Comparative genome analysis of Listeria bacteriophages reveals extensive mosaicism, programmed translational frameshifting, and a novel prophage insertion site

Journal of Bacteriology

Volumn 191, Issue 23, 2009, Pages 7206-7215

  Dorscht, Julia ^a   Klumpp, Jochen ^c   Bielmann, Regula ^c   Schmelcher, Mathias ^c   Born, Yannick ^c   Zimmer, Markus ^c   Calendar, Richard ^b   Loessner, Martin J ^c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; PROLINE; TRANSFER RNA; VIRUS PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; CONTROLLED STUDY; GENE STRUCTURE; GENOME ANALYSIS; LISTERIA; LYSOGENIZATION; MOSAICISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROPHAGE; RIBOSOMAL FRAMESHIFTING; TSF GENE; VIRUS CAPSID;

AMINO ACID SEQUENCE; BACTERIOPHAGES; BASE SEQUENCE; FRAMESHIFTING, RIBOSOMAL; GENOME, VIRAL; GENOMICS; LISTERIA; MICROSCOPY, ELECTRON; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PHYLOGENY; PROPHAGES; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, NUCLEIC ACID; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS); FIRMICUTES; LISTERIA; MIRIDAE; SIPHOVIRIDAE;

EID: 72249094991     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01041-09     Document Type: Article

References (42)

