Comparative Genomics Reveal That Host-Innate Immune Responses Influence the Clinical Prevalence of Legionella pneumophila Serogroups

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Khan, Mohammad Adil ^a,b   Knox, Natalie ^c   Prashar, Akriti ^d   Alexander, David ^a,b   Abdel Nour, Mena ^a,b   Duncan, Carla ^a   Tang, Patrick ^a   Amatullah, Hajera ^e   Dos Santos, Claudia C ^e   Tijet, Nathalie ^a   Low, Donald E ^a,b,f   Pourcel, Christine ^g   Van Domselaar, Gary ^d   Terebiznik, Mauricio ^c   Ensminger, Alexander W ^a,b   Guyard, Cyril ^a,b,f  

^a PUBLIC HEALTH ONTARIO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e ST MICHAEL'S HOSPITAL   (Canada)

^f MOUNT SINAI HOSPITAL   (Canada)

^g UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM DETECTION; BACTERIUM ISOLATE; BIOSYNTHESIS; BLOOD GROUP TYPING; COMPLEMENT ALTERNATIVE PATHWAY; CONTROLLED STUDY; FEMALE; GENE CLUSTER; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MOUSE; NONHUMAN; PHYLOGENY; SEQUENCE HOMOLOGY; SG1 LPG GENE; SINGLE NUCLEOTIDE POLYMORPHISM; VARIABLE NUMBER OF TANDEM REPEAT; ACANTHAMOEBA CASTELLANII; ANIMAL; BIOFILM; CLASSIFICATION; COMPARATIVE STUDY; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LEGIONNAIRES' DISEASE; METABOLISM; MICROBIOLOGY; ONTARIO; PREVALENCE; PROTEIN CONFORMATION; SEROTYPE; U-937 CELL LINE;

LEGIONELLA; LEGIONELLA PNEUMOPHILA; LEGIONELLA PNEUMOPHILA SEROGROUP 1; MURINAE;

BACTERIAL PROTEIN; O ANTIGEN; PROTEOME;

ACANTHAMOEBA CASTELLANII; ANIMALS; BACTERIAL PROTEINS; BIOFILMS; DISEASE MODELS, ANIMAL; FEMALE; GENOME, BACTERIAL; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MICE; O ANTIGENS; ONTARIO; PHYLOGENY; PREVALENCE; PROTEIN CONFORMATION; PROTEOME; SEROGROUP; U937 CELLS;

EID: 84879520243     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067298     Document Type: Article

References (143)

1. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, et al. (1977) Legionnaires' disease: description of an epidemic of pneumonia. N Engl J Med 297: 1189-1197.
2. Newton HJ, Ang DK, van Driel IR, Hartland EL, (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23: 274-298.
3. Winn WC Jr, (1988) Legionnaires disease: historical perspective. Clin Microbiol Rev 1: 60-81.
4. Sanford JP, (1979) Legionnaires' disease: one person's perspective. Ann Intern Med 90: 699-703.
5. McDade JE, Shepard CC, Fraser DW, Tsai TR, Redus MA, et al. (1977) Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297: 1197-1203.
6. Yu VL, Plouffe JF, Pastoris MC, Stout JE, Schousboe M, et al. (2002) Distribution of Legionella species and serogroups isolated by culture in patients with sporadic community-acquired legionellosis: an international collaborative survey. J Infect Dis 186: 127-128.
7. Carratala J, Garcia-Vidal C, (2010) An update on Legionella. Curr Opin Infect Dis 23: 152-157.
8. Skaza AT, Beskovnik L, Storman A, Kese D, Ursic S, (2012) Epidemiological investigation of a legionellosis outbreak in a Slovenian nursing home, August 2010. Scand J Infect Dis 44: 263-269.
9. Haupt TE, Heffernan RT, Kazmierczak JJ, Nehls-Lowe H, Rheineck B, et al. (2012) An outbreak of legionnaires disease associated with a decorative water wall fountain in a hospital. Infect Control Hosp Epidemiol 33: 185-191.
