Skip to main content

Taxonomic reassessment of N4-like viruses using comparative genomics and proteomics suggests a new subfamily - “Enquartavirinae”

Archives of Virology volume 160, pages 3053–3062 (2015)Cite this article

Abstract

The GenBank database currently contains sequence data for 33 N4-like viruses, with only one, Escherichia phage N4, being formally recognized by the ICTV. The genus N4likevirus is uniquely characterized by that fact that its members possess an extremely large, virion-associated RNA polymerase. Using a variety of proteomic, genomic and phylogenetic tools, we have demonstrated that the N4-like phages are not monophyletic and that N4 is actually a genomic orphan. We propose to create four new genera: “G7cvirus” (consisting of phages G7C, IME11, KBNP21, vB_EcoP_PhAPEC5, vB_EcoP_PhAPEC7, Bp4, EC1-UPM and pSb-1), “Lit1virus” (LIT1, PA26 and vB_PaeP_C2-10_Ab09), “Sp58virus” (SP058 and SP076), and “Dss3virus” (DSS3φ2 and EE36φ1). We propose that coliphage N4, the members of “G7cvirus”, Erwinia phage Ea9-2, and Achromobacter phage JWAlpha should be considered members of the same subfamily, which we tentatively call the “Enquartavirinae”.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  1. Schito GC, Rialdi G, Pesce A (1966) Biophysical properties of N4 coliphage. Biochim Biophys Acta 129:482–490

    CAS  Article  PubMed  Google Scholar 

  2. Paddison P, Abedon ST, Dressman HK, Gailbreath K, Tracy J et al (1998) The roles of the bacteriophage T4 r genes in lysis inhibition and fine-structure genetics: a new perspective. Genetics 148:1539–1550

    PubMed Central  CAS  PubMed  Google Scholar 

  3. Ohmori H, Haynes LL, Rothman-Denes LB (1988) Structure of the ends of the coliphage N4 genome. J Mol Biol 202:1–10

    CAS  Article  PubMed  Google Scholar 

  4. Ackermann H-W, DuBow M (1987) Natural groups of bacteriophages. Viruses of prokaryotes. CRC Press, Boca Raton, pp 85–100

    Google Scholar 

  5. Van Regenmortel M (2000) Virus taxonomy. Classification and nomenclature of viruses. VIIth report of the International Committee of Viruses, San Diego, p 108

  6. Zhao Y, Wang K, Jiao N, Chen F (2009) Genome sequences of two novel phages infecting marine roseobacters. Environ Microbiol 11:2055–2064

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  7. Wittmann J, Dreiseikelmann B, Rohde M, Meier-Kolthoff JP, Bunk B et al (2014) First genome sequences of Achromobacter phages reveal new members of the N4 family. Virol J 11:14

    PubMed Central  Article  PubMed  Google Scholar 

  8. Ceyssens PJ, Brabban A, Rogge L, Lewis MS, Pickard D et al (2010) Molecular and physiological analysis of three Pseudomonas aeruginosa phages belonging to the “N4-like viruses”. Virology 405:26–30

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  9. Fouts DE, Klumpp J, Bishop-Lilly KA, Rajavel M, Willner KM et al (2013) Whole genome sequencing and comparative genomic analyses of two Vibrio cholerae O139 Bengal-specific Podoviruses to other N4-like phages reveal extensive genetic diversity. Virol J 10:165

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  10. Kazmierczak KM, Rothman-Denes LB (2006) Bacteriophage N4. In: Calendar R (ed) The bacteriophages, 2nd edn. Oxford University Pres, New York, pp 302–314

    Google Scholar 

  11. Falco SC, Laan KV, Rothman-Denes LB (1977) Virion-associated RNA polymerase required for bacteriophage N4 development. Proc Natl Acad Sci USA 74:520–523

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  12. Zivin R, Zehring W, Rothman-Denes LB (1981) Transcriptional map of bacteriophage N4: Location and polarity of N4 RNAs. J Mol Biol 152:335–356

    CAS  Article  PubMed  Google Scholar 

  13. Kulikov E, Kropinski AM, Golomidova A, Lingohr E, Govorun V et al (2012) Isolation and characterization of a novel indigenous intestinal N4-related coliphage vB_EcoP_G7C. Virology 426:93–99

    CAS  Article  PubMed  Google Scholar 

  14. Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  15. Willis SH, Kazmierczak KM, Carter RH, Rothman-Denes LB (2002) N4 RNA polymerase II, a heterodimeric RNA polymerase with homology to the single-subunit family of RNA polymerases. J Bacteriol 184:4952–4961

