Regulation, integrase-dependent excision, and horizontal transfer of genomic islands in Legionella pneumophila

Journal of Bacteriology

Volumn 195, Issue 7, 2013, Pages 1583-1597

  Lautner, Monika ^a   Schunder, Eva ^a   Herrmann, Vroni ^a   Heuner, Klaus ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE;

ARTICLE; BACTERIAL STRAIN; BACTERIUM CONJUGATION; BINDING SITE; CELL SURVIVAL; CONTROLLED STUDY; DNA BASE COMPOSITION; ENZYME BINDING; EPISOME; GENE CONTROL; GENOMIC ISLAND; IN VITRO STUDY; LEGIONELLA PNEUMOPHILA; NONHUMAN; PRIORITY JOURNAL;

ACANTHAMOEBA CASTELLANII; BACTERIAL SECRETION SYSTEMS; CHROMOSOMES, BACTERIAL; CONJUGATION, GENETIC; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; HUMANS; INTEGRASES; LEGIONELLA PNEUMOPHILA; PLASMIDS; RECOMBINATION, GENETIC;

ACANTHAMOEBA CASTELLANII; LEGIONELLA; LEGIONELLA PNEUMOPHILA; NEGIBACTERIA;

EID: 84875528671     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01739-12     Document Type: Article

References (61)