1. Adams, M. H. 1959. Bacteriophages. Interscience Publishers Inc., New York, NY.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Auzat, I., A. Droge, F. Weise, R. Lurz, and P. Tavares. 2008. Origin and function of the two major tail proteins of bacteriophage SPP1. Mol. Microbiol. 70:557-569.
4. Baranov, P. V., O. Fayet, R. W. Hendrix, and J. F. Atkins. 2006. Recoding in bacteriophages and bacterial IS elements. Trends Genet. 22:174-181.
5. Bossi, L., J. A. Fuentes, G. Mora, and N. Figueroa-Bossi. 2003. Prophage contribution to bacterial population dynamics. J. Bacteriol. 185:6467-6471. (Pubitemid 37305548)
6. Bruggemann, H., S. Baumer, W. F. Fricke, A. Wiezer, H. Liesegang, I. Decker, C. Herzberg, R. Martinez-Arias, R. Merkl, A. Henne, and G. Gottschalk. 2003. The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc. Natl. Acad. Sci. USA 100:1316-1321.
7. Brussow, H., and F. Desiere. 2001. Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol. Microbiol. 39:213-222.
8. Campbell, A. 2003. The future of bacteriophage biology. Nat. Rev. Genet. 4:471-477.
9. Carlton, R. M., W. H. Noordman, B. Biswas, E. D. de Meester, and M. J. Loessner. 2005. Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul. Toxicol. Pharmacol. 43:301-312.
10. Casjens, S. R., E. B. Gilcrease, D. A. Winn-Stapley, P. Schicklmaier, H. Schmieger, M. L. Pedulla, M. E. Ford, J. M. Houtz, G. F. Hatfull, and R. W. Hendrix. 2005. The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J. Bacteriol. 187:1091-1104.
11. Caspar, D. L., and A. Klug. 1962. Physical principles in the construction of regular viruses. Cold Spring Harbor Symp. Quant. Biol. 27:1-24.
12. Doumith, M., C. Cazalet, N. Simoes, L. Frangeul, C. Jacquet, F. Kunst, P. Martin, P. Cossart, P. Glaser, and C. Buchrieser. 2004. New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect. Immun. 72:1072-1083.
13. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. (Pubitemid 38832724)
14. Farber, J. M., and P. I. Peterkin. 1991. Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev. 55:476-511.
15. Glaser, P., L. Frangeul, C. Buchrieser, C. Rusniok, A. Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couve, A. de Daruvar, P. Dehoux, E. Domann, G. Dominguez-Bernal, E. Duchaud, L. Durant, O. Dussurget, K. D. Entian, H. Fsihi, F. Garcia-del Portillo, P. Garrido, L. Gautier, W. Goebel, N. Gomez-Lopez, T. Hain, J. Hauf, D. Jackson, L. M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueno, A. Maitournam, J. M. Vicente, E. Ng, H. Nedjari, G. Nordsiek, S. Novella, B. de Pablos, J. C. Perez-Diaz, R. Purcell, B. Remmel, M. Rose, T. Schlueter, N. Simoes, A. Tierrez, J. A. Vazquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294:849-852.
16. Groth, A. C., and M. P. Calos. 2004. Phage integrases: biology and applications. J. Mol. Biol. 335:667-678.
17. Hendrix, R. W. 2002. Bacteriophages: evolution of the majority. Theor. Popul. Biol. 61:471-480.
18. Hodgson, D. A. 2000. Generalized transduction of serotype 1/2 and serotype 4b strains of Listeria monocytogenes. Mol. Microbiol. 35:312-323.
19. Klumpp, J., J. Dorscht, R. Lurz, R. Bielmann, M. Wieland, M. Zimmer, R. Calendar, and M. J. Loessner. 2008. The terminally redundant, nonpermuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of gram-positive bacteria. J. Bacteriol. 190:5753-5765.
20. Kwan, T., J. Liu, M. DuBow, P. Gros, and J. Pelletier. 2005. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc. Natl. Acad. Sci. USA 102:5174-5179.
21. Lauer, P., M. Y. Chow, M. J. Loessner, D. A. Portnoy, and R. Calendar. 2002. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J. Bacteriol. 184:4177-4186.
22. Levin, M. E., R. W. Hendrix, and S. R. Casjens. 1993. A programmed translational frameshift is required for the synthesis of a bacteriophage lambda tail assembly protein. J. Mol. Biol. 234:124-139.
23. Loessner, M. J. 1991. Improved procedure for bacteriophage typing of Listeria strains and evaluation of new phages. Appl. Environ. Microbiol. 57:882-884.
24. Loessner, M. J., and M. Busse. 1990. Bacteriophage typing of Listeria species. Appl. Environ. Microbiol. 56:1912-1918.
25. Loessner, M. J., L. A. Estela, R. Zink, and S. Scherer. 1994. Taxonomical classification of 20 newly isolated Listeria bacteriophages by electron microscopy and protein analysis. Intervirology 37:31-35.
26. Loessner, M. J., R. B. Inman, P. Lauer, and R. Calendar. 2000. Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol. Microbiol. 35:324-340.
27. Loessner, M. J., I. B. Krause, T. Henle, and S. Scherer. 1994. Structural proteins and DNA characteristics of 14 Listeria typing bacteriophages. J. Gen. Virol. 75:701-710.
28. Loessner, M. J., and C. E. Rees. 2005. Listeria phages: basics and applications, p. 362-379. In M. K. Waldor, D. I. Friedman, and L. A. Sankar (ed.), Phages: their role in bacterial pathogenesis and biotechnology. ASM Press, Washington, DC.
29. Loessner, M. J., C. E. Rees, G. S. Stewart, and S. Scherer. 1996. Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells. Appl. Environ. Microbiol. 62:1133-1140.
30. McLauchlin, J., R. T. Mitchell, W. J. Smerdon, and K. Jewell. 2004. Listeria monocytogenes and listeriosis: a review of hazard characterisation for use in microbiological risk assessment of foods. Int. J. Food Microbiol. 92:15-33.
31. Nadon, C. A., D. L. Woodward, C. Young, F. G. Rodgers, and M. Wiedmann. 2001. Correlations between molecular subtyping and serotyping of Listeria monocytogenes. J. Clin. Microbiol. 39:2704-2707.
32. Nelson, K. E., D. E. Fouts, E. F. Mongodin, J. Ravel, R. T. DeBoy, J. F. Kolonay, D. A. Rasko, S. V. Angiuoli, S. R. Gill, I. T. Paulsen, J. Peterson, O. White, W. C. Nelson, W. Nierman, M. J. Beanan, L. M. Brinkac, S. C. Daugherty, R. J. Dodson, A. S. Durkin, R. Madupu, D. H. Haft, J. Selengut, S. Van Aken, H. Khouri, N. Fedorova, H. Forberger, B. Tran, S. Kathariou, L. D. Wonderling, G. A. Uhlich, D. O. Bayles, J. B. Luchansky, and C. M. Fraser. 2004. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 32:2386-2395.
33. Ochman, H., A. S. Gerber, and D. L. Hartl. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120:621-623. (Pubitemid 18260496)
34. Paulsen, I. T., L. Banerjei, G. S. Myers, K. E. Nelson, R. Seshadri, T. D. Read, D. E. Fouts, J. A. Eisen, S. R. Gill, J. F. Heidelberg, H. Tettelin, R. J. Dodson, L. Umayam, L. Brinkac, M. Beanan, S. Daugherty, R. T. DeBoy, S. Durkin, J. Kolonay, R. Madupu, W. Nelson, J. Vamathevan, B. Tran, J. Upton, T. Hansen, J. Shetty, H. Khouri, T. Utterback, D. Radune, K. A. Ketchum, B. A. Dougherty, and C. M. Fraser. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-2074.
35. Sambrook, J., and D. W. Russell. 2001. Molecular cloning, 3rd ed., vol.1 to 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Sokal, R. R., and C. D. Mitchener. 1958. A statistical method for evaluating systematic relationships. Univ. Kansas Sci. Bull. 38:1409-1438.
37. Vazquez-Boland, J. A., M. Kuhn, P. Berche, T. Chakraborty, G. Dominguez-Bernal, W. Goebel, B. Gonzalez-Zorn, J. Wehland, and J. Kreft. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14:584-640.
38. Ward, T. J., L. Gorski, M. K. Borucki, R. E. Mandrell, J. Hutchins, and K. Pupedis. 2004. Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J. Bacteriol. 186:4994-5002.
39. Wikoff, W. R., L. Liljas, R. L. Duda, H. Tsuruta, R. W. Hendrix, and J. E. Johnson. 2000. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289:2129-2133.
40. Xu, J., R. W. Hendrix, and R. L. Duda. 2004. Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol. Cell 16:11-21. (Pubitemid 39330148)
41. Zimmer, M., E. Sattelberger, R. B. Inman, R. Calendar, and M. J. Loessner. 2003. Genome and proteome of Listeria monocytogenes phage PSA: an unusual case for programmed + 1 translational frameshifting in structural protein synthesis. Mol. Microbiol. 50:303-317.
42. Zink, R., and M. J. Loessner. 1992. Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Appl. Environ. Microbiol. 58:296-302.