Skip to main content

Advertisement

SpringerLink
Log in

Genome sequence of the temperate bacteriophage PH10 from Streptococcus oralis

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Exponential growing cultures of Streptococcus oralis strain OMZ 1038, isolated from human supragingival dental plaque, were found to release a bacteriophage (designated PH10) upon treatment with mitomycin C. The complete genome sequence of phage PH10 was determined. The genome was 31276 bp in size and contained 54 open reading frames. The module encoding structural proteins was highly similar to that of Streptococcus pneumoniae prophage PhiSpn_3. The most abundant phage structural protein was encoded by ORF35 and was likely processed by proteolytic cleavage. The putative endolysin from PH10, which contained a muramidase domain and a choline-binding domain, was purified and shown to have lytic activity with S. oralis, S. pneumoniae and Streptococcus mitis, but not with other streptococcal species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. B.J. Paster, S.K. Boches, J.L. Galvin, R.E. Ericson, C.N. Lau, V.A. Levanos, A. Sahasrabudhe, F.E. Dewhirst, Bacterial diversity in human subgingival plaque. J. Bacteriol. 183, 3770–3783 (2001)

    Article  CAS  PubMed  Google Scholar 

  2. C. Pearce, G.H. Bowden, M. Evans, S.P. Fitzsimmons, J. Johnson, M.J. Sheridan, R. Wientzen, M.F. Cole, Identification of pioneer viridans streptococci in the oral cavity of human neonates. J. Med. Microbiol. 42, 67–72 (1995)

    Article  CAS  PubMed  Google Scholar 

  3. M.F. Cole, S. Bryan, M.K. Evans, C.L. Pearce, M.J. Sheridan, P.A. Sura, R. Wientzen, G.H.W. Bowden, Humoral immunity to commensal oral bacteria in human infants: salivary antibodies reactive with Actinomyces naeslundii genospecies 1 and 2 during colonization. Infect. Immun. 66, 4283–4289 (1998)

    CAS  PubMed  Google Scholar 

  4. C.W. Douglas, J. Heath, K.K. Hampton, F.E. Preston, Identity of viridans streptococci isolated from cases of infective endocarditis. J. Med. Microbiol. 39, 179–182 (1993)

    Article  CAS  PubMed  Google Scholar 

  5. L.S. Håvarstein, P. Gaustad, I.F. Nes, D.A. Morrison, Identification of the streptococcal competence-pheromone receptor. Mol. Microbiol. 21, 863–869 (1996)

    Article  PubMed  Google Scholar 

  6. F. Chi, O. Nolte, C. Bergmann, M. Ip, R. Hakenbeck, Crossing the barrier: evolution and spread of a major class of mosaic pbp2x in Streptococcus pneumoniae, S. mitis and S. oralis. Int. J. Med. Microbiol. 297, 503–512 (2007)

    Article  CAS  PubMed  Google Scholar 

  7. C.A. Tylenda, C. Calvert, P.E. Kolenbrander, A. Tylenda, Isolation of Actinomyces bacteriophage from human dental plaque. Infect. Immun. 49, 1–6 (1985)

    CAS  PubMed  Google Scholar 

  8. A.L. Delisle, C.A. Rostkowski, Lytic bacteriophages of Streptococcus mutans. Curr. Microbiol. 27, 163–167 (1993)

    Article  CAS  Google Scholar 

  9. G. Bachrach, M. Leizerovici-Zigmond, A. Zlotkin, R. Naor, D. Steinberg, Bacteriophage isolation from human saliva. Lett. Appl. Microbiol. 36, 50–53 (2003)

    Article  PubMed  Google Scholar 

  10. G. Hitch, J. Pratten, P.W. Taylor, Isolation of bacteriophages from the oral cavity. Lett. Appl. Microbiol. 39, 215–219 (2004)

    Article  CAS  PubMed  Google Scholar 

  11. R.H. Stevens, B.F. Hammond, C.H. Lai, Characterization of an inducible bacteriophage from a leukotoxic strain of Actinobacillus actinomycetemcomitans. Infect. Immun. 35, 343–349 (1982)