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  16. Krumsiek J, Arnold R, Rattei T (2007) Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23:1026–1028

    CAS  Article  PubMed  Google Scholar 

  17. Zafar N, Mazumder R, Seto D (2002) CoreGenes: a computational tool for identifying and cataloging “core” genes in a set of small genomes. BMC Bioinform 3:12

    Article  Google Scholar 

  18. Bao Y, Chetvernin V, Tatusova T (2014) Improvements to pairwise sequence comparison (PASC): a genome-based web tool for virus classification. Arch Virol

  19. Niu YD, McAllister TA, Nash JH, Kropinski AM, Stanford K (2014) Four Escherichia coli O157:H7 phages: a new bacteriophage genus and taxonomic classification of T1-like phages. PLoS One 9:e100426

    PubMed Central  Article  PubMed  Google Scholar 

  20. Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P et al (2009) Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9:224

    PubMed Central  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  22. Choi KH, McPartland J, Kaganman I, Bowman VD, Rothman-Denes LB et al (2008) Insight into DNA and protein transport in double-stranded DNA viruses: the structure of bacteriophage N4. J Mol Biol 378:726–736

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  23. Born Y, Fieseler L, Marazzi J, Lurz R, Duffy B et al (2011) Novel virulent and broad-host-range Erwinia amylovora bacteriophages reveal a high degree of mosaicism and a relationship to Enterobacteriaceae phages. Appl Environ Microbiol 77:5945–5954

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  24. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  25. Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:1009–1010

    PubMed Central  CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Professor Manfred Rohde (Helmholtz Centre for Infection Research) for the TEM picture of phage JWDelta.

Author information

Affiliations

  1. Leibniz Institute DSMZ, German Collection of Microorganisms and Cell Cultures, Inhoffenstrasse 7B, 38124, Braunschweig, Germany

    Johannes Wittmann

  2. Institute of Food, Nutrition and Health, ETH Zurich, Schmelzbergstrasse 7, 8092, Zurich, Switzerland

    Jochen Klumpp

  3. Escuela de Medicina Veterinaria, Facultad de Ecología y Recursos Naturales, Universidad Andres Bello, Republica 440, 8370251, Santiago, Chile

    Andrea I. Moreno Switt

  4. Agriculture and Agri-Food Canada, 4902 Victoria Avenue North, P.O. Box 6000, Vineland Station, ON, L0R 2E0, Canada

    Abdelbaset Yagubi & Antonet Svircev

  5. Department of Microbiology, Immunology, and Infectiology, Faculty of Medicine, Laval University, Quebec, QC, G1X 4C6, Canada

    Hans-Wolfgang Ackermann

  6. Laboratory of Food Safety, Department of Food Science, Cornell University, Ithaca, NY, 14850, USA

    Martin Wiedmann

  7. Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, Guelph, ON, N1G 3W4, Canada

    John H. E. Nash

  8. Department of Food Science, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Andrew M. Kropinski

  9. Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Andrew M. Kropinski

  10. Department of Pathobiology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Andrew M. Kropinski

Authors
  1. Johannes Wittmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jochen Klumpp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrea I. Moreno Switt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdelbaset Yagubi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hans-Wolfgang Ackermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Martin Wiedmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Antonet Svircev
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. John H. E. Nash
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Andrew M. Kropinski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew M. Kropinski.

Electronic supplementary material

Below is the link to the electronic supplementary material.

705_2015_2609_MOESM1_ESM.tif

Supplementary Figure S1 Composite figure of negatively stained phage PhiJA1 stained with uranyl acetate (A); B. PhiJA1 with ammonium molybdate; C. JWDelta; D. N4 stained with phosphotungstate; and E. Salmonella phage SP058. (TIFF 1639 kb)

705_2015_2609_MOESM2_ESM.tif

Supplementary Figure S2. Overall DNA identities between the N4-like phages, calculated using BLASTN and multiplying the % coverage by the % identity. (TIFF 746 kb)

Supplementary material 3 (DOCX 17 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wittmann, J., Klumpp, J., Moreno Switt, A.I. et al. Taxonomic reassessment of N4-like viruses using comparative genomics and proteomics suggests a new subfamily - “Enquartavirinae”. Arch Virol 160, 3053–3062 (2015). https://doi.org/10.1007/s00705-015-2609-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-015-2609-6

Keywords

  • Phage Genome
  • Endolysin
  • Portal Protein
  • Transcriptional Direction
  • Large Terminase Subunit