Comparative genomics and transduction potential of Enterococcus faecalis temperate bacteriophages

Journal of Bacteriology

Volumn 192, Issue 4, 2010, Pages 1122-1130

  Yasmin, Azra ^a,b   Kenny, John G ^a   Shankar, Jayendra ^a   Darby, Alistair C ^a   Hall, Neil ^a   Edwards, Clive ^a   Horsburgh, Malcolm J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b FATIMA JINNAH WOMEN UNIVERSITY   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CALCIUM CHLORIDE; DNA; ERYTHROMYCIN; KANAMYCIN; MITOMYCIN C; NORFLOXACIN; RIFAMPICIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM CULTURE; BACTERIUM ISOLATE; CATERPILLAR; COMPARATIVE STUDY; CONTROLLED STUDY; CULTURE MEDIUM; DNA SEQUENCE; ENTEROCOCCUS FAECALIS; GENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; SCANNING ELECTRON MICROSCOPY;

ANTI-BACTERIAL AGENTS; BACTEREMIA; BACTERIOPHAGES; DNA FINGERPRINTING; DNA, VIRAL; ELECTROPHORESIS, GEL, PULSED-FIELD; ENTEROCOCCUS FAECALIS; GENE ORDER; GENOME, VIRAL; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MITOMYCIN; MOLECULAR SEQUENCE DATA; NORFLOXACIN; PROPHAGES; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SYNTENY; TRANSDUCTION, GENETIC; ULTRAVIOLET RAYS; VIRION; VIRUS ACTIVATION;

ENTEROCOCCUS FAECALIS; GALLERIA MELLONELLA; LACTOCOCCUS LACTIS SUBSP. CREMORIS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS MITIS; STREPTOCOCCUS PYOGENES;

EID: 75749148402     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01293-09     Document Type: Article

References (61)