    CAS  PubMed  Google Scholar 

  12. I.R. Siboo, B.A. Bensing, P.M. Sullam, Genomic organization and molecular characterization of SM1, a temperate bacteriophage of Streptococcus mitis. J. Bacteriol. 185, 6968–6975 (2003)

    Article  CAS  PubMed  Google Scholar 

  13. J.R. van der Ploeg, Characterization of Streptococcus gordonii prophage PH15: complete genome sequence and functional analysis of phage-encoded integrase and endolysin. Microbiology 154, 2970–2978 (2008)

    Article  PubMed  Google Scholar 

  14. H.L. Mitchell, S.G. Dashper, D.V. Catmull, R.A. Paolini, S.M. Cleal, N. Slakeski, K.H. Tan, E.C. Reynolds, Treponema denticola biofilm-induced expression of a bacteriophage, toxin-antitoxin systems and transposases. Microbiology 156, 774–788 (2010)

    Article  CAS  PubMed  Google Scholar 

  15. P. Romero, E. García, T.J. Mitchell, Development of a prophage typing system and analysis of prophage carriage in Streptococcus pneumoniae. Appl. Environ. Microbiol. 75, 1642–1649 (2009)

    Article  CAS  PubMed  Google Scholar 

  16. R. López, E. García, Recent trends on the molecular biology of pneumococcal capsules, lytic enzymes, and bacteriophage. FEMS Microbiol. Rev. 28, 553–580 (2004)

    Article  PubMed  Google Scholar 

  17. P. Romero, R. López, E. García, Characterization of LytA-like N-acetylmuramoyl-L-alanine amidases from two new Streptococcus mitis bacteriophages provides insights into the properties of the major pneumococcal autolysin. J. Bacteriol. 186, 8229–8239 (2004)

    Article  CAS  PubMed  Google Scholar 

  18. C. Ronda, E. García, R. López, Infection of Streptococcus oralis NCTC 11427 by pneumococcal phages. FEMS Microbiol. Lett. 65, 187–192 (2001)

    Article  Google Scholar 

  19. F.M. Ausubel, R. Brent, R.E. Kingston, D.E. Moore, J.G. Seidman, J.A. Smith, K. Struhl, Current Protocols in Molecular Biology (Wiley, New York, 1987)

    Google Scholar 

  20. X. Huang, A. Madan, CAP3: A DNA sequence assembly program. Genome Res. 9, 868–877 (1999)

    Article  CAS  PubMed  Google Scholar 

  21. A. Lukashin, M. Borodovsky, GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26, 1107–1115 (1998)

    Article  CAS  PubMed  Google Scholar 

  22. M. Kilian, L. Mikkelsen, J. Henrichsen, Taxonomic study of viridans streptococci: description of Streptococcus gordonii sp. nov. and emended descriptions of Streptococcus sanguis (White and Niven 1946), Streptococcus oralis (Bridge and Sneath 1982), and Streptococcus mitis (Andrewes and Horder 1906). Int. J. Syst. Bacteriol. 39, 471–484 (1989)

    Article  Google Scholar 

  23. C. Canchaya, C. Proux, G. Fournous, A. Bruttin, H. Brüssow, Prophage genomics. Microbiol. Mol. Biol. Rev. 67, 238–276 (2003)

    Article  CAS  PubMed  Google Scholar 

  24. P. Romero, N.J. Croucher, N.L. Hiller, F.Z. Hu, G.D. Ehrlich, S.D. Bentley, E. García, T.J. Mitchell, Comparative genomic analysis of 10 Streptococcus pneumoniae temperate bacteriophages. J. Bacteriol. 191, 4854–4862 (2009)

    Article  CAS  PubMed  Google Scholar 

  25. S. Lucchini, F. Desiere, H. Brüssow, Similarly organized lysogeny modules in temperate Siphoviridae from low GC content Gram-positive bacteria. Virology 263, 427–435 (1999)

    Article  CAS  PubMed  Google Scholar 

  26. D. Llull, R. López, E. García, Skl, a novel choline-binding N-acetylmuramoyl-l-alanine amidase of Streptococcus mitis SK137 containing a CHAP domain. FEBS Lett. 580, 1959–1964 (2006)