10. Silk BJ, Moore MR, Bergtholdt M, Gorwitz RJ, Kozak NA, et al. (2012) Eight years of Legionnaires' disease transmission in travellers to a condominium complex in Las Vegas, Nevada. Epidemiol Infect: 1-10.
11. Legionellosis - United States, 2000-2009. MMWR Morb Mortal Wkly Rep 60: 1083-1086.
12. Hicks LA, Garrison LE, Nelson GE, Hampton LM, (2012) Legionellosis-United States, 2000-2009. Am J Transplant 12: 250-253.
13. Fields BS, Benson RF, Besser RE, (2002) Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 15: 506-526.
14. Straus WL, Plouffe JF, File TM Jr, Lipman HB, Hackman BH, et al. (1996) Risk factors for domestic acquisition of legionnaires disease. Ohio legionnaires Disease Group. Arch Intern Med 156: 1685-1692.
15. Stout JE, Yu VL, Yee YC, Vaccarello S, Diven W, et al. (1992) Legionella pneumophila in residential water supplies: environmental surveillance with clinical assessment for Legionnaires' disease. Epidemiol Infect 109: 49-57.
16. Stout JE, Yu VL, Muraca P, Joly J, Troup N, et al. (1992) Potable water as a cause of sporadic cases of community-acquired legionnaires' disease. N Engl J Med 326: 151-155.
17. Leoni E, Legnani PP, Bucci Sabattini MA, Righi F, (2001) Prevalence of Legionella spp. in swimming pool environment. Water Res 35: 3749-3753.
18. Tobin JO, Bartlett CL, Waitkins SA, Barrow GI, Macrae AD, et al. (1981) Legionnaires' disease: further evidence to implicate water storage and distribution systems as sources. Br Med J (Clin Res Ed) 282: 573.
19. Costa J, Tiago I, da Costa MS, Verissimo A, (2005) Presence and persistence of Legionella spp. in groundwater. Appl Environ Microbiol 71: 663-671.
20. Rogers J, Keevil CW, (1992) Immunogold and fluorescein immunolabelling of Legionella pneumophila within an aquatic biofilm visualized by using episcopic differential interference contrast microscopy. Appl Environ Microbiol 58: 2326-2330.
21. Mampel J, Spirig T, Weber SS, Haagensen JA, Molin S, et al. (2006) Planktonic replication is essential for biofilm formation by Legionella pneumophila in a complex medium under static and dynamic flow conditions. Appl Environ Microbiol 72: 2885-2895.
22. Berk SG, Faulkner G, Garduno E, Joy MC, Ortiz-Jimenez MA, et al. (2008) Packaging of live Legionella pneumophila into pellets expelled by Tetrahymena spp. does not require bacterial replication and depends on a Dot/Icm-mediated survival mechanism. Appl Environ Microbiol 74: 2187-2199.
23. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y, (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71: 20-28.
24. Rowbotham TJ, (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33: 1179-1183.
25. Abu Kwaik Y, Gao LY, Stone BJ, Venkataraman C, Harb OS, (1998) Invasion of protozoa by Legionella pneumophila and its role in bacterial ecology and pathogenesis. Appl Environ Microbiol 64: 3127-3133.
26. Berk SG, Ting RS, Turner GW, Ashburn RJ, (1998) Production of respirable vesicles containing live Legionella pneumophila cells by two Acanthamoeba spp. Appl Environ Microbiol 64: 279-286.
27. Brieland JK, Fantone JC, Remick DG, LeGendre M, McClain M, et al. (1997) The role of Legionella pneumophila-infected Hartmannella vermiformis as an infectious particle in a murine model of Legionnaire's disease. Infect Immun 65: 5330-5333.
28. Shi C, Pamer EG, (2011) Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11: 762-774.
29. Horwitz MA, Silverstein SC, (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest 66: 441-450.
30. Horwitz MA, (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158: 2108-2126.
31. Kagan JC, Roy CR, (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4: 945-954.
32. Vogel JP, Andrews HL, Wong SK, Isberg RR, (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
33. 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.
34. Helbig JH, Luck PC, Witzleb W, (1994) Serogroup-specific and serogroup-cross-reactive epitopes of Legionella pneumophila. Zentralbl Bakteriol 281: 16-23.
