Archives of Virology

, Volume 160, Issue 4, pp 1021–1033 | Cite as

A proposed new bacteriophage subfamily: “Jerseyvirinae

  • Hany Anany
  • Andrea I. Moreno Switt
  • Niall De Lappe
  • Hans-Wolfgang Ackermann
  • Darren M. Reynolds
  • Andrew M. Kropinski
  • Martin Wiedmann
  • Mansel W. Griffiths
  • Denise Tremblay
  • Sylvain Moineau
  • John H. E. Nash
  • Dann Turner
Original Article

Abstract

Based on morphology and comparative nucleotide and protein sequence analysis, a new subfamily of the family Siphoviridae is proposed, named “Jerseyvirinae” and consisting of three genera, “Jerseylikevirus”, “Sp3unalikevirus” and “K1glikevirus”. To date, this subfamily consists of 18 phages for which the genomes have been sequenced. Salmonella phages Jersey, vB_SenS_AG11, vB_SenS-Ent1, vB_SenS-Ent2, vB_SenS-Ent3, FSL SP-101, SETP3, SETP7, SETP13, SE2, SS3e and wksl3 form the proposed genus “Jerseylikevirus”. The proposed genus “K1glikevirus” consists of Escherichia phages K1G, K1H, K1ind1, K1ind2 and K1ind3. The proposed genus “Sp3unalikevirus” contains one member so far. Jersey-like phages appear to be widely distributed, as the above phages were isolated in the UK, Canada, the USA and South Korea between 1970 and the present day. The distinguishing features of this subfamily include a distinct siphovirus morphotype, genomes of 40.7-43.6 kb (49.6-51.4 mol % G+C), a syntenic genome organisation, and a high degree of nucleotide sequence identity and shared proteins. All known members of the proposed subfamily are strictly lytic.