    Article  CAS  PubMed  Google Scholar 

  27. C. Weigel, H. Seitz, Bacteriophage replication modules. FEMS Microbiol. Rev. 30, 321–381 (2006)

    Article  CAS  PubMed  Google Scholar 

  28. M. Zuniga, B. Franke-Fayard, G. Venema, J. Kok, A. Nauta, Characterization of the putative replisome organizer of the lactococcal bacteriophage r1t. J. Virol. 76, 10234–10244 (2002)

    Article  CAS  PubMed  Google Scholar 

  29. V. Obregón, P. García, R. López, J.L. García, VO1, a temperate bacteriophage of the type 19A multiresistant epidemic 8249 strain of Streptococcus pneumoniae: analysis of variability of lytic and putative C5 methyltransferase genes. Microb. Drug Resist. 9, 7–15 (2003)

    Article  PubMed  Google Scholar 

  30. M. Radlińska, A. Piekarowicz, Cloning and characterization of the gene encoding a new DNA methyltransferase from Neisseria gonorrhoeae. Biol. Chem. 379, 1391–1395 (1998)

    PubMed  Google Scholar 

  31. M. Radlińska, J.M. Bujnicki, A. Piekarowicz, Structural characterization of two tandemly arranged DNA methyltransferase genes from Neisseria gonorrhoeae MS11: N4-cytosine specific M.NgoMXV and nonfunctional 5-cytosine-type M. NgoMorf2P. Proteins 37, 717–728 (1999)

    Article  PubMed  Google Scholar 

  32. A. van Belkum, S. Scherer, L. van Alphen, H. Verbrugh, Short-sequence DNA repeats in prokaryotic genomes. Microbiol. Mol. Biol. Rev. 62, 275–293 (1998)

    PubMed  Google Scholar 

  33. G.T. Chung, J.S. Yoo, H.B. Oh, Y.S. Lee, S.H. Cha, S.J. Kim, C.K. Yoo, Complete genome sequence of Neisseria gonorrhoeae NCCP11945. J. Bacteriol. 190, 6035–6036 (2008)

    Article  CAS  PubMed  Google Scholar 

  34. E. García, J.L. García, P. García, A. Arrarás, J.M. Sánchez-Puelles, R. López, Molecular evolution of lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Proc. Natl. Acad. Sci. USA 85, 914–918 (1988)

    Article  PubMed  Google Scholar 

  35. J.A. Hermoso, B. Monterroso, A. Albert, B. Galan, O. Ahrazem, P. García, M. Martinez-Ripoll, J.L. García, M. Menéndez, Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure 11, 1239–1249 (2003)

    Article  CAS  PubMed  Google Scholar 

  36. I. Pérez-Dorado, N.E. Campillo, B. Monterroso, D. Hesek, M. Lee, J.A. Páez, P. García, M. Martínez-Ripoll, J.L. García, S. Mobashery, M. Menéndez, J.A. Hermoso, Elucidation of the molecular recognition of bacterial cell wall by modular pneumococcal phage endolysin Cpl-1. J Biol. Chem. 34, 24990–24999 (2007)

    Article  Google Scholar 

Download references

Acknowledgments

The excellent technical assistance of Verena Osterwalder and Steve Reese is gratefully acknowledged. I thank Peter Brunisholz and Serge Chesnov for mass spectrometry analysis.

Author information

Authors and Affiliations

  1. Institute of Oral Biology, University of Zurich, Plattenstrasse 11, 8032, Zurich, Switzerland

    Jan R. van der Ploeg

  2. Ottikerstrasse 56, 8006, Zurich, Switzerland

    Jan R. van der Ploeg

Authors
  1. Jan R. van der Ploeg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jan R. van der Ploeg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

van der Ploeg, J.R. Genome sequence of the temperate bacteriophage PH10 from Streptococcus oralis . Virus Genes 41, 450–458 (2010). https://doi.org/10.1007/s11262-010-0525-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-010-0525-0

Keywords

Search

Navigation