Advertisement

Annals of Microbiology

, Volume 68, Issue 12, pp 889–897 | Cite as

Interstrain transfer of the prophage ϕNM2 in staphylococcal strains

  • Bing Yan
  • Yiming Pan
  • Zeyu Jin
  • Xiaoyu Liu
  • Wei Li
  • Baolin SunEmail author
Original Article
  • 53 Downloads

Abstract

Staphylococcus aureus is a successful pathogen in part because the bacterium can adapt rapidly to selective pressures imparted by the external environment. Horizontal gene transfer (HGT) plays an integral role in the evolution of bacterial genomes, and phage transduction is likely to be the most common and important HGT mechanism for S. aureus. Phage can transfer not only its own genome DNA but also host bacterial DNA with or without pathogenicity islands to other bacteria. Here, we demonstrate that the staphylococcal prophage ϕNM2 could transfer between strains Newman and NCTC8325/NCTC8325-4 by simulating a natural situation in laboratory without mitomycin C or ultra-violet light treatment. This transference may be caused by direct contact between Newman and NCTC8325/NCTC8325-4 instead of phage particles released in Newman culture’s supernatant. The rates of successful horizontal genetic transfer in recipients NCTC8325 and NCTC8325-4 were 2.1% and 1.8%, respectively. Prophage ϕNM2 was integrated with one direction at an intergenic region between rpmF and isdB in all 17 lysogenic isolates. Phage particles were spontaneously released from lysogenic strains again and had no noticeable influence on the growth of host cells. The results reported herein provide insight into how mobile genetic elements such as prophages can lead to the emergence of genetic diversity among S. aureus strains.

Keywords

Staphylococcus aureus Prophage ϕNM2 Interstrain transfer NCTC8325/NCTC8325-4 Newman 

Notes

Acknowledgments

We thank Professor M Li at Shanghai Jiaotong University for providing the clinical strains of Staphylococcus aureus.

Funding information

This study was supported in part by Mudanjiang Normal University (SY201230).

