Legionella pneumophila strain 130b possesses a unique combination of type IV secretion systems and novel Dot/Icm secretion system effector proteins

Journal of Bacteriology

Volumn 192, Issue 22, 2010, Pages 6001-6016

  Schroeder, Gunnar N ^a   Petty, Nicola K ^b   Mousnier, Aurélie ^a   Harding, Clare R ^a   Vogrin, Adam J ^d   Wee, Bryan ^b   Fry, Norman K ^c   Harrison, Timothy G ^c   Newton, Hayley J ^d   Thomson, Nicholas R ^e   Beatson, Scott A ^b   Dougan, Gordon ^e   Hartland, Elizabeth L ^d   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENETICS; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; GENE CLUSTER; GENE SEQUENCE; GENE TRANSLOCATION; LEGIONELLA; LEGIONELLA PNEUMOPHILA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SECRETION; SEQUENCE ANALYSIS; TYPE IV SECRETION SYSTEM;

CONSERVED SEQUENCE; DNA, BACTERIAL; ENVIRONMENTAL MICROBIOLOGY; GENOME, BACTERIAL; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; VIRULENCE FACTORS;

LEGIONELLA PNEUMOPHILA; PROTOZOA;

EID: 78049436241     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00778-10     Document Type: Article

References (98)

1. Alli, O. A., S. Zink, N. K. von Lackum, and Y. Abu-Kwaik. 2003. Comparative assessment of virulence traits in Legionella spp. Microbiology 149:631-641.
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. Alvarez-Martinez, C. E., and P. J. Christie. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775-808.
4. Asare, R., M. Santic, I. Gobin, M. Doric, J. Suttles, J. E. Graham, C. D. Price, and Y. Abu Kwaik. 2007. Genetic susceptibility and caspase activation in mouse and human macrophages are distinct for Legionella longbeachae and L. pneumophila. Infect. Immun. 75:1933-1945. (Pubitemid 46559463)
5. Backert, S., and T. F. Meyer. 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9:207-217.
6. Bandyopadhyay, P., S. Liu, C. B. Gabbai, Z. Venitelli, and H. M. Steinman. 2007. Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect. Immun. 75:723-735.
7. Brüggemann, H., C. Cazalet, and C. Buchrieser. 2006. Adaptation of Legionella pneumophila to the host environment: role of protein secretion, effectors and eukaryotic-like proteins. Curr. Opin. Microbiol. 9:86-94.
8. Bryant, C., and K. A. Fitzgerald. 2009. Molecular mechanisms involved in inflammasome activation. Trends Cell Biol. 19:455-464.
9. Burstein, D., T. Zusman, E. Degtyar, R. Viner, G. Segal, and T. Pupko. 2009. Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog. 5:e1000508.
10. Cambronne, E. D., and C. R. Roy. 2006. Recognition and delivery of effector proteins into eukaryotic cells by bacterial secretion systems. Traffic 7:929-939.
11. Campodonico, E. M., L. Chesnel, and C. R. Roy. 2005. A yeast genetic system for the identification and characterization of substrate proteins transferred into host cells by the Legionella pneumophila Dot/Icm system. Mol. Microbiol. 56:918-933.
12. Carver, T., N. Thomson, A. Bleasby, M. Berriman, and J. Parkhill. 2009. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25:119-120.
13. Carver, T. J., K. M. Rutherford, M. Berriman, M. A. Rajandream, B. G. Barrell, and J. Parkhill. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
14. Cazalet, C., L. Gomez-Valero, C. Rusniok, M. Lomma, D. Dervins-Ravault, H. J. Newton, F. M. Sansom, S. Jarraud, N. Zidane, L. Ma, C. Bouchier, J. Etienne, E. L. Hartland, and C. Buchrieser. 2010. Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet. 6:e1000851.
15. Cazalet, C., S. Jarraud, Y. Ghavi-Helm, F. Kunst, P. Glaser, J. Etienne, and C. Buchrieser. 2008. Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species. Genome Res. 18:431-441.
16. Cazalet, C., C. Rusniok, H. Bruggemann, N. Zidane, A. Magnier, L. Ma, M. Tichit, S. Jarraud, C. Bouchier, F. Vandenesch, F. Kunst, J. Etienne, P. Glaser, and C. Buchrieser. 2004. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36:1165-1173.
