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Superinfection exclusion reveals heteroimmunity between Pseudomonas aeruginosa temperate phages

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Abstract

Temperate siphophages (MP29, MP42, and MP48) were isolated from the culture supernatant of clinical Pseudomonas aeruginosa isolates. The complete nucleotide sequences and annotation of the phage genomes revealed the overall synteny to the known temperate P. aeruginosa phages such as MP22, D3112, and DMS3. Genome-level sequence analysis showed the conservation of both ends of the linear genome and the divergence at the previously identified dissimilarity regions (R1 to R9). Protein sequence alignment of the c repressor (ORF1) of each phage enabled us to divide the six phages into two groups: D3112 group (D3112, MP29, MP42, and MP48) and MP22 group (MP22 and DMS3). Superinfection exclusion was observed between the phages belonging to the same group, which was mediated by the specific interaction between the c repressor and the cognate operator. Based on these, we suggest that the temperate siphophages prevalent in the clinical strains of P. aeruginosa represent at least two distinct heteroimmunity groups.

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Refrerences

  • Alonso A., Rojo F., and Martinez J.L. 1999. Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ. Microbiol. 1, 421–430.

    Article  CAS  PubMed  Google Scholar 

  • Bondy-Denomy J., Pawluk A., Maxwell K.L., and Davidson A.R. 2013. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493, 429–432.

    Article  CAS  PubMed  Google Scholar 

  • Brussow H., Canchaya C., and Hardt W.D. 2004. Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68, 560–602.

    Article  PubMed Central  PubMed  Google Scholar 

  • Brussow H. and Hendrix R.W. 2002. Phage genomics: Small is beautiful. Cell 108, 13–16.

    Article  CAS  PubMed  Google Scholar 

  • Cady K.C., Bondy-Denomy J., Heussler G.E., Davidson A.R., and O’Toole G.A. 2012. The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol. 194, 5728–5738.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cady K.C. and O’Toole G.A. 2011. Non-identity-mediated CRISPRbacteriophage interaction mediated via the Csy and Cas3 proteins. J. Bacteriol. 193, 3433–3445.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chibani-Chennoufi S., Bruttin A., Dillmann M.L., and Brussow H. 2004. Phage-host interaction: An ecological perspective. J. Bacteriol. 186, 3677–3686.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chung I.Y. and Cho Y.H. 2012. Complete genome sequences of two Pseudomonas aeruginosa temperate phages, MP29 and MP42, which lack the phage-host CRISPR interaction. J. Virol. 86, 83–6.

    Article  Google Scholar 

  • Chung I.Y., Sim N., and Cho Y.H. 2012. Antibacterial efficacy of temperate phage-mediated inhibition of bacterial group motilities. Antimicrob. Agents Chemother. 56, 5612–5617.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clokie M.R., Millard A.D., Letarov A.V., and Heaphy S. 2011. Phages in nature. Bacteriophage 1, 31–45.

    Article  PubMed Central  PubMed  Google Scholar 

  • Darling A.C., Mau B., Blattner F.R., and Perna N.T. 2004. Mauve: Multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394–1403.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Darzins A. and Casadaban M.J. 1989. In vivo cloning of Pseudomonas aeruginosa genes with mini-D3112 transposable bacteriophage. J. Bacteriol. 171, 3917–3925.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Favero M.S., Carson L.A., Bond W.W., and Petersen N.J. 1971. Pseudomonas aeruginosa: Growth in distilled water from hospitals. Science 173, 836–838.

    Article  CAS  PubMed  Google Scholar 

  • Frimmersdorf E., Horatzek S., Pelnikevich A., Wiehlmann L., and Schomburg D. 2010. How Pseudomonas aeruginosa adapts to various environments: A metabolomic approach. Environ. Microbiol. 12, 1734–1747.

    Article  CAS  PubMed  Google Scholar 

  • Fuhrman J.A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548.

    Article  CAS  PubMed  Google Scholar 

  • Gomez P. and Buckling A. 2011. Bacteria-phage antagonistic coevolution in soil. Science 332, 106–109.