1. 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.
2. Aziz, R. K., S. A. Ismail, H. W. Park, and M. Kotb. 2004. Post-proteomic identification of a novel phage-encoded streptodornase, Sda1, in invasive M1T1 Streptococcus pyogenes. Mol. Microbiol. 54:184-197.
3. Aziz, R. K., R. A. Edwards, W. W. Taylor, D. E. Low, A. McGeer, and M. Kotb. 2005. Mosaic prophages with horizontally acquired genes account for the emergence and diversification of the globally disseminated M1T1 clone of Streptococcus pyogenes. J. Bacteriol. 187:3311-3318.
4. Banks, D. J., B. Lei, and J. M. Musser. 2003. Prophage induction and expression of prophage-encoded virulence factors in group A Streptococcus serotype M3 strain MGAS315. Infect. Immun. 71:7079-7086.
5. Barrangou, R., C. Fremaux, H. Deveau, M. Richards, P. Boyaval, S. Moineau, D. A. Romero, and P. Horvath. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709-1712.
6. Beloglazova, N., G. Brown, M. D. Zimmerman, M. Proudfoot, K. S. Makarova, M. Kudritska, S. Kochinyan, S. Wang, M. Chruszcz, W. Minor, E. V. Koonin, A. M. Edwards, A. Savchenko, and A. F. Yakunin. 2008. A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. J. Biol. Chem. 283:20361-20371.
7. Bensing. B. A., I. R. Siboo, and P. M. Sullam. 2001. Proteins PblA and PblB of Streptococcus mitis, which promote binding to human platelets, are encoded within a lysogenic bacteriophage. Infect. Immun. 69:6186-6192.
8. Bourgogne, A., D. A. Garsin, X. Qin, K. V. Singh, J. Sillanpaa, S. Yerrapragada, Y. Ding, S. Dugan-Rocha, C. Buhay, H. Shen, G. Chen, G. Williams, D. Muzny, A. Maadani, K. A. Fox, J. Gioia, L. Chen, Y. Shang, C. A. Arias, S. R. Nallapareddy, M. Zhao, V. P. Prakash, S. Chowdhury, H. Jiang, R. A. Gibbs, B. E. Murray, S. K. Highlander, and G. M. Weinstock. 2008. Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol. 9:R110.
9. Brouns, S. J., M. M. Jore, M. Lundgren, E. R. Westra, R. J. Slijkhuis, A. P. Snijders, M. J. Dickman, K. S. Makarova, E. V. Koonin, and J. van der Oost. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960-964.
10. Carte, J., R. Wang, H. Li, R. M. Terns, and M. P. Terns. 2008. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev. 22:3489-3496.
11. Chang, S., D. M. Sievert, J. C. Hageman, M. L. Boulton, F. C. Tenover, F. P. Downes, S. Shah, J. T. Rudrik, G. R. Pupp, W. J. Brown, D. Cardo, and S. K. Fridkin. 2003. Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene N. Engl. J. Med. 348:1342-1347.
12. Chopin, M. C., A. Chopin, and C. Roux. 1976. Definition of bacteriophage groups according to their lytic action on mesophilic lactic streptococci. Appl. Environ. Microbiol. 32:741-746.
13. Delcher, A., D. Harmon, S. Kasif, O. White, and S. Salzberg. 1999. Improved microbial gene identification with glimmer. Nucleic Acids Res. 27:4636-4641.
14. Desiere, F., S. Lucchini, C. Canchaya, M. Ventura, and H. Brüssow. 2002. Comparative genomics of phages and prophages in lactic acid bacteria. Antonie Van Leeuwenhoek 82:73-79.
15. Dunny, G. M., B. L. Brown, and D. B. Clewell. 1978. Induced cell aggregation and mating in Streptococcus faecalis: evidence for a bacterial sex pheromone. Proc. Natl. Acad. Sci. U. S. A. 75:3479-3483.
16. Hatfull, G. F., S. G. Cresawn, and R. W. Hendrix. 2008. Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution. Res. Microbiol. 159:332-339.
17. B modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184:5457-5467.
18. Hunter, S., R. Apweiler, T. K. Attwood, A. Bairoch, A. Bateman, D. Binns, P. Bork, U. Das, L. Daugherty, L. Duquenne, R. D. Finn, J. Gough, D. Haft, N. Hulo, D. Kahn, E. Kelly, A. Laugraud, I. Letunic, D. Lonsdale, R. Lopez, M. Madera, J. Maslen, C. McAnulla, J. McDowall, J. Mistry, A. Mitchell, N. Mulder, D. Natale, C. Orengo, A. F. Quinn, J. D. Selengut, C. J. A. Sigrist, M. Thimma, P. D. Thomas, F. Valentin, D. Wilson, C. H. Wu, and C. Yeats. 2009. Interpro: the integrative protein signature database. Nucleic Acids Res. 37:D211-D215.
19. Huycke, M. M., D. F. Sahm, and M. S. Gilmore. 1998. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4:239-249.