References

  1. Baba T et al (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819–1827.  https://doi.org/10.1016/s0140-6736(02)08713-5 CrossRefGoogle Scholar
  2. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K (2008) Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J Bacteriol 190:300–310.  https://doi.org/10.1128/jb.01000-07 CrossRefPubMedGoogle Scholar
  3. Bae T, Baba T, Hiramatsu K, Schneewind O (2006) Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62:1035–1047.  https://doi.org/10.1111/j.1365-2958.2006.05441.x CrossRefPubMedGoogle Scholar
  4. Barrangou R et al (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712CrossRefGoogle Scholar
  5. Boyd EF, Moyer KE, Shi L, Waldor MK (2000) Infectious CTX Phi, and the Vibrio pathogenicity island prophage in Vibrio mimicus: evidence for recent horizontal transfer between V. mimicus and V. cholerae. Infect Immun 68:1507–1513.  https://doi.org/10.1128/Iai.68.3.1507-1513.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brussow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560.  https://doi.org/10.1128/mmbr.68.3.560-602.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Coleman DC, Sullivan DJ, Russel RJ, Arbuthnott JP, Carey BF, Pomeroy HM (1989) Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of β-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. Microbiology 135:1679–1697CrossRefGoogle Scholar
  8. Diep BA et al (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367:731–739.  https://doi.org/10.1016/s0140-6736(06)68231-7 CrossRefPubMedGoogle Scholar
  9. Duthie E, Lorenz LL (1952) Staphylococcal coagulase: mode of action and antigenicity. Microbiology 6:95–107CrossRefGoogle Scholar
  10. Fortier LC, Sekulovic O (2013) Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354–365.  https://doi.org/10.4161/viru.24498 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Ghosh P, Wasil LR, Hatfull GF (2006) Control of phage Bxb1 excision by a novel recombination directionality factor. PLoS Biol 4:964–974.  https://doi.org/10.1371/journal.pbio.0040186 CrossRefGoogle Scholar
  12. Goerke C et al (2009) Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191:3462–3468.  https://doi.org/10.1128/jb.01804-08 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Grindley NDF, Whiteson KL, Rice PA (2006) Mechanisms of site-specific recombination. Annu Rev Biochem 75:567–605.  https://doi.org/10.1146/annurev.biochem.73.011303.073908 CrossRefPubMedGoogle Scholar
  14. Grundmeier M, Hussain M, Becker P, Heilmann C, Peters G, Sinha B (2004) Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect Immun 72:7155–7163.  https://doi.org/10.1128/IAI.72.12.7155-7163.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hershey AD, Kalmanson G, Bronfenbrenner J (1943) Quantitative methods in the study of the phage-antiphage reaction. J Immunol 46:267–279Google Scholar
  16. Holden MTG et al (2004) Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A 101:9786–9791.  https://doi.org/10.1073/pnas.0402521101 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hoskisson PA, Smith MCM (2007) Hypervariation and phase variation in the bacteriophage ‘resistome’. Curr Opin Microbiol 10:396–400.  https://doi.org/10.1016/j.mib.2007.04.003 CrossRefPubMedGoogle Scholar
  18. Khaleel T, Younger E, McEwan AR, Varghese AS, Smith MCM (2011) A phage protein that binds phi C31 integrase to switch its directionality. Mol Microbiol 80:1450–1463.  https://doi.org/10.1111/j.1365-2958.2011.07696.x CrossRefPubMedGoogle Scholar
  19. Li M, Rigby K, Lai Y, Nair V, Peschel A, Schittek B, Otto M (2009) Staphylococcus aureus mutant screen reveals interaction of the human antimicrobial peptide dermcidin with membrane phospholipids. Antimicrob Agents Chemother 53:4200–4210.  https://doi.org/10.1128/AAC.00428-09 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lindsay JA, Holden MTG (2004) Staphylococcus aureus: superbug, super genome? Trends Microbiol 12:378–385.  https://doi.org/10.1016/j.tim.2004.06.004 CrossRefPubMedGoogle Scholar
  21. Maiques E, Ubeda C, Tormo MA, Ferrer MD, Lasa I, Novick RP, Penades JR (2007) Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J Bacteriol 189:5608–5616.  https://doi.org/10.1128/jb.00619-07 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Malachowa N, DeLeo FR (2010) Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci 67:3057–3071.  https://doi.org/10.1007/s00018-010-0389-4 CrossRefPubMedPubMedCentralGoogle Scholar
  23. McCarthy AJ, Witney AA, Lindsay JA (2012) Staphylococcus aureus temperate bacteriophage: carriage and horizontal gene transfer is lineage associated. Front Cell Infect Microbiol 2:6CrossRefGoogle Scholar
  24. Merril CR, Scholl D, Adhya SL (2003) The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov 2:489–497CrossRefGoogle Scholar
  25. Novick RP (1991) Genetic systems in staphylococci. Methods Enzymol 204:587–636CrossRefGoogle Scholar
  26. Novick RP (2003) Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49:93–105.  https://doi.org/10.1016/s0147-619x(02)00157-9 CrossRefPubMedGoogle Scholar
  27. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304.  https://doi.org/10.1038/35012500 CrossRefPubMedGoogle Scholar
  28. Singh S, Ghosh P, Hatfull GF (2013) Attachment site selection and identity in Bxb1 serine integrase-mediated site-specific recombination. PLoS Genet 9:e1003490.  https://doi.org/10.1371/journal.pgen.1003490 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Smith MCM, Thorpe HM (2002) Diversity in the serine recombinases. Mol Microbiol 44:299–307.  https://doi.org/10.1046/j.1365-2958.2002.02891.x CrossRefPubMedGoogle Scholar
  30. Smith MC, Till R, Smith MC (2004) Switching the polarity of a bacteriophage integration system. Mol Microbiol 51:1719–1728CrossRefGoogle Scholar
  31. Tao L, Wu X, Sun B (2010) Alternative sigma factor sigma(H) modulates prophage integration and excision in Staphylococcus aureus. PLoS Pathog 6.  https://doi.org/10.1371/journal.ppat.1000888 CrossRefGoogle Scholar
  32. Udden SMN et al (2008) Acquisition of classical CTX prophage from Vibrio cholerae O141 by El Tor strains aided by lytic phages and chitin-induced competence. Proc Natl Acad Sci U S A 105:11951–11956.  https://doi.org/10.1073/pnas.0805560105 CrossRefPubMedPubMedCentralGoogle Scholar
  33. van Wamel WJ, Rooijakkers SH, Ruyken M, van Kessel KP, van Strijp JA (2006) The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on β-hemolysin-converting bacteriophages. J Bacteriol 188:1310–1315CrossRefGoogle Scholar
  34. Waldron DE, Lindsay JA (2006) Sau1: a novel line age-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J Bacteriol 188:5578–5585.  https://doi.org/10.1128/jb.00418-06 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Wang G-H, Jia L-Y, Xiao J-H, Huang D-W (2016) Discovery of a new Wolbachia supergroup in cave spider species and the lateral transfer of phage WO among distant hosts. Infect Genet Evol 41:1–7.  https://doi.org/10.1016/j.meegid.2016.03.015 CrossRefPubMedGoogle Scholar
  36. Wardenburg JB, Bae T, Otto M, DeLeo FR, Schneewind O (2007) Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13:1405–1406.  https://doi.org/10.1038/nm1207-1405 CrossRefGoogle Scholar
  37. Winstel V et al (2013) Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens. Nat Commun 4.  https://doi.org/10.1038/ncomms3345
  38. Yacoby I, Bar H, Benhar I (2007) Targeted drug-carrying bacteriophages as antibacterial nanomedicines. Antimicrob Agents Chemother 51:2156–2163.  https://doi.org/10.1128/aac.00163-07 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Yu D, Zhao L, Xue T, Sun B (2012) Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiol 12:1CrossRefGoogle Scholar
  40. Zhang S (2003) Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol 21:1171–1178CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature and the University of Milan 2018

Authors and Affiliations

  1. 1.School of Life SciencesMudanjiang Normal UniversityMudanjiangChina
  2. 2.School of Life SciencesUniversity of Science and Technology of ChinaHefeiChina

Personalised recommendations