    Article  CAS  PubMed  Google Scholar 

  • Heo Y.J., Chung I.Y., Cho W.J., Lee B.Y., Kim J.H., Choi K.H., Lee J.W., Hassett D.J., and Cho Y.H. 2010. The major catalase gene (katA) of Pseudomonas aeruginosa PA14 is under both positive and negative control of the global transactivator OxyR in response to hydrogen peroxide. J. Bacteriol. 192, 381–390.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heo Y.J., Chung I.Y., Choi K.B., Lau G.W., and Cho Y.H. 2007. Genome sequence comparison and superinfection between two related Pseudomonas aeruginosa phages, D3112 and MP22. Microbiology 153, 2885–2895.

    Article  CAS  PubMed  Google Scholar 

  • Kielhofner M., Atmar R.L., Hamill R.J., and Musher D.M. 1992. Life-threatening Pseudomonas aeruginosa infections in patients with human immunodeficiency virus infection. Clin. Infect. Dis. 14, 403–411.

    Article  CAS  PubMed  Google Scholar 

  • Krylov V.N., Akhverdian V.Z., Bogush V.G., Khrenova E.A., and Reulets M.A. 1985. Modular structure of the genes of phagestransposons of Pseudomonas aeruginosa. Genetika 21, 724–734.

    CAS  PubMed  Google Scholar 

  • Lu G. and Moriyama E.N. 2004. Vector NTI, a balanced all-in-one sequence analysis suite. Brief. Bioinform. 5, 378–388.

    Article  CAS  PubMed  Google Scholar 

  • Lyczak J.B., Cannon C.L., and Pier G.B. 2000. Establishment of Pseudomonas aeruginosa infection: Lessons from a versatile opportunist. Microbes Infect. 2, 1051–1060.

    Article  CAS  PubMed  Google Scholar 

  • Murray T.S., Egan M., and Kazmierczak B.I. 2007. Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients. Curr. Opin. Pediatr. 19, 83–88.

    Article  PubMed  Google Scholar 

  • Pabo C.O. and Sauer R.T. 1992. Transcription factors: Structural families and principles of DNA recognition. Annu. Rev. Biochem. 61, 1053–1095.

    Article  CAS  PubMed  Google Scholar 

  • Rice L.B. 2008. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: No ESKAPE. J. Infect. Dis. 197, 1079–1081.

    Article  PubMed  Google Scholar 

  • Salmon K.A., Freedman O., Ritchings B.W., and DuBow M.S. 2000. Characterization of the lysogenic repressor (c) gene of the Pseudomonas aeruginosa transposable bacteriophage D3112. Virology 272, 85–97.

    Article  CAS  PubMed  Google Scholar 

  • Tamura K., Peterson D., Peterson N., Stecher G., Nei M., and Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson J.D., Higgins D.G., and Gibson T.J. 1994. Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang P.W., Chu L., and Guttman D.S. 2004. Complete sequence and evolutionary genomic analysis of the Pseudomonas aeruginosa transposable bacteriophage D3112. J. Bacteriol. 186, 400–410.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weinbauer M.G. and Rassoulzadegan F. 2004. Are viruses driving microbial diversification and diversity? Environ. Microbiol. 6, 1–11.

    Article  PubMed  Google Scholar 

  • Zegans M.E., Wagner J.C., Cady K.C., Murphy D.M., Hammond J.H., and O’Toole G.A. 2009. Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J. Bacteriol. 191, 210–219.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacy, College of Pharmacy, CHA University, Gyeonggi-do, 463-840, Republic of Korea

    In-Young Chung, Hee-Won Bae, Hye-Jung Jang, Bi-o Kim & You-Hee Cho

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  1. In-Young Chung
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  2. Hee-Won Bae
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  3. Hye-Jung Jang
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  4. Bi-o Kim
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  5. You-Hee Cho
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Correspondence to You-Hee Cho.

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Chung, IY., Bae, HW., Jang, HJ. et al. Superinfection exclusion reveals heteroimmunity between Pseudomonas aeruginosa temperate phages. J Microbiol. 52, 515–520 (2014). https://doi.org/10.1007/s12275-014-4012-5

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  • DOI: https://doi.org/10.1007/s12275-014-4012-5

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