17. Charpentier, X., J. E. Gabay, M. Reyes, J. W. Zhu, A. Weiss, and H. A. Shuman. 2009. Chemical genetics reveals bacterial and host cell functions critical for type IV effector translocation by Legionella pneumophila. PLoS Pathog. 5:e1000501.
18. Chien, M., I. Morozova, S. Shi, H. Sheng, J. Chen, S. M. Gomez, G. Asamani, K. Hill, J. Nuara, M. Feder, J. Rineer, J. J. Greenberg, V. Steshenko, S. H. Park, B. Zhao, E. Teplitskaya, J. R. Edwards, S. Pampou, A. Georghiou, I. C. Chou, W. Iannuccilli, M. E. Ulz, D. H. Kim, A. Geringer-Sameth, C. Goldsberry, P. Morozov, S. G. Fischer, G. Segal, X. Qu, A. Rzhetsky, P. Zhang, E. Cayanis, P. J. De Jong, J. Ju, S. Kalachikov, H. A. Shuman, and J. J. Russo. 2004. The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305:1966-1968.
19. Christie, P. J., K. Atmakuri, V. Krishnamoorthy, S. Jakubowski, and E. Cascales. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451-485.
20. Cianciotto, N. P. 2009. Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila. Future Microbiol. 4:797-805.
21. Cirillo, S. L., J. Lum, and J. D. Cirillo. 2000. Identification of novel loci involved in entry by Legionella pneumophila. Microbiology 146:1345-1359.
22. Coburn, B., I. Sekirov, and B. B. Finlay. 2007. Type III secretion systems and disease. Clin. Microbiol. Rev. 20:535-549.
23. D'Auria, G., N. Jimenez-Hernandez, F. Peris-Bondia, A. Moya, and A. Latorre. 2010. Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11:181.
24. de Felipe, K. S., R. T. Glover, X. Charpentier, O. R. Anderson, M. Reyes, C. D. Pericone, and H. A. Shuman. 2008. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog. 4:e1000117.
25. de Felipe, K. S., S. Pampou, O. S. Jovanovic, C. D. Pericone, S. F. Ye, S. Kalachikov, and H. A. Shuman. 2005. Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J. Bacteriol. 187:7716-7726.
26. Diez, E., S. H. Lee, S. Gauthier, Z. Yaraghi, M. Tremblay, S. Vidal, and P. Gros. 2003. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 33:55-60.
27. Doléans-Jordheim, A., M. Akermi, C. Ginevra, C. Cazalet, E. Kay, D. Schneider, C. Buchrieser, D. Atlan, F. Vandenesch, J. Etienne, and S. Jarraud. 2006. Growth-phase-dependent mobility of the lvh-encoding region in Legionella pneumophila strain Paris. Microbiology 152:3561-3568.
28. Drosten, M., A. Dhawahir, E. Y. Sum, J. Urosevic, C. G. Lechuga, L. M. Esteban, E. Castellano, C. Guerra, E. Santos, and M. Barbacid. 2010. Genetic analysis of Ras signalling pathways in cell proliferation, migration and survival. EMBO J. 29:1091-1104.
29. Edelstein, P. H. 1986. Control of Legionella in hospitals. J. Hosp. Infect. 8:109-115.
30. Engleberg, N. C., D. J. Drutz, and B. I. Eisenstein. 1984. Cloning and expression of Legionella pneumophila antigens in Escherichia coli. Infect. Immun. 44:222-227.
31. Ensminger, A. W., and R. R. Isberg. 2009. Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr. Opin. Microbiol. 12:67-73.
32. Finn, R. D., J. Tate, J. Mistry, P. C. Coggill, S. J. Sammut, H. R. Hotz, G. Ceric, K. Forslund, S. R. Eddy, E. L. Sonnhammer, and A. Bateman. 2008. The Pfam protein families database. Nucleic Acids Res. 36:D281-D288.
33. Franco, I. S., H. A. Shuman, and X. Charpentier. 2009. The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell. Microbiol. 11:1435-1443.
34. Fraser, D. W., T. R. Tsai, W. Orenstein, W. E. Parkin, H. J. Beecham, R. G. Sharrar, J. Harris, G. F. Mallison, S. M. Martin, J. E. McDade, C. C. Shepard, and P. S. Brachman. 1977. Legionnaires' disease: description of an epidemic of pneumonia. N. Engl. J. Med. 297:1189-1197.
35. Fritz, J. H., R. L. Ferrero, D. J. Philpott, and S. E. Girardin. 2006. Nod-like proteins in immunity, inflammation and disease. Nat. Immunol. 7:1250-1257.