References

  1. 1.
    Ackermann H-W, Berthiaume L, Kasatiya SS (1972) Morphologie des phages de lysotypie de Salmonella paratyphi B (schéma de Felix et Callow). Can J Microbiol 18:77–81CrossRefPubMedGoogle Scholar
  2. 2.
    Ackermann HW, Gershman M (1992) Morphology of phages of a general Salmonella typing set. Res Virol 143:303–310CrossRefPubMedGoogle Scholar
  3. 3.
    Ackermann HW, DuBow MS, Gershman M, Karska-Wysocki B, Kasatiya SS, Loessner MJ, Mamet-Bratley MD, Regué M (1997) Taxonomic changes in tailed phages of enterobacteria. Arch Virol 142:1381–1390CrossRefPubMedGoogle Scholar
  4. 4.
    Alonso C, Murtaugh MP, Dee SA, Davies PR (2013) Epidemiological study of air filtration systems for preventing PRRSV infection in large sow herds. Prev Vet Med 112:109–117CrossRefPubMedGoogle Scholar
  5. 5.
    Anany H (2010) Biocontrol of foodborne bacterial pathogens using immobilized bacteriophages. Food Science. University of Guelph, GuelphGoogle Scholar
  6. 6.
    Barbirz S, Muller JJ, Uetrecht C, Clark AJ, Heinemann U, Seckler R (2008) Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Mol Microbiol 69:303–316CrossRefPubMedGoogle Scholar
  7. 7.
    Brovko LY, Anany H, Griffiths MW (2012) Bacteriophages for detection and control of bacterial pathogens in food and food-processing environment. Adv Food Nutr Res 67:241–288CrossRefPubMedGoogle Scholar
  8. 8.
    Bull JJ, Vimr ER, Molineux IJ (2010) A tale of tails: sialidase is key to success in a model of phage therapy against K1-capsulated Escherichia coli. Virology 398:79–86CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Byl CV, Kropinski AM (2000) Sequence of the genome of Salmonella bacteriophage P22. J Bacteriol 182:6472–6481CrossRefPubMedCentralGoogle Scholar
  10. 10.
    Carey-Smith GV, Billington C, Cornelius AJ, Hudson JA, Heinemann JA (2006) Isolation and characterization of bacteriophages infecting Salmonella spp. FEMS Microbiol Lett 258:182–186CrossRefPubMedGoogle Scholar
  11. 11.
    Chibani-Chennoufi S, Sidoti J, Bruttin A, Dillmann M-L, Kutter E, Qadri F, Sarker SA, Brüssow H (2004) Isolation of Escherichia coli bacteriophages from the stool of pediatric diarrhea patients in Bangladesh. J Bacteriol 186:8287–8294CrossRefPubMedCentralPubMedGoogle Scholar
  12. 12.
    Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome Alignment with gene gain, loss and rearrangement. PLoS One 5:e11147CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    De Lappe N, Doran G, O’Connor J, O’Hare C, Cormican M (2009) Characterization of bacteriophages used in the Salmonella enterica serovar Enteritidis phage-typing scheme. J Med Microbiol 58:86–93CrossRefPubMedGoogle Scholar
  14. 14.
    Demczuk W, Ahmed R, Ackermann H-W (2004) Morphology of Salmonella enterica serovar Heidelberg typing phages. Can J Microbiol 50:873–875CrossRefPubMedGoogle Scholar
  15. 15.
    Denyes J, Krell P, Manderville R, Ackermann H-W, She Y-M, Kropinski A (2014) The genome and proteome of Serratia bacteriophage eta which forms unstable lysogens. Virol J 11:6CrossRefPubMedCentralPubMedGoogle Scholar
  16. 16.
    Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Fokine A, Leiman PG, Shneider MM, Ahvazi B, Boeshans KM, Steven AC, Black LW, Mesyanzhinov VV, Rossmann MG (2005) Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc Natl Acad Sci USA 102:7163–7168CrossRefPubMedCentralPubMedGoogle Scholar
  18. 18.
    Fraser JS, Yu Z, Maxwell KL, Davidson AR (2006) Ig-like domains on bacteriophages: a tale of promiscuity and deceit. J Mol Biol 359:496–507CrossRefPubMedGoogle Scholar
  19. 19.
    Gajewski S, Webb MR, Galkin V, Egelman EH, Kreuzer KN, White SW (2011) Crystal structure of the phage T4 recombinase UvsX and its functional interaction with the T4 SF2 helicase UvsW. J Mol Biol 405:65–76CrossRefPubMedCentralPubMedGoogle Scholar
  20. 20.
    Gilcrease EB, Winn-Stapley DA, Hewitt FC, Joss L, Casjens SR (2005) nucleotide sequence of the head assembly gene cluster of bacteriophage L and decoration protein characterization. J Bacteriol 187:2050–2057CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Grant J, Arantes A, Stothard P (2012) Comparing thousands of circular genomes using the CGView Comparison Tool. BMC Genomics 13:202CrossRefPubMedCentralPubMedGoogle Scholar
  22. 22.
    Grimont PAD, Weill F-X (2007) Antigenic formulae of the Salmonella serovars. WHO Collaborating Centre for Reference and Research on Salmonella, Paris, France, p 166Google Scholar
  23. 23.
    Grose JH, Casjens SR (2014) Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae. Virology 468–470:421–443CrossRefPubMedGoogle Scholar