35. Luck PC, Helbig JH, Ehret W, Ott M, (1995) Isolation of a Legionella pneumophila strain serologically distinguishable from all known serogroups. Zentralbl Bakteriol 282: 35-39.
36. Olsen CW, Elverdal P, Jorgensen CS, Uldum SA, (2009) Comparison of the sensitivity of the Legionella urinary antigen EIA kits from Binax and Biotest with urine from patients with infections caused by less common serogroups and subgroups of Legionella. Eur J Clin Microbiol Infect Dis 28: 817-820.
37. Helbig JH, Uldum SA, Luck PC, Harrison TG, (2001) Detection of Legionella pneumophila antigen in urine samples by the BinaxNOW immunochromatographic assay and comparison with both Binax Legionella Urinary Enzyme Immunoassay (EIA) and Biotest Legionella Urin Antigen EIA. J Med Microbiol 50: 509-516.
38. Svarrer CW, Luck C, Elverdal PL, Uldum SA, (2012) Immunochromatic kits Xpect Legionella and BinaxNOW Legionella for detection of Legionella pneumophila urinary antigen have low sensitivities for the diagnosis of Legionnaires' disease. J Med Microbiol 61: 213-217.
39. Ng V, Tang P, Jamieson F, Guyard C, Low DE, et al. (2009) Laboratory-based evaluation of legionellosis epidemiology in Ontario, Canada, 1978 to 2006. BMC Infect Dis 9: 68.
40. Helbig JH, Bernander S, Castellani Pastoris M, Etienne J, Gaia V, et al. (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.
41. Doleans A, Aurell H, Reyrolle M, Lina G, Freney J, et al. (2004) Clinical and environmental distributions of Legionella strains in France are different. J Clin Microbiol 42: 458-460.
42. Cazalet C, Jarraud S, Ghavi-Helm Y, Kunst F, Glaser P, et al. (2008) Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species. Genome Res 18: 431-441.
43. Gaia V, Fry NK, Afshar B, Luck PC, Meugnier H, et al. (2005) Consensus sequence-based scheme for epidemiological typing of clinical and environmental isolates of Legionella pneumophila. J Clin Microbiol 43: 2047-2052.
44. Ratzow S, Gaia V, Helbig JH, Fry NK, Luck PC, (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.
45. Visca P, D'Arezzo S, Ramisse F, Gelfand Y, Benson G, et al. (2011) Investigation of the population structure of Legionella pneumophila by analysis of tandem repeat copy number and internal sequence variation. Microbiology 157: 2582-2594.
46. Sobral D, Le Cann P, Gerard A, Jarraud S, Lebeau B, et al. (2011) High-throughput typing method to identify a non-outbreak-involved Legionella pneumophila strain colonizing the entire water supply system in the town of Rennes, France. Appl Environ Microbiol 77: 6899-6907.
47. Giongo A, Tyler HL, Zipperer UN, Triplett EW, (2010) Two genome sequences of the same bacterial strain, Gluconacetobacter diazotrophicus PAl 5, suggest a new standard in genome sequence submission. Stand Genomic Sci 2: 309-317.
48. Latreille P, Norton S, Goldman BS, Henkhaus J, Miller N, et al. (2007) Optical mapping as a routine tool for bacterial genome sequence finishing. BMC Genomics 8: 321.
49. Ramirez MS, Adams MD, Bonomo RA, Centron D, Tolmasky ME, (2011) Genomic analysis of Acinetobacter baumannii A118 by comparison of optical maps: identification of structures related to its susceptibility phenotype. Antimicrob Agents Chemother 55: 1520-1526.
50. Shukla SK, Kislow J, Briska A, Henkhaus J, Dykes C, (2009) Optical mapping reveals a large genetic inversion between two methicillin-resistant Staphylococcus aureus strains. J Bacteriol 191: 5717-5723.
51. Lau HY, Ashbolt NJ, (2009) The role of biofilms and protozoa in Legionella pathogenesis: implications for drinking water. J Appl Microbiol 107: 368-378.