36. Fronzes, R., P. J. Christie, and G. Waksman. 2009. The structural biology of type IV secretion systems. Nat. Rev. Microbiol. 7:703-714.
37. Glöckner, G., C. Albert-Weissenberger, E. Weinmann, S. Jacobi, E. Schunder, M. Steinert, J. Hacker, and K. Heuner. 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.
38. Gomez-Valero, L., C. Rusniok, and C. Buchrieser. 2009. Legionella pneumophila: population genetics, phylogeny and genomics. Infect. Genet. Evol. 9:727-739.
39. Gordon, D., C. Abajian, and P. Green. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8:195-202. (Pubitemid 28177231)
40. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
41. Habyarimana, F., S. Al-Khodor, A. Kalia, J. E. Graham, C. T. Price, M. T. Garcia, and Y. A. Kwaik. 2008. Role for the Ankyrin eukaryotic-like genes of Legionella pneumophila in parasitism of protozoan hosts and human macrophages. Environ. Microbiol. 10:1460-1474.
42. Harrison, T. G., B. Afshar, N. Doshi, N. K. Fry, and J. V. Lee. 2009. Distribution of Legionella pneumophila serogroups, monoclonal antibody subgroups and DNA sequence types in recent clinical and environmental isolates from England and Wales (2000-2008). Eur. J. Clin. Microbiol. Infect. Dis. 28:781-791.
43. Helbig, J. H., S. Bernander, M. Castellani Pastoris, J. Etienne, V. Gaia, S. Lauwers, D. Lindsay, P. C. Luck, T. Marques, S. Mentula, M. F. Peeters, C. Pelaz, M. Struelens, S. A. Uldum, G. Wewalka, and T. G. Harrison. 2002. Pan-European study on culture-proven Legionnaires' disease: distribution of Legionella pneumophila serogroups and monoclonal subgroups. Eur. J. Clin. Microbiol. Infect. Dis. 21:710-716.
44. Hilbi, H., G. Segal, and H. A. Shuman. 2001. Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol. Microbiol. 42:603-617.
45. Hilbi, H., S. S. Weber, C. Ragaz, Y. Nyfeler, and S. Urwyler. 2007. Environmental predators as models for bacterial pathogenesis. Environ. Microbiol. 9:563-575.
46. Horwitz, M. A. 1983. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158:1319-1331.
47. Horwitz, M. A., and F. R. Maxfield. 1984. Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J. Cell Biol. 99:1936-1943.
48. Isberg, R. R., T. J. O'Connor, and M. Heidtman. 2009. The Legionella pneumophila replication vacuole: making a cozy niche inside host cells. Nat. Rev. Microbiol. 7:13-24.
49. Jacobi, S., and K. Heuner. 2003. Description of a putative type I secretion system in Legionella pneumophila. Int. J. Med. Microbiol. 293:349-358.
50. Juhas, M., D. W. Crook, I. D. Dimopoulou, G. Lunter, R. M. Harding, D. J. Ferguson, and D. W. Hood. 2007. Novel type IV secretion system involved in propagation of genomic islands. J. Bacteriol. 189:761-771.
51. Juhas, M., D. W. Crook, and D. W. Hood. 2008. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell. Microbiol. 10:2377-2386.
52. Jules, M., and C. Buchrieser. 2007. Legionella pneumophila adaptation to intracellular life and the host response: clues from genomics and transcriptomics. FEBS Lett. 581:2829-2838.
53. Kagan, J. C., and C. R. Roy. 2002. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol. 4:945-954.
54. Kinch, L. N., M. L. Yarbrough, K. Orth, and N. V. Grishin. 2009. Fido, a novel AMPylation domain common to fic, doc, and AvrB. PLoS One 4:e5818.
55. Komano, T., R. Utsumi, and M. Kawamukai. 1991. Functional analysis of the fic gene involved in regulation of cell division. Res. Microbiol. 142:269-277.
56. Kozak, N. A., M. Buss, C. E. Lucas, M. Frace, D. Govil, T. Travis, M. Olsen-Rasmussen, R. F. Benson, and B. S. Fields. 2010. Virulence factors encoded by Legionella longbeachae identified on the basis of the genome sequence analysis of clinical isolate D-4968. J. Bacteriol. 192:1030-1044.
57. Kubori, T., A. Hyakutake, and H. Nagai. 2008. Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol. Microbiol. 67:1307-1319.
