Virus Genes

, Volume 52, Issue 1, pp 117–126 | Cite as

Genomic characterization of Salmonella bacteriophages isolated from India

  • Yogesh A. KarpeEmail author
  • Gayatri D. Kanade
  • Kunal D. Pingale
  • Vidya A. Arankalle
  • Kalyan Banerjee


Salmonella are a medically important Gram-negative foodborne pathogen. Genomic diversity of Salmonella is increasingly studied but at the same time, we have limited knowledge of Salmonella phage diversity. In this study, we have isolated Salmonella phages from sewage and river water. Genomic characterization of 12 Salmonella phages was carried out using next-generation sequencing platform. Newly sequenced phages were classified based on amino acid sequence phylogenetic analysis. In newly sequenced phages, several virulence genes, DNA metabolism genes, tRNA genes, antibiotic resistance genes and genes not having known role in the life cycle of phages were identified. Annotations of newly sequenced phage genome showed the presence of polymyxin-b resistance gene and penicillin binding protein. Annotation identified number of genes which are involved in DNA metabolism. Results suggest that most of the phages having G + C content different than their host possess DNA metabolism genes. The presence of tRNAs in the genome of Salmonella_phage38-India was identified; however, we did not observe any correlation between tRNA genes and overall codon usage in the phage genome. It is suggested that the phage-encoded tRNAs may increase fitness of phages. In summary, we isolated novel Salmonella phages, determined full genome sequences and provided phylogenetic analysis-based classification.


Virus Bacteriophages Salmonella bacteriophages Bacteriophage genome 



Authors are thankful to Dr. K. M. Paknikar, Director, MACS-ARI, Pune for all support. Authors are grateful to Dr. H. W. Ackermann and Dr. H. Gelderblom for electron microscopy analysis. Authors are thankful to Ms. Rupali Bambe for technical support, also authors are thankful to Ms. Priyanka Patel for carrying out phylogenetic analysis.

Authors contribution

Conceived and designed the experiments: YK, KB, VA; Performed the experiments: GK, KP, YK; Performed the phylogenetic analysis: VA; Analyzed the data: YK, GK, KP; Wrote the manuscript: YK, GK, KP, VA, KB.


This work is funded by the intramural Grant of Agharkar Research Institute, Pune (VIR001).

Compliance with ethical standards

Conflict of interest

The authors have declared that he/she has no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors.

Human and animal rights and Informed consent

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

Supplementary material

11262_2015_1269_MOESM1_ESM.docx (23 kb)
Supplementary material 1 (DOCX 22 kb)
11262_2015_1269_MOESM2_ESM.docx (16 kb)
Supplementary material 2 (DOCX 15 kb)