52. Wingender J, Flemming HC, (2011) Biofilms in drinking water and their role as reservoir for pathogens. Int J Hyg Environ Health 214: 417-423.
53. Dutka BJ, Walsh K, Ewan P, El-Shaarawi A, Tobin RS, (1984) Incidence of Legionella organisms in selected Ontario (Canada) cities. Sci Total Environ 39: 237-249.
54. Barker J, Brown MR, (1994) Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 140 (Pt 6): 1253-1259.
55. Philippe C, Blech MF, Hartemann P, (2006) Intra-amoebal development of Legionella pneumophila and the potential role of amoebae in the transmission of Legionnaires' disease. Med Mal Infect 36: 196-200.
56. Jules M, Buchrieser C, (2007) Legionella pneumophila adaptation to intracellular life and the host response: clues from genomics and transcriptomics. FEBS Lett 581: 2829-2838.
57. Arakawa K, Tomita M, (2007) The GC skew index: a measure of genomic compositional asymmetry and the degree of replicational selection. Evol Bioinform Online 3: 159-168.
58. 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.
59. Merault N, Rusniok C, Jarraud S, Gomez-Valero L, Cazalet C, et al. (2011) Specific real-time PCR for simultaneous detection and identification of Legionella pneumophila serogroup 1 in water and clinical samples. Appl Environ Microbiol 77: 1708-1717.
60. Gillespie JJ, Ammerman NC, Dreher-Lesnick SM, Rahman MS, Worley MJ, et al. (2009) An anomalous type IV secretion system in Rickettsia is evolutionarily conserved. PLoS One 4: e4833.
61. Sexton JA, Vogel JP, (2002) Type IVB secretion by intracellular pathogens. Traffic 3: 178-185.
62. Christie PJ, Vogel JP, (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8: 354-360.
63. 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.
64. Land AD, Winkler ME, (2011) The requirement for pneumococcal MreC and MreD is relieved by inactivation of the gene encoding PBP1a. J Bacteriol 193: 4166-4179.
65. Wachi M, Doi M, Okada Y, Matsuhashi M, (1989) New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells. J Bacteriol 171: 6511-6516.
66. Luneberg E, Zetzmann N, Alber D, Knirel YA, Kooistra O, et al. (2000) Cloning and functional characterization of a 30 kb gene locus required for lipopolysaccharide biosynthesis in Legionella pneumophila. Int J Med Microbiol 290: 37-49.
67. Greenfield LK, Whitfield C (2012) Synthesis of lipopolysaccharide O-antigens by ABC transporter-dependent pathways. Carbohydr Res.
68. Whitfield C, (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75: 39-68.
69. Trent MS, (2004) Biosynthesis, transport, and modification of lipid A. Biochem Cell Biol. 82: 71-86.
70. Rangarajan ES, Proteau A, Cui Q, Logan SM, Potetinova Z, et al. (2009) Structural and functional analysis of Campylobacter jejuni PseG: a udp-sugar hydrolase from the pseudaminic acid biosynthetic pathway. J Biol Chem 284: 20989-21000.
71. Raymond CK, Sims EH, Kas A, Spencer DH, Kutyavin TV, et al. (2002) Genetic variation at the O-antigen biosynthetic locus in Pseudomonas aeruginosa. J Bacteriol 184: 3614-3622.
72. Amaro F, Gilbert JA, Owens S, Trimble W, Shuman HA, (2012) Whole-genome sequence of the human pathogen Legionella pneumophila serogroup 12 strain 570-CO-H. J Bacteriol 194: 1613-1614.
73. Schroeder GN, Petty NK, Mousnier A, Harding CR, Vogrin AJ, et al. (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.
74. Tsai CM, Frasch CE, (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119: 115-119.
75. Ciesielski CA, Blaser MJ, Wang WL, (1986) Serogroup specificity of Legionella pneumophila is related to lipopolysaccharide characteristics. Infect Immun 51: 397-404.
76. Thomason BM, Bibb WF, (1984) Use of absorbed antisera for demonstration of antigenic variation among strains of Legionella pneumophila serogroup 1. J Clin Microbiol 19: 794-797.