1. Rowbotham TJ. 1980. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33: 1179-1183.
2. Fields BS. 1996. The molecular ecology of legionellae. Trends Microbiol. 4:286-290.
3. Rowbotham TJ. 1986. Current views on the relationships between amoebae, legionellae and man. Isr. J. Med. Sci. 22:678-689.
4. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG, Harris J, Mallison GF, Martin SM, McDade JE, Shepard CC, Brachman PS. 1977. Legionnaires' disease: description of an epidemic of pneumonia. N. Engl. J. Med. 297:1189-1197.
5. Jepras RI, Fitzgeorge RB, Baskerville A. 1985. A comparison of virulence of two strains of Legionella pneumophila based on experimental aerosol infection of guinea-pigs. J. Hyg. (Lond.) 95:29-38.
6. Schunder E, Adam P, Higa F, Remer KA, Lorenz U, Bender J, Schulz T, Flieger A, Steinert M, Heuner K. 2010. Phospholipase PlaB is a new virulence factor of Legionella pneumophila. Int. J. Med. Microbiol. 300: 313-323.
7. Horwitz MA. 1983. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158:2108-2126.
8. Swanson MS, Isberg RR. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609-3620.
9. Berger KH, Isberg RR. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7:7-19.
10. Cianciotto NP. 2009. Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila. Future Microbiol. 4:797-805.
11. Segal G, Purcell M, Shuman HA. 1998. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. U. S. A. 95:1669-1674.
12. Zhu W, Banga S, Tan Y, Zheng C, Stephenson R, Gately J, Luo ZQ. 2011. Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS One 6:e17638. doi:10 .1371/journal.pone.0017638.
13. Alvarez-Martinez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775-808.
14. Juhas M, Crook DW, Hood DW. 2008. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell. Microbiol. 10: 2377-2386.
15. Voth DE, Broederdorf LJ, Graham JG. 2012. Bacterial type IV secretion systems: versatile virulence machines. Future Microbiol. 7:241-257.
16. Christie PJ, Vogel JP. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354-360.
17. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451-485.
18. Andrews HL, Vogel JP, Isberg RR. 1998. Identification of linked Legionella pneumophila genes essential for intracellular growth and evasion of the endocytic pathway. Infect. Immun. 66:950-958.
19. Brand BC, Sadosky AB, Shuman HA. 1994. The Legionella pneumophila icm locus: a set of genes required for intracellular multiplication in human macrophages. Mol. Microbiol. 14:797-808.
20. Edelstein PH, Edelstein MA, Higa F, Falkow S. 1999. Discovery of virulence genes of Legionella pneumophila by using signature tagged mutagenesis in a guinea pig pneumonia model. Proc. Natl. Acad. Sci. U. S. A. 96:8190-8195.
21. Luo ZQ, Isberg RR. 2004. Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc. Natl. Acad. Sci. U. S. A. 101:841-846.
22. Adamczyk M, Jagura-Burdzy G. 2003. Spread and survival of promiscuous IncP-1 plasmids. Acta Biochim. Pol. 50:425-453.
23. Bandyopadhyay P, Liu S, Gabbai CB, Venitelli Z, Steinman HM. 2007. Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect. Immun. 75:723-735.
24. Samrakandi MM, Cirillo SL, Ridenour DA, Bermudez LE, Cirillo JD. 2002. Genetic and phenotypic differences between Legionella pneumophila strains. J. Clin. Microbiol. 40:1352-1362.
25. Segal G, Russo JJ, Shuman HA. 1999. Relationships between a new type IV secretion system and the icm/dot virulence system of Legionella pneumophila. Mol. Microbiol. 34:799-809.
26. Glöckner G, Albert-Weissenberger C, Weinmann E, Jacobi S, Schunder E, Steinert M, Hacker J, Heuner K. 2008. Identification and characterization of a new conjugation/type IVA secretion system (trb/tra) of Legionella pneumophila Corby localized on two mobile genomic islands. Int. J. Med. Microbiol. 298:411-428.
27. Gomez-Valero L, Rusniok C, Jarraud S, Vacherie B, Rouy Z, Barbe V, Medigue C, Etienne J, Buchrieser C. 2011. Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes. BMC Genomics 12:536. doi:10.1186/1471-2164-12-536.
28. Miyamoto H, Yoshida S, Taniguchi H, Shuman HA. 2003. Virulence conversion of Legionella pneumophila by conjugal transfer of chromosomal DNA. J. Bacteriol. 185:6712-6718.
29. Lawley TD, Klimke WA, Gubbins MJ, Frost LS. 2003. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 224:1-15. 30. Juhas M, Crook DW, Dimopoulou ID, Lunter G, Harding RM, Ferguson DJ, Hood DW. 2007. Novel type IV secretion system involved in propagation of genomic islands. J. Bacteriol. 189:761-771.
30. Juhas M, Crook DW, Dimopoulou ID, Lunter G, Harding RM, Ferguson DJ, Hood DW. 2007. Novel type IV secretion system involved in propagation of genomic islands. J. Bacteriol. 189:761-771.
31. Juhas M, Power PM, Harding RM, Ferguson DJ, Dimopoulou ID, Elamin AR, Mohd-Zain Z, Hood DW, Adegbola R, Erwin A, Smith A, Munson RS, Harrison A, Mansfield L, Bentley S, Crook DW. 2007. Sequence and functional analyses of Haemophilus spp. genomic islands. Genome Biol. 8:R237. doi:10.1186/gb-2007-8-11-r237.