  1. 1.
    E. Kutter, D. DeVos, G. Gvasalia, Z. Alavidze, L. Gogokhia, S. Kuhl, S.T. Abedon, Curr. Pharm. Biotechnol. 11, 69–86 (2010)CrossRefPubMedGoogle Scholar
  2. 2.
    M. Sharma, Bacteriophage 3, 1–6 (2013)CrossRefGoogle Scholar
  3. 3.
    S.A. Jassim, R.G. Limoges, World J. Microbiol. Biotechnol. 30, 2153–2170 (2014)PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    G.F. Hatfull, R.W. Hendrix, Curr. Opin. Virol. 1, 298–303 (2011)PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    F. Rohwer, Cell 113, 141 (2003)CrossRefPubMedGoogle Scholar
  6. 6.
    A.I.M. Switt, R.H. Orsi, H.C. Bakker, K. Vongkamjan, C. Altier, M. Wiedmann, BMC Genom. 14(481), 1–15 (2013)Google Scholar
  7. 7.
    K.J. Cummings, L.D. Warnick, M. Elton, Y.T. Gröhn, P.L. McDonough, J.D. Siler, Foodborne Pathog. Dis. 7, 815–823 (2010)PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    G. Hitch, J. Pratten, P.W. Taylor, Lett. Appl. Microbiol. 39, 215–219 (2004)CrossRefPubMedGoogle Scholar
  9. 9.
    H. Anany, E.J. Lingohr, A. Villegas, H.W. Ackermann, Y.M. She, M.W. Griffiths, A.M. Kropinski, Virol. J. 8, 242 (2011)PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    H. Shin, J.H. Lee, H. Kim, Y. Choi, S. Heu, S. Ryu, PLoS One 7(8), e43392 (2012)PubMedCentralCrossRefPubMedGoogle Scholar
  11. 11.
    S.J. Olsen, R. Bishop, F.W. Brenner, T.H. Roels, N. Bean, R.V. Tauxe, L. Slutsker, J. Infect. Dis. 183(5), 753–761 (2001)CrossRefPubMedGoogle Scholar
  12. 12.
    X. Li, L.A. Bethune, Y. Jia, R.A. Lovell, T.A. Proescholdt, S.A. Benz, T.C. Schell, G. Kaplan, D.G. McChesney, Foodborne Pathog. Dis. 9(8), 692–698 (2012)CrossRefPubMedGoogle Scholar
  13. 13.
    E. J, Summer, Methods Mol Biol, 502, 27-46(2009)Google Scholar
  14. 14.
    J.D. Thompson, D.G. Higgins, T.J. Gibson, Nucleic Acids Res. 22, 4673–4680 (1994)PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, S. Kumar, Mol. Biol. Evol. 28, 2731–2739 (2011)PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    D.V. Bhensdadia, H.D. Bhimani, N.M. Nathani, C.M. Rawal, P.G. Koringa, C.G. Joshi, C.R. Kothari, R.K. Kothari, Next Gener. Seq. Appl. 1(101), 1–7 (2014)Google Scholar
  17. 17.
    A.P. Zavascki, L.Z. Goldani, J. Li, R.L. Nation, J. Antimicrob. Chemother. 60(6), 1206–1215 (2007)CrossRefPubMedGoogle Scholar
  18. 18.
    N. Ghosh, T.J. McKillop, T.A. Jowitt, M. Howard, H. Davies, D.F. Holmes, I.S. Roberts, J. Bella, PLoS One 7(6), e37872 (2012)PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    C.M. Guinane, P.D. Cotter, R.P. Ross, C. Hill, Antimicrob. Agents Chemother. 50(8), 2824–2828 (2006)PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    R.W. Hendrix, Curr. Opin. Microbiol. 6, 506–511 (2003)CrossRefPubMedGoogle Scholar
  21. 21.
    H. Brussow, R.W. Hendrix, Cell 108, 13–16 (2002)CrossRefPubMedGoogle Scholar
  22. 22.
    A. Singh, S.K. Arya, N. Glass, P. Hanifi-Moghaddam, R. Naidoo, C.M. Szymanskic, J. Tanha, S. Evoy, Biosens. Bioelectron. 26, 131–138 (2010)CrossRefPubMedGoogle Scholar
  23. 23.
    D. Andres, U. Baxa, C. Hanke, R. Seckler, S. Barbirz, Biochem. Soc. Trans. 38(5), 1386–1389 (2010)CrossRefPubMedGoogle Scholar
  24. 24.
    H.W. Ackermann, M.S. DuBow, M. Gershman, B. Karska-Wysocki, S.S. Kasatiya, M.J. Loessner, M.D. Mamet-Bratley, M. Regue, Arch. Virol. 142, 1381–1390 (1997)CrossRefPubMedGoogle Scholar
  25. 25.
    M.K. Waldor, J.J. Mekalanos, Science 272(5270), 1910–1914 (1996)CrossRefPubMedGoogle Scholar
  26. 26.
    H. Brussow, C. Canchaya, W.D. Hardt, Microbiol. Mol. Biol. Rev. 68(3), 560–602 (2004)PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    A.D. Brabban, E. Hite, T.R. Callaway, Foodborne Pathog. Dis. 2, 287–303 (2005)CrossRefPubMedGoogle Scholar
  28. 28.
    J.H. Paul, S.C. Jiang, Marine Microbiology-Methods in Microbiology (Academic Press, London, 2001), pp. 106–125Google Scholar
  29. 29.
    F. Baggi, A. Demarta, R. Peduzzi, Res. Microbiol. 152, 743–751 (2001)CrossRefPubMedGoogle Scholar
  30. 30.
    A.E. Durán, M. Muniesa, X. Méndez, F. Valero, F. Lucena, J. Jofre, J. Appl. Microbiol. 92, 338–347 (2002)CrossRefPubMedGoogle Scholar
  31. 31.
    M. Colomer-Lluch, L. Imamovic, J. Jofre, M. Muniesa, Antimicrob. Agents Chemother. 55, 4908–4911 (2011)PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    M. Bailly-Bechet, M. Vergassola, E. Rocha, Genome Res. 17, 1486–1495 (2007)PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Yogesh A. Karpe
    • 1
    Email author
  • Gayatri D. Kanade
    • 1
  • Kunal D. Pingale
    • 1
  • Vidya A. Arankalle
    • 1
  • Kalyan Banerjee
    • 1
  1. 1.Nanobioscience GroupAgharkar Research InstitutePuneIndia

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