  24. 24.
    Hagens S, Loessner MJ (2010) Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Curr Pharm Biotechnol 11:58–68CrossRefPubMedGoogle Scholar
  25. 25.
    Hong S, Jeong J, Lee J, Kim S, Min W, Myung H (2013) Therapeutic effects of bacteriophages against Salmonella gallinarum infection in chickens. J Microbiol Biotechnol 23:1478–1483CrossRefPubMedGoogle Scholar
  26. 26.
    Hooton SPT, Atterbury RJ, Connerton IF (2011) Application of a bacteriophage cocktail to reduce Salmonella Typhimurium U288 contamination on pig skin. Int J Food Microbiol 151:157–163CrossRefPubMedGoogle Scholar
  27. 27.
    Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong S-Y, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Joshi A, Siddiqi JZ, Rao GR, Chakravorty M (1982) MB78, a virulent bacteriophage of Salmonella typhimurium. J Virol 41:1038–1043PubMedCentralPubMedGoogle Scholar
  29. 29.
    Kang H-W, Kim J-W, Jung T-S, Woo G-J (2013) wksl3, a New biocontrol agent for Salmonella enterica serovars enteritidis and typhimurium in foods: characterization, application, sequence analysis, and oral acute toxicity study. Appl Environ Microbiol 79:1956–1968CrossRefPubMedCentralPubMedGoogle Scholar
  30. 30.
    Kim S-H, Park J-H, Lee B-K, Kwon H-J, Shin J-H, Kim J, Kim S (2012) Complete genome sequence of Salmonella bacteriophage SS3e. J Virol 86:10253–10254CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580CrossRefPubMedGoogle Scholar
  32. 32.
    Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327CrossRefPubMedGoogle Scholar
  33. 33.
    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  34. 34.
    Lavigne R, Seto D, Mahadevan P, Ackermann H-W, Kropinski AM (2008) Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 159:406–414CrossRefPubMedGoogle Scholar
  35. 35.
    Lavigne R, Darius P, Summer E, Seto D, Mahadevan P, Nilsson A, Ackermann H, Kropinski A (2009) Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9:224CrossRefPubMedCentralPubMedGoogle Scholar
  36. 36.
    Lawrence JG, Hatfull GF, Hendrix RW (2002) Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 184:4891–4905CrossRefPubMedCentralPubMedGoogle Scholar
  37. 37.
    Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189CrossRefPubMedCentralPubMedGoogle Scholar
  38. 38.
    Lima-Mendez G, Van Helden J, Toussaint A, Leplae R (2008) Reticulate representation of evolutionary and functional relationships between phage genomes. Mol Biol Evol 25:762–777CrossRefPubMedGoogle Scholar
  39. 39.
    Lima-Mendez G, Toussaint A, Leplae R (2011) A modular view of the bacteriophage genomic space: identification of host and lifestyle marker modules. Res Microbiol 162:737–746CrossRefPubMedGoogle Scholar
  40. 40.
    McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Du F, Hou S, Layman D, Leonard S, Nguyen C, Scott K, Holmes A, Grewal N, Mulvaney E, Ryan E, Sun H, Florea L, Miller W, Stoneking T, Nhan M, Waterston R, Wilson RK (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852–856CrossRefPubMedGoogle Scholar
  41. 41.
    Mollov D, Lockhart B, Zlesak D (2013) Complete nucleotide sequence of rose yellow mosaic virus, a novel member of the family Potyviridae. Arch Virol 158:1917–1923CrossRefPubMedGoogle Scholar
  42. 42.
    Moreno Switt A, Orsi R, den Bakker H, Vongkamjan K, Altier C, Wiedmann M (2013) Genomic characterization provides new insight into Salmonella phage diversity. BMC Genomics 14:481CrossRefPubMedCentralPubMedGoogle Scholar
  43. 43.
    Moreno Switt AI, den Bakker HC, Vongkamjan K, Hoelzer K, Warnick LD, Cummings KJ, Wiedmann M (2013) Salmonella bacteriophage diversity reflects host diversity on dairy farms. Food Microbiol 36:275–285CrossRefGoogle Scholar
  44. 44.
    Myers EW, Miller W (1988) Optimal alignments in linear space. Computer applications in the biosciences : CABIOS 4:11–17PubMedGoogle Scholar
  45. 45.
    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:e100426CrossRefPubMedCentralPubMedGoogle Scholar
  46. 46.
    Papanikolaou N, Trachana K, Theodosiou T, Promponas V, Iliopoulos I (2009) Gene socialization: gene order, GC content and gene silencing in Salmonella. BMC Genomics 10:597CrossRefPubMedCentralPubMedGoogle Scholar
  47. 47.
    Perler FB, Olsen GJ, Adam E (1997) Compilation and analysis of intein sequences. Nucleic Acids Res 25:1087–1093CrossRefPubMedCentralPubMedGoogle Scholar
  48. 48.
    Rohwer F, Edwards R (2002) The phage proteomic tree: a genome-based taxonomy for phage. J Bacteriol 184:4529–4535CrossRefPubMedCentralPubMedGoogle Scholar
  49. 49.