20. Jacob, A. E., and S. J. Hobbs. 1974. Conjugal transfer of plasmid-borne multiple antibiotic resistance in Streptococcus faecalis var. zymogenes. J. Bacteriol. 117:360-372.
21. Jett, B. D., M. M. Huycke, and M. S. Gilmore. 1994. Virulence of enterococci. Clin. Microbiol. Rev. 7:462-478.
22. Kenny, J. G., D. Ward, E. Josefsson, I. M. Jonsson, J. Hinds, H. H. Rees, J. A. Lindsay, A. Tarkowski, and M. J. Horsburgh. 2009. The Staphylococcus aureus response to unsaturated long chain free fatty acids: survival mechanisms and virulence implications. PLoS One 4:e4344.
23. Krzywinski, M., J. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S. J. Jones, and M. A. Marra. 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19:1639-1645.
24. Kurtz, S., A. Phillippy, A. L. Delcher, M. Smoot, M. Shumway, C. Antonescu, and S. L. Salzberg. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:R12.
25. Lebreton, F., E. Riboulet-Bisson, P. Serror, M. Sanguinetti, B. Posteraro, R. Torelli, A. Hartke, Y. Auffray, and J. C. Giard. 2009. ace, which encodes an adhesin in Enterococcus faecalis, is regulated by Ers and is involved in virulence. Infect. Immun. 77:2832-2839.
26. Lepage, E., S. Brinster, C. Caron, C. Ducroix-Crepy, L. Rigottier-Gois, G. Dunny, C. Hennequet-Antier, and P. Serror. 2006. Comparative genomic hybridization analysis of Enterococcus faecalis: identification of genes absent from food strains. J. Bacteriol. 188:6858-6868.
27. Li, L., C. J. Stoeckert, and D. S. Roos. 2003. Orthomcl: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189.
28. Lillestøl, R. K., P. Redder, R. A. Garrett, and K. Brugger. 2006. A putative viral defence mechanism in archaeal cells. Archaea 2:59-72.
29. Lukashin, A., and M. Borodovsky. 1998. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26:1107-1115.
30. Makarova, K. S., N. V. Grishin, S. A. Shabalina, Y. I. Wolf, and E. V. Koonin. 2006. A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct 1:7.
31. Makarova, K., A. Slesarev, Y. Wolf, A. Sorokin, B. Mirkin, E. Koonin, A. Pavlov, N. Pavlova, V. Karamychev, N. Polouchine, V. Shakhova, I. Grigoriev, Y. Lou, D. Rohksar, S. Lucas, K. Huang, D. M. Goodstein, T. Hawkins, V. Plengvidhya, D. Welker, J. Hughes, Y. Goh, A. Benson, K. Baldwin, J. H. Lee, I. Díaz-Muñiz, B. Dosti, V. Smeianov, W. Wechter, R. Barabote, G. Lorca, E. Altermann, R. Barrangou, B. Ganesan, Y. Xie, H. Rawsthorne, D. Tamir, C. Parker, F. Breidt, J. Broadbent, R. Hutkins, D. O'Sullivan, J. Steele, G. Unlu, M. Saier, T. Klaenhammer, P. Richardson, S. Kozyavkin, B. Weimer, and D. Mills. 2006. Comparative genomics of the lactic acid bacteria. Proc. Natl. Acad. Sci. U. S. A. 103:15611-15616.
32. Marraffini, L. A., and E. J. Sontheimer. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: 1843-1845.
33. McBride, S. M., V. A. Fischetti, D. J. LeBlanc, R. C. Moellering, Jr., and M. S. Gilmore. 2007. Genetic diversity among Enterococcus faecalis. PLoS One 2:e582.
34. McBride, S. M., P. S. Coburn, A. S. Baghdayan, R. J. Willems, M. J. Grande, N. Shankar, and M. S. Gilmore. 2009. Genetic variation and evolution of the pathogenicity island of Enterococcus faecalis. J. Bacteriol. 191:3392-3402.
35. Mitchell, J., and P. M. Sullam. 2009 Streptococcus mitis phage-encoded adhesins mediate attachment to 2-8-linked sialic acid residues on platelet membrane gangliosides. Infect. Immun. 77:3485-3490.
36. Mojica, F. J., C. Diez-Villasenor, J. Garcia-Martinez, and E. Soria. 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:174-182.
37. Murray, B. E. 1990. The life and times of the Enterococcus. Clin. Microbiol. Rev. 3:46-65.
38. Mylonakis, E., R. Moreno, J. B. El Khoury, A. Idnurm, J. Heitman, S. B. Calderwood, F. M. Ausubel, and A. Diener. 2005. Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect. Immun. 73:3842-3850.
39. Obregón, V., J. L. García, E. García, R. López, and P. García. 2003. Genome organization and molecular analysis of the temperate bacteriophage MM1 of Streptococcus pneumoniae. J. Bacteriol. 185:2362-2368.
40. Paulsen, I. T., L. Banerjei, G. S. Myers, K. E. Nelson, R. Seshadri, et al. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-2074.