77. Joly JR, McKinney RM, Tobin JO, Bibb WF, Watkins ID, et al. (1986) Development of a standardized subgrouping scheme for Legionella pneumophila serogroup 1 using monoclonal antibodies. J Clin Microbiol 23: 768-771.
78. Pluschke G, Mayden J, Achtman M, Levine RP, (1983) Role of the capsule and the O antigen in resistance of O18:K1 Escherichia coli to complement-mediated killing. Infect Immun 42: 907-913.
79. Grossman N, Schmetz MA, Foulds J, Klima EN, Jimenez-Lucho VE, et al. (1987) Lipopolysaccharide size and distribution determine serum resistance in Salmonella montevideo. J Bacteriol 169: 856-863.
80. Goebel EM, Wolfe DN, Elder K, Stibitz S, Harvill ET, (2008) O antigen protects Bordetella parapertussis from complement. Infect Immun 76: 1774-1780.
81. Schneider MC, Exley RM, Ram S, Sim RB, Tang CM, (2007) Interactions between Neisseria meningitidis and the complement system. Trends Microbiol 15: 233-240.
82. Vogel U, Weinberger A, Frank R, Muller A, Kohl J, et al. (1997) Complement factor C3 deposition and serum resistance in isogenic capsule and lipooligosaccharide sialic acid mutants of serogroup B Neisseria meningitidis. Infect Immun 65: 4022-4029.
83. Peitsch MC, Tschopp J, (1991) Assembly of macromolecular pores by immune defense systems. Curr Opin Cell Biol 3: 710-716.
84. Marcus RL, Shin HS, Mayer MM, (1971) An alternate complement pathway: C-3 cleaving activity, not due to C4,2a, on endotoxic lipopolysaccharide after treatment with guinea pig serum; relation to properdin. Proc Natl Acad Sci U S A 68: 1351-1354.
85. Daha MR, (2010) Role of complement in innate immunity and infections. Crit Rev Immunol 30: 47-52.
86. Lachmann PJ, Thompson RA, (1970) Reactive lysis: the complement-mediated lysis of unsensitized cells. II. The characterization of activated reactor as C56 and the participation of C8 and C9. J Exp Med 131: 643-657.
87. Rossi V, Wang Y, Esser AF, (2010) Topology of the membrane-bound form of complement protein C9 probed by glycosylation mapping, anti-peptide antibody binding, and disulfide modification. Mol Immunol 47: 1553-1560.
88. Brieland J, Freeman P, Kunkel R, Chrisp C, Hurley M, et al. (1994) Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J mice. A murine model of human Legionnaires' disease. Am J Pathol 145: 1537-1546.
89. Ogawa M, Yoshida S, Mizuguchi Y, (1994) 2-Deoxy-D-glucose inhibits intracellular multiplication and promotes intracellular killing of Legionella pneumophila in A/J mouse macrophages. Infect Immun 62: 266-270.
90. Takayanagi N, Ishiguro T, Matsushita A, Yoshii Y, Kagiyama N, et al. (2009) Severe complications and their outcomes in 65 patients with Legionella pneumonia. Nihon Kokyuki Gakkai Zasshi 47: 558-568.
91. Demello D, Kierol-Andrews L, Scalise PJ (2007) Severe sepsis and acute respiratory distress syndrome from community-acquired Legionella pneumonia: case report. Am J Crit Care 16: 320, 317.
92. Pan YJ, Lin TL, Hsu CR, Wang JT, (2011) Use of a Dictyostelium model for isolation of genetic loci associated with phagocytosis and virulence in Klebsiella pneumoniae. Infect Immun 79: 997-1006.
93. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, et al. (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5: e1000344.
94. Canals R, Jimenez N, Vilches S, Regue M, Merino S, et al. (2007) Role of Gne and GalE in the virulence of Aeromonas hydrophila serotype O34. J Bacteriol 189: 540-550.
95. Kooistra O, Luneberg E, Lindner B, Knirel YA, Frosch M, et al. (2001) Complex O-acetylation in Legionella pneumophila serogroup 1 lipopolysaccharide. Evidence for two genes involved in 8-O-acetylation of legionaminic acid. Biochemistry 40: 7630-7640.