58. Lamoth, F., and G. Greub. 2009. Amoebal pathogens as emerging causal agents of pneumonia. FEMS Microbiol. Rev. 10.1111/j.1574-6976.2009.00207.x.
59. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
60. Lehnherr, H., E. Maguin, S. Jafri, and M. B. Yarmolinsky. 1993. Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J. Mol. Biol. 233:414-428.
61. Letunic, I., T. Doerks, and P. Bork. 2009. SMART 6: recent updates and new developments. Nucleic Acids Res. 37:D229-D232.
62. Lomma, M., D. Dervins-Ravault, M. Rolando, T. Nora, H. J. Newton, F. M. Samson, T. Sahr, L. Gomez-Valero, M. Jules, E. L. Hartland, and C. Buchrieser. 2010. The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication. Cell. Microbiol. 10.1111/j.1462-5822.2010.01467.x.
63. Luo, Z. Q., and R. R. Isberg. 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.
64. Malumbres, M., and M. Barbacid. 2003. RAS oncogenes: the first 30 years. Nat. Rev. Cancer 3:459-465.
65. Marchler-Bauer, A., J. B. Anderson, F. Chitsaz, M. K. Derbyshire, C. DeWeese-Scott, J. H. Fong, L. Y. Geer, R. C. Geer, N. R. Gonzales, M. Gwadz, S. He, D. I. Hurwitz, J. D. Jackson, Z. Ke, C. J. Lanczycki, C. A. Liebert, C. Liu, F. Lu, S. Lu, G. H. Marchler, M. Mullokandov, J. S. Song, A. Tasneem, N. Thanki, R. A. Yamashita, D. Zhang, N. Zhang, and S. H. Bryant. 2009. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37:D205-D210.
66. McDade, J. E., C. C. Shepard, D. W. Fraser, T. R. Tsai, M. A. Redus, and W. R. Dowdle. 1977. Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N. Engl. J. Med. 297:1197-1203.
67. Mohd-Zain, Z., S. L. Turner, A. M. Cerdeno-Tarraga, A. K. Lilley, T. J. Inzana, A. J. Duncan, R. M. Harding, D. W. Hood, T. E. Peto, and D. W. Crook. 2004. Transferable antibiotic resistance elements in Haemophilus influenzae share a common evolutionary origin with a diverse family of syntenic genomic islands. J. Bacteriol. 186:8114-8122.
68. Molmeret, M., M. Horn, M. Wagner, M. Santic, and Y. Abu Kwaik. 2005. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71:20-28.
69. Morozova, I., X. Qu, S. Shi, G. Asamani, J. E. Greenberg, H. A. Shuman, and J. J. Russo. 2004. Comparative sequence analysis of the icm/dot genes in Legionella. Plasmid 51:127-147.
70. Newton, H. J., D. K. Ang, I. R. van Driel, and E. L. Hartland. 2010. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin. Microbiol. Rev. 23:274-298.
71. Newton, H. J., F. M. Sansom, V. Bennett-Wood, and E. L. Hartland. 2006. Identification of Legionella pneumophila-specific genes by genomic subtractive hybridization with Legionella micdadei and identification of lpnE, a gene required for efficient host cell entry. Infect. Immun. 74:1683-1691.
72. Ninio, S., J. Celli, and C. R. Roy. 2009. A Legionella pneumophila effector protein encoded in a region of genomic plasticity binds to Dot/Icm-modified vacuoles. PLoS Pathog. 5:e1000278.
73. Pan, X., A. Luhrmann, A. Satoh, M. A. Laskowski-Arce, and C. R. Roy. 2008. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320:1651-1654.
74. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
75. Price, C. T., S. Al-Khodor, T. Al-Quadan, M. Santic, F. Habyarimana, A. Kalia, and Y. A. Kwaik. 2009. Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog. 5:e1000704.
76. Pukatzki, S., S. B. McAuley, and S. T. Miyata. 2009. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12:11-17.
77. Ratzow, S., V. Gaia, J. H. Helbig, N. K. Fry, and P. C. Luck. 2007. Addition of neuA, the gene encoding N-acylneuraminate cytidylyl transferase, increases the discriminatory ability of the consensus sequence-based scheme for typing Legionella pneumophila serogroup 1 strains. J. Clin. Microbiol. 45:1965-1968.
