobacter virus Kellezio

    2

    Siphoviridae

     

    Laroyevirus

    Arthrobacter virus Laroye

    1

    Siphoviridae

     

    Marvinvirus

    Mycobacterium virus Marvin

    2

    Siphoviridae

     

    Mudcatvirus

    Arthrobacter virus Mudcat

    2

    Siphoviridae

     

    Np1virus

    Pseudomonas virus NP1

    2

    Siphoviridae

     

    P12002virus

    Polaribacter virus P12002L

    2

    Siphoviridae

     

    P12024virus

    Nonlabens virus P12024S

    2

    Siphoviridae

     

    Pa6virus

    Propionibacterium virus PA6

    57

    Siphoviridae

     

    PaMx74virus

    Pseudomonas virus PaMx74

    2

    Siphoviridae

     

    Patiencevirus

    Mycobacterium virus Patience

    0 (1)

    Siphoviridae

     

    Pepy6virus

    Rhodococcus virus Pepy6

    2

    Siphoviridae

     

    Pis4avirus

    Aeromonas virus pIS4A

    1

    Siphoviridae

     

    Rdjlvirus

    Roseobacter virus RDJL1

    2

    Siphoviridae

     

    Rer2virus

    Rhodococcus virus RER2

    1

    Siphoviridae

     

    Send513virus

    Mycobacterium virus Send513

    2

    Siphoviridae

     

    Smoothievirus

    Gordonia virus Smoothie

    4

    Siphoviridae

     

    Soupsvirus

    Gordonia virus Soups

    1

    Siphoviridae

     

    Tankvirus

    Arthrobacter virus Tank

    1

    Siphoviridae

     

    Tin2virus

    Tsukamurella virus TIN2

    3

    Siphoviridae

     

    Titanvirus

    Rhodobacter virus RcTitan

    2

    Siphoviridae

     

    Vegasvirus

    Paenibacillus virus Vegas

    1

    Siphoviridae

     

    Vendettavirus

    Gordonia virus Vendetta

    1

    Siphoviridae

     

    Wildcatvirus

    Mycobacterium virus Wildcat

    1

    Siphoviridae

     

    Woesvirus

    Gordonia virus Woes

    3

    Siphoviridae

     

    Ydn12virus

    Streptomyces virus YDN12

    2

    Tristromaviridae

     

    Alphatristromavirus

    Pyrobaculum filamentous virus 1

    1 (2)

     

Notes

Acknowledgements

The committee would like to thank Dr. Igor Tolstoy (NCBI) for making available unpublished data on the structure of the NCBI viral database, and Dr. Graham Hatfull (University of Pittsburgh) for permitting us to use Actinobacteriophage Database electron micrographs in this year’s taxonomy proposals. The authors thank Laura Bollinger (NIH/NIAID Integrated Research Facility at Fort Detrick, Frederick, MD, USA) for editing this paper.

Compliance with ethical standards

The views and conclusions contained in this document are those of the authors and should not be interpreted as necessarily representing the official policies, either expressed or implied, of the US Department of Health and Human Services or of the institutions and companies affiliated with the authors.

Funding

This work was funded in part through Battelle Memorial Institute’s prime contract with the US National Institute of Allergy and Infectious Diseases (NIAID) under Contract No. HHSN272200700016I. A subcontractor to Battelle Memorial Institute who performed this work is: J.H.K., an employee of Tunnell Government Services, Inc. B.E.D. was supported by the Netherlands Organization for Scientific Research (NWO) Vidi Grant 864.14.004. R.A.E was supported by grant MCB-1330800 from the National Science Foundation. J.R.B. was supported by the Intramural Research Program of the National Institutes of Health, National Library of Medicine. R.L. is a member of the phagebiotics research community, supported by FWO Vlaanderen. M.M.P. was supported by the Academy of Finland (272507 and 250113). A.G. was supported by the National Fund for Scientific Research (FNRS). H.M.O. was supported by University of Helsinki funding for Instruct research infrastructure, a Landmark ESFRI project. E.M.A was funded by project funding from the National Environmental Research Council (NERC, UK) and a Postdoctoral Fellowship from the Claude Leon Foundation (South Africa).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

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Copyright information

© Springer-Verlag Wien (Outside the USA) 2016

Authors and Affiliations

  1. 1.Institute of Integrative BiologyUniversity of LiverpoolLiverpoolUnited Kingdom
  2. 2.Unit of Molecular Biology of the Gene in Extremophiles, Department of MicrobiologyInstitut PasteurParisFrance
  3. 3.Department of Biology and Ecology, Faculty of SciencesUniversity of Novi SadNovi SadSerbia
  4. 4.L’Institut de biologie intégrative et des systemsUniversité LavalQuebecCanada
  5. 5.Department of Molecular Virology, Institute of Experimental BiologyAdam Mickiewicz UniversityPoznanPoland
  6. 6.National Center for Biotechnology Information, National Library of MedicineNational Institutes of HealthBethesdaUSA
  7. 7.Department of Infection, Immunity and InflammationUniversity of LeicesterLeicesterUK
  8. 8.Department of Ecology, Evolution and Natural ResourcesRutgers UniversityNew BrunswickUSA
  9. 9.Theoretical Biology and BioinformaticsUtrecht UniversityUtrechtThe Netherlands
  10. 10.Centre for Molecular and Biomolecular InformaticsRadboud University Medical CentreNijmegenThe Netherlands
  11. 11.Departments of Computer Science and BiologySan Diego State UniversitySan DiegoUSA
  12. 12.Laboratoire Microorganismes: Génome et Environnement, Clermont UniversitéUniversité Blaise PascalClermont-FerrandFrance
  13. 13.CNRS UMR 6023, LMGEAubièreFrance
  14. 14.Department of MicrobiologyThe Ohio State UniversityColumbusUSA
  15. 15.Institute of Food, Nutrition and Health, ETH ZurichZurichSwitzerland
  16. 16.Departments of Food ScienceMolecular and Cellular Biologyand PathobiologyUniversity of GuelphGuelphCanada
  17. 17.Laboratory of Gene TechnologyKU LeuvenLeuvenBelgium
  18. 18.Department of BiosciencesUniversity of HelsinkiHelsinkiFinland
  19. 19.Latvian Biomedical Research and Study CenterRigaLatvia
  20. 20.Leibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbHBraunschweigGermany
  21. 21.Institute of BiotechnologyUniversity of HelsinkiHelsinkiFinland
  22. 22.Laboratory of Food and Environmental MicrobiologyUniversité catholique de LouvainLouvain-la-NeuveBelgium
  23. 23.Integrated Research Facility at Fort DetrickNational Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort DetrickFrederickUSA
  24. 24.Centre for Microbial Ecology and Genomics, Department of GeneticsUniversity of PretoriaPretoriaSouth Africa

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