96. Luck PC, Freier T, Steudel C, Knirel YA, Luneberg E, et al. (2001) A point mutation in the active site of Legionella pneumophila O-acetyltransferase results in modified lipopolysaccharide but does not influence virulence. Int J Med Microbiol 291: 345-352.
97. Zahringer U, Knirel YA, Lindner B, Helbig JH, Sonesson A, et al. (1995) The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog Clin Biol Res 392: 113-139.
98. Knirel YA, Senchenkova SN, Kocharova NA, Shashkov AS, Helbig JH, et al. (2001) Identification of a homopolymer of 5-acetamidino-7-acetamido-3,5,7,9-tetradeoxy-D-glycero-D-talo-nonulosonic acid in the lipopolysaccharides of Legionella pneumophila Non-1 serogroups. Biochemistry (Mosc) 66: 1035-1041.
99. Otten S, Iyer S, Johnson W, Montgomery R, (1986) Serospecific antigens of Legionella pneumophila. J Bacteriol 167: 893-904.
100. Lau PC, Lindhout T, Beveridge TJ, Dutcher JR, Lam JS, (2009) Differential lipopolysaccharide core capping leads to quantitative and correlated modifications of mechanical and structural properties in Pseudomonas aeruginosa biofilms. J Bacteriol 191: 6618-6631.
101. Wildschutte H, Wolfe DM, Tamewitz A, Lawrence JG, (2004) Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. Proc Natl Acad Sci U S A 101: 10644-10649.
102. Nakao R, Senpuku H, Watanabe H, (2006) Porphyromonas gingivalis galE is involved in lipopolysaccharide O-antigen synthesis and biofilm formation. Infect Immun 74: 6145-6153.
103. Holden EP, Winkler HH, Wood DO, Leinbach ED, (1984) Intracellular growth of Legionella pneumophila within Acanthamoeba castellanii Neff. Infect Immun 45: 18-24.
104. Napoli C, Fasano F, Iatta R, Barbuti G, Cuna T, et al. (2010) Legionella spp. and legionellosis in southeastern Italy: disease epidemiology and environmental surveillance in community and health care facilities. BMC Public Health 10: 660.
105. Boccia S, Laurenti P, Borella P, Moscato U, Capalbo G, et al. (2006) Prospective 3-year surveillance for nosocomial and environmental Legionella pneumophila: implications for infection control. Infect Control Hosp Epidemiol 27: 459-465.
106. Harrison TG, Afshar B, Doshi N, Fry NK, Lee JV, (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.
107. Mekkour M, Ben-Driss EK, Cohen N, (2012) Prevalence of Legionella pneumophila in production networks and distribution of domestic hot water in Morocco. World Environment 2: 11-15.
108. Ewan BJDaP, (1983) First Isolation of Legionella pneumophila from the Canadian Great Lakes. Journal of Great Lakes Research 9: 430-432.
109. McCallum KL, Schoenhals G, Laakso D, Clarke B, Whitfield C, (1989) A high-molecular-weight fraction of smooth lipopolysaccharide in Klebsiella serotype O1:K20 contains a unique O-antigen epitope and determines resistance to nonspecific serum killing. Infect Immun 57: 3816-3822.
110. Williams P, Lambert PA, Brown MR, Jones RJ, (1983) The role of the O and K antigens in determining the resistance of Klebsiella aerogenes to serum killing and phagocytosis. J Gen Microbiol 129: 2181-2191.
111. Mintz CS, Schultz DR, Arnold PI, Johnson W, (1992) Legionella pneumophila lipopolysaccharide activates the classical complement pathway. Infect Immun 60: 2769-2776.
112. Kojouharova M, Reid K, Gadjeva M, (2010) New insights into the molecular mechanisms of classical complement activation. Mol Immunol 47: 2154-2160.
113. Conrad DH, Carlo JR, Ruddy S, (1978) Interaction of beta1H globulin with cell-bound C3b: quantitative analysis of binding and influence of alternative pathway components on binding. J Exp Med 147: 1792-1805.