    Schwarzer D, Stummeyer K, Gerardy-Schahn R, Muhlenhoff M (2007) Characterization of a novel intramolecular chaperone domain conserved in endosialidases and other bacteriophage tail spike and fiber proteins. J Biol Chem 282:2821–2831CrossRefPubMedGoogle Scholar
  50. 50.
    Söding J (2005) Protein homology detection by HMM–HMM comparison. Bioinformatics 21:951–960CrossRefPubMedGoogle Scholar
  51. 51.
    Söding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248CrossRefPubMedCentralPubMedGoogle Scholar
  52. 52.
    Spinelli S, Bebeacua C, Orlov I, Tremblay D, Klaholz BP, Moineau S, Cambillau C (2014) Cryo-electron microscopy structure of lactococcal siphophage 1358 virion. J Virol 88:8900–8910CrossRefPubMedCentralPubMedGoogle Scholar
  53. 53.
    Summer EJ, Gill JJ, Upton C, Gonzalez CF, Young R (2007) Role of phages in the pathogenesis of Burkholderia, or ‘where are the toxin genes in Burkholderia phages?’. Curr Opin Microbiol 10:410–417CrossRefPubMedCentralPubMedGoogle Scholar
  54. 54.
    Susskind MM, Botstein D (1975) Mechanism of action of Salmonella phage P22 antirepressor. J Mol Biol 98:413–424CrossRefPubMedGoogle Scholar
  55. 55.
    Switt AIM, Sulakvelidze A, Wiedmann M, Kropinski AM, Wishart DS, Poppe C, Liang Y (2014) Salmonella phages and prophages—genomics, taxonomy and applied aspects. In: Schatten H, Eisenstark A (eds) Salmonella: methods and protocols (methods in molecular biology). Humana Press, New YorkGoogle Scholar
  56. 56.
    Tiwari BR, Kim S, Kim J (2012) Complete genomic sequence of Salmonella enterica serovar Enteritidis phage SE2. J Virol 86:7712CrossRefPubMedCentralPubMedGoogle Scholar
  57. 57.
    Turner D, Hezwani M, Nelson S, Salisbury V, Reynolds D (2012) Characterization of the Salmonella bacteriophage vB_SenS-Ent1. J Gen Virol 93:2046–2056CrossRefPubMedGoogle Scholar
  58. 58.
    Westover KM, Rusinko JP, Hoin J, Neal M (2013) Rogue taxa phenomenon: a biological companion to simulation analysis. Mol Phylogenet Evol 69:1–3CrossRefPubMedCentralPubMedGoogle Scholar
  59. 59.
    Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, Roth JR, Baumler AJ (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426–429CrossRefPubMedCentralPubMedGoogle Scholar
  60. 60.
    Xu J, Hendrix RW, Duda RL (2004) Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol Cell 16:11–21CrossRefPubMedGoogle Scholar
  61. 61.
    Xu J, Hendrix RW, Duda RL (2013) A balanced ratio of proteins from gene G and frameshift-extended gene GT is required for phage lambda tail assembly. J Mol Biol 425:3476–3487CrossRefPubMedCentralPubMedGoogle Scholar
  62. 62.
    Xu J, Hendrix RW, Duda RL (2014) Chaperone-protein interactions that mediate assembly of the bacteriophage lambda tail to the correct length. J Mol Biol 426:1004–1018CrossRefPubMedCentralPubMedGoogle Scholar
  63. 63.
    Young R, Bläsi U (1995) Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev 17:195–205CrossRefGoogle Scholar
  64. 64.
    Zafar N, Mazumder R, Seto D (2002) CoreGenes: a computational tool for identifying and cataloging “core” genes in a set of small genomes. BMC Bioinformatics 3:12CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Hany Anany
    • 1
    • 2
  • Andrea I. Moreno Switt
    • 3
  • Niall De Lappe
    • 4
  • Hans-Wolfgang Ackermann
    • 5
  • Darren M. Reynolds
    • 8
  • Andrew M. Kropinski
    • 6
  • Martin Wiedmann
    • 7
  • Mansel W. Griffiths
    • 1
  • Denise Tremblay
    • 9
  • Sylvain Moineau
    • 9
  • John H. E. Nash
    • 10
    • 11
  • Dann Turner
    • 8
  1. 1.Canadian Research Institute for Food SafetyUniversity of GuelphGuelphCanada
  2. 2.Faculty of Science, Microbiology DepartmentAin Shams UniversityCairoEgypt
  3. 3.Facultad de Ecología y Recursos NaturalesEscuela de Medicina Veterinaria, Universidad Andres BelloSantiagoChile
  4. 4.National Salmonella, Shigella and Listeria Reference Laboratory, Medical Microbiology DepartmentUniversity Hospital GalwayGalwayIreland
  5. 5.Faculty of Medicine, Department of Microbiology, Immunology, and InfectiologyUniversité LavalQuebecCanada
  6. 6.Department of Molecular and Cellular BiologyUniversity of GuelphGuelphCanada
  7. 7.Department of Food ScienceCornell UniversityIthacaUSA
  8. 8.Faculty of Health and Applied Sciences, Centre for Research in BiosciencesUniversity of the West of EnglandBristolUK
  9. 9.Faculté des Sciences et de Génie, Département de Biochimie, de Microbiologie et de bio-informatiqueUniversité LavalQuebecCanada
  10. 10.Public Health Agency of Canada, Laboratory for Foodborne ZoonosesGuelphCanada
  11. 11.Department of PathobiologyOntario Veterinary College, University of GuelphGuelphCanada

Personalised recommendations