32. Schroeder GN, Petty NK, Mousnier A, Harding CR, Vogrin AJ, Wee B, Fry NK, Harrison TG, Newton HJ, Thomson NR, Beatson SA, Dougan G, Hartland EL, Frankel G. 2010. Legionella pneumophila strain 130b possesses a unique combination of type IV secretion systems and novel Dot/Icm secretion system effector proteins. J. Bacteriol. 192:6001-6016.
33. Molofsky AB, Swanson MS. 2003. Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol. Microbiol. 50:445-461.
34. Marra A, Shuman HA. 1989. Isolation of a Legionella pneumophila restriction mutant with increased ability to act as a recipient in heterospecific matings. J. Bacteriol. 171:2238-2240.
35. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
36. Hall J, Voelz H. 1985. Bacterial endosymbionts of Acanthamoeba sp. J. Parasitol. 71:89-95.
37. Stone BJ, Kwaik YA. 1999. Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J. Bacteriol. 181:1395-1402.
38. Orrison LH, Cherry WB, Tyndall RL, Fliermans CB, Gough SB, Lambert MA, McDougal LK, Bibb WF, Brenner DJ. 1983. Legionella oakridgensis: unusual new species isolated from cooling tower water. Appl. Environ. Microbiol. 45:536-545.
39. Brüggemann H, Hagman A, Jules M, Sismeiro O, Dillies MA, Gouyette C, Kunst F, Steinert M, Heuner K, Coppee JY, Buchrieser C. 2006. Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell. Microbiol. 8:1228-1240.
40. Eylert E, Herrmann V, Jules M, Gillmaier N, Lautner M, Buchrieser C, Eisenreich W, Heuner K. 2010. Isotopologue profiling of Legionella pneumophila: role of serine and glucose as carbon substrates. J. Biol. Chem. 285:22232-22243.
41. Cianciotto NP, Fields BS. 1992. Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc. Natl. Acad. Sci. U. S. A. 89:5188-5191.
42. Flieger A, Rydzewski K, Banerji S, Broich M, Heuner K. 2004. Cloning and characterization of the gene encoding the major cell-associated phospholipaseAof Legionella pneumophila, plaB, exhibiting hemolytic activity. Infect. Immun. 72:2648-2658.
43. Liles MR, Edelstein PH, Cianciotto NP. 1999. The prepilin peptidase is required for protein secretion by and the virulence of the intracellular pathogen Legionella pneumophila. Mol. Microbiol. 31:959-970.
44. Boyd EF, Almagro-Moreno S, Parent MA. 2009. Genomic islands are dynamic, ancient integrative elements in bacterial evolution. Trends Microbiol. 17:47-53.
45. Sahr T, Brüggemann H, Jules M, Lomma M, Albert-Weissenberger C, Cazalet C, Buchrieser C. 2009. Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol. Microbiol. 72: 741-762.
46. Neumeister B, Schoniger S, Faigle M, Eichner M, Dietz K. 1997. Multiplication of different Legionella species in Mono Mac 6 cells and in Acanthamoeba castellanii. Appl. Environ. Microbiol. 63:1219-1224.
47. Doleans-Jordheim A, Akermi M, Ginevra C, Cazalet C, Kay E, Schneider D, Buchrieser C, Atlan D, Vandenesch F, Etienne J, Jarraud S. 2006. Growth-phase-dependent mobility of the lvh-encoding region in Legionella pneumophila strain Paris. Microbiology 152:3561-3568.
48. Sam MD, Cascio D, Johnson RC, Clubb RT. 2004. Crystal structure of the excisionase-DNA complex from bacteriophage lambda. J. Mol. Biol. 338:229-240.
49. Lesic B, Carniel E. 2005. Horizontal transfer of the high-pathogenicity island of Yersinia pseudotuberculosis. J. Bacteriol. 187:3352-3358.
50. Goosen N, van de Putte P. 1995. The regulation of transcription initiation by integration host factor. Mol. Microbiol. 16:1-7.
51. Hales LM, Gumport RI, Gardner JF. 1994. Determining the DNA sequence elements required for binding integration host factor to two different target sites. J. Bacteriol. 176:2999-3006.
52. Turner SA, Luck SN, Sakellaris H, Rajakumar K, Adler B. 2004. Role of attP in integrase-mediated integration of the Shigella resistance locus pathogenicity island of Shigella flexneri. Antimicrob. Agents Chemother. 48:1028-1031.
53. Wilde C, Mazel D, Hochhut B, Middendorf B, Le Roux F, Carniel E, Dobrindt U, Hacker J. 2008. Delineation of the recombination sites necessary for integration of pathogenicity islands II and III into the Escherichia coli 536 chromosome. Mol. Microbiol. 68:139-151.
54. Williams KP. 2002. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res. 30:866-875.
55. D'Auria G, Jimenez-Hernandez N, Peris-Bondia F, Moya A, Latorre A. 2010. Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11:181. doi:10.1186/1471-2164-11-181.
56. Romeo T. 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol. Microbiol. 29:1321-1330.
57. Little JW. 1984. Autodigestion of lexA and phage lambda repressors. Proc. Natl. Acad. Sci. U. S. A. 81:1375-1379.
58. Little JW, Mount DW. 1982. The SOS regulatory system of Escherichia coli. Cell 29:11-22.
59. Kim EH, Charpentier X, Torres-Urquidy O, McEvoy MM, Rensing C. 2009. The metal efflux island of Legionella pneumophila is not required for survival in macrophages and amoebas. FEMS Microbiol. Lett. 301:164-170.
60. Bellanger X, Roberts AP, Morel C, Choulet F, Pavlovic G, Mullany P, Decaris B, Guedon G. 2009. Conjugative transfer of the integrative conjugative elements ICESt1 and ICESt3 from Streptococcus thermophilus. J. Bacteriol. 191:2764-2775.
61. Burrus V, Pavlovic G, Decaris B, Guedon G. 2002. Conjugative transposons: the tip of the iceberg. Mol. Microbiol. 46:601-610.