114. Bellinger-Kawahara C, Horwitz MA, (1990) Complement component C3 fixes selectively to the major outer membrane protein (MOMP) of Legionella pneumophila and mediates phagocytosis of liposome-MOMP complexes by human monocytes. J Exp Med 172: 1201-1210.
115. Ohno A, Isii Y, Tateda K, Matumoto T, Miyazaki S, et al. (1995) Role of LPS length in clearance rate of bacteria from the bloodstream in mice. Microbiology 141 (Pt 10): 2749-2756.
116. Plouffe JF, Para MF, Fuller KA, (1985) Serum bactericidal activity against Legionella pneumophila. J Clin Microbiol 22: 863-864.
117. Horwitz MA, Silverstein SC, (1981) Interaction of the legionnaires' disease bacterium (Legionella pneumophila) with human phagocytes. II. Antibody promotes binding of L. pneumophila to monocytes but does not inhibit intracellular multiplication. J Exp Med 153: 398-406.
118. Ferguson JS, Weis JJ, Martin JL, Schlesinger LS, (2004) Complement protein C3 binding to Mycobacterium tuberculosis is initiated by the classical pathway in human bronchoalveolar lavage fluid. Infect Immun 72: 2564-2573.
119. Chiaraviglio L, Brown DA, Kirby JE, (2008) Infection of cultured human endothelial cells by Legionella pneumophila. PLoS One 3: e2012.
120. O'Connor TJ, Adepoju Y, Boyd D, Isberg RR, (2011) Minimization of the Legionella pneumophila genome reveals chromosomal regions involved in host range expansion. Proc Natl Acad Sci U S A 108: 14733-14740.
121. Cherry WB, Pittman B, Harris PP, Hebert GA, Thomason BM, et al. (1978) Detection of Legionnaires disease bacteria by direct immunofluorescent staining. J Clin Microbiol 8: 329-338.
122. Thacker WL, Wilkinson HW, Benson RF, (1983) Comparison of slide agglutination test and direct immunofluorescence assay for identification of Legionella isolates. J Clin Microbiol 18: 1113-1118.
123. Tijet N, Tang P, Romilowych M, Duncan C, Ng V, et al. (2010) New endemic Legionella pneumophila serogroup I clones, Ontario, Canada. Emerg Infect Dis 16: 447-454.
124. Duncan C, Prashar A, So J, Tang P, Low DE, et al. (2011) Lcl of Legionella pneumophila is an immunogenic GAG binding adhesin that promotes interactions with lung epithelial cells and plays a crucial role in biofilm formation. Infect Immun 79: 2168-2181.
125. Lebeau I, Lammertyn E, De Buck E, Maes L, Geukens N, et al. (2004) Novel transcriptional regulators of Legionella pneumophila that affect replication in Acanthamoeba castellanii. Arch Microbiol 181: 362-370.
126. Ensminger AW, Yassin Y, Miron A, Isberg RR, (2012) Experimental Evolution of Legionella pneumophila in Mouse Macrophages Leads to Strains with Altered Determinants of Environmental Survival. PLoS Pathog 8: e1002731.
127. Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, et al. (2003) GenDB-an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31: 2187-2195.
128. Reimer AR, Van Domselaar G, Stroika S, Walker M, Kent H, et al. (2011) Comparative genomics of Vibrio cholerae from Haiti, Asia, and Africa. Emerg Infect Dis 17: 2113-2121.
129. Linke B, McHardy AC, Neuweger H, Krause L, Meyer F, (2006) REGANOR: a gene prediction server for prokaryotic genomes and a database of high quality gene predictions for prokaryotes. Appl Bioinformatics 5: 193-198.
130. Badger JH, Olsen GJ, (1999) CRITICA: coding region identification tool invoking comparative analysis. Mol Biol Evol 16: 512-524.
131. Delcher AL, Bratke KA, Powers EC, Salzberg SL, (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
132. Suzek BE, Ermolaeva MD, Schreiber M, Salzberg SL, (2001) A probabilistic method for identifying start codons in bacterial genomes. Bioinformatics 17: 1123-1130.
133. Schattner P, Brooks AN, Lowe TM, (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33: W686-689