41. Pedulla, M. L., M. E. Ford, J. M. Houtz, T. Karthikeyan, C. Wadsworth, J. A. Lewis, D. Jacobs-Sera, J. Falbo, J. Gross, N. R. Pannunzio, W. Brucker, V. Kumar, J. Kandasamy, L. Keenan, S. Bardarov, J. Kriakov, J. G. Lawrence, W. R. Jacobs, Jr., R. W. Hendrix, and G. F. Hatfull. 2003. Origins of highly mosaic mycobacteriophage genomes. Cell 113:171-182.
42. Pourcel, C., G. Salvignol, and G. Vergnaud. 2005. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151:653-663.
43. Prévost, G., B. Cribier, P. Couppie, P. Petiau, G. Supersac, V. Finck-Barbancon, H. Monteil, and Y. Piemont. 1995. Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect. Immun. 63:4121-4129.
44. Qin, X., K. V. Singh, G. M. Weinstock, and B. E. Murray. 2000. Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect. Immun. 68:2579-2586.
45. Ruiz-Garbajosa, P., M. J. Bonten, D. A. Robinson, J. Top, S. R. Nallapareddy, C. Torres, T. M. Coque, R. Cantón, F. Baquero, B. E. Murray, R. del Campo, and R. J. Willems. 2006. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J. Clin. Microbiol. 44:2220-2228.
46. Rutherford, K., J. Parkhill, J. Crook, T. Horsnell, P. Rice, M. A. Rajandream, and B. Barrell. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
47. Sahm, D. F., J. Kissinger, M. S. Gilmore, P. R. Murray, R. Mulder, J. Solliday, and B. Clarke. 1989. In vitro susceptibility studies of vancomycinresistant Enterococcus faecalis. Antimicrob. Agents Chemother. 33:1588-1591.
48. Sambrook, J., E. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. Shankar, N., A. S. Baghdayan, and M. S. Gilmore. 2002. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417:746-750.
50. Sievert, D. M., J. T. Rudrik, J. B. Patel, L. C. McDonald, M. J. Wilkins, and J. C. Hageman. 2008. Vancomycin-resistant Staphylococcus aureus in the United States, 2002-2006. Clin. Infect. Dis. 46:668-674.
51. Sifri, C. D., E. Mylonakis, K. V. Singh, X. Qin, D. A. Garsin, B. E. Murray, F. M. Ausubel, and S. B. Calderwood. 2002. Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect. Immun. 70:5647-5650.
52. Singh, K. V., X. Qin, G. M. Weinstock, and B. E. Murray. 1998. Generation and testing of mutants of Enterococcus faecalis in a mouse peritonitis model. J. Infect. Dis. 178:1416-1420.
53. Stanley, E., G. F. Fitzgerald, C. Le Marrec, B. Fayard, and D. van Sinderen. 1997. Sequence analysis and characterization of phi O1205, a temperate bacteriophage infecting Streptococcus thermophilus CNRZ1205. Microbiology 143:3417-3429.
54. Tormo, M. A., M. D. Ferrer, E. Maiques, C. Ubeda, L. Selva, I. Lasa, J. J. Calvete, R. P. Novick, and J. R. Penadés. 2008. Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J. Bacteriol. 190:2434-2440.
55. van Wamel, W. J., S. H. Rooijakkers, M. Ruyken, K. P. van Kessel, and J. A. van Strijp. 2006. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 188:1310-1315.
56. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59:69-89.
57. Villion, M., M. C. Chopin, H. Deveau, S. D. Ehrlich, S. Moineau, and A. Chopin. 2009. P087, a lactococcal phage with a morphogenesis module similar to an Enterococcus faecalis prophage. Virology 388:49-56.
58. Waters, C. M., M. H. Antiporta, B. E. Murray, and G. M. Dunny. 2003. Role of the Enterococcus faecalis GelE protease in determination of cellular chain length, supernatant pheromone levels, and degradation of fibrin and misfolded surface proteins. J. Bacteriol. 185:3613-3623.
59. Wegmann, U., M. O'Connell-Motherway, A. Zomer, G. Buist, C. Shearman, C. Canchaya, M. Ventura, A. Goesmann, M. J. Gasson, O. P. Kuipers, D. van Sinderen, and J. Kok. 2007. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189:3256-3270.
60. Woodford, N., R. Reynolds, J. Turton, F. Scott, A. Sinclair, A. Williams, and D. Livermore. 2003. Two widely disseminated strains of Enterococcus faecalis highly resistant to gentamicin and ciprofloxacin from bacteraemias in the UK and Ireland. J. Antimicrob. Chemother. 52:711-714.
61. Zhao, Z., E. Sagulenko, Z. Ding, and P. J. Christie. 2001. Activities of virE1 and the VirE1 secretion chaperone in export of the multifunctional VirE2 effector via an Agrobacterium type IV secretion pathway. J. Bacteriol. 183: 3855-3865.