78. Ridenour, D. A., S. L. Cirillo, S. Feng, M. M. Samrakandi, and J. D. Cirillo. 2003. Identification of a gene that affects the efficiency of host cell infection by Legionella pneumophila in a temperature-dependent fashion. Infect. Immun. 71:6256-6263.
79. Rossier, O., and N. P. Cianciotto. 2001. Type II protein secretion is a subset of the PilD-dependent processes that facilitate intracellular infection by Legionella pneumophila. Infect. Immun. 69:2092-2098.
80. Rowbotham, T. J. 1980. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33:1179-1183.
81. Roy, C. R., and S. Mukherjee. 2009. Bacterial FIC proteins AMP up infection. Sci. Signal. 2:pe14.
82. 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.
83. Samrakandi, M. M., S. L. Cirillo, D. A. Ridenour, L. E. Bermudez, and J. D. Cirillo. 2002. Genetic and phenotypic differences between Legionella pneumophila strains. J. Clin. Microbiol. 40:1352-1362.
84. Sansom, F. M., H. J. Newton, S. Crikis, N. P. Cianciotto, P. J. Cowan, A. J. d'Apice, and E. L. Hartland. 2007. A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell. Microbiol. 9:1922-1935.
85. Segal, G., M. Purcell, and H. A. Shuman. 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.
86. Segal, G., J. J. Russo, and H. A. Shuman. 1999. Relationships between a new type IV secretion system and the icm/dot virulence system of Legionella pneumophila. Mol. Microbiol. 34:799-809.
87. Shohdy, N., J. A. Efe, S. D. Emr, and H. A. Shuman. 2005. Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc. Natl. Acad. Sci. U. S. A. 102:4866-4871.
88. Steinert, M., K. Heuner, C. Buchrieser, C. Albert-Weissenberger, and G. Glockner. 2007. Legionella pathogenicity: genome structure, regulatory networks and the host cell response. Int. J. Med. Microbiol. 297:577-587.
89. Swanson, M. S., and R. R. Isberg. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609-3620.
90. Thomson, N. R., D. J. Clayton, D. Windhorst, G. Vernikos, S. Davidson, C. Churcher, M. A. Quail, M. Stevens, M. A. Jones, M. Watson, A. Barron, A. Layton, D. Pickard, R. A. Kingsley, A. Bignell, L. Clark, B. Harris, D. Ormond, Z. Abdellah, K. Brooks, I. Cherevach, T. Chillingworth, J. Woodward, H. Norberczak, A. Lord, C. Arrowsmith, K. Jagels, S. Moule, K. Mungall, M. Sanders, S. Whitehead, J. A. Chabalgoity, D. Maskell, T. Humphrey, M. Roberts, P. A. Barrow, G. Dougan, and J. Parkhill. 2008. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 18:1624-1637.
91. Vogel, J. P., H. L. Andrews, S. K. Wong, and R. R. Isberg. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279:873-876.
92. Weber, S. S., C. Ragaz, K. Reus, Y. Nyfeler, and H. Hilbi. 2006. Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog. 2:e46.
93. Wilkinson, P., K. Paszkiewicz, A. Moorhouse, J. M. Szubert, S. Beatson, J. Gerrard, N. R. Waterfield, and R. H. Ffrench-Constant. 2010. New plasmids and putative virulence factors from the draft genome of an Australian clinical isolate of Photorhabdus asymbiotica. FEMS Microbiol. Lett. 309:136-143.
94. Worby, C. A., S. Mattoo, R. P. Kruger, L. B. Corbeil, A. Koller, J. C. Mendez, B. Zekarias, C. Lazar, and J. E. Dixon. 2009. The FIC domain: regulation of cell signaling by adenylylation. Mol. Cell 34:93-103.
95. Wright, E. K., S. A. Goodart, J. D. Growney, V. Hadinoto, M. G. Endrizzi, E. M. Long, K. Sadigh, A. L. Abney, I. Bernstein-Hanley, and W. F. Dietrich. 2003. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13:27-36.
96. Wu, M., and J. A. Eisen. 2008. A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 9:R151.
97. Yarbrough, M. L., Y. Li, L. N. Kinch, N. V. Grishin, H. L. Ball, and K. Orth. 2009. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323:269-272.
98. Zusman, T., E. Degtyar, and G. Segal. 2008. Identification of a hypervariable region containing new Legionella pneumophila Icm/Dot translocated substrates by using the conserved icmQ regulatory signature. Infect. Immun. 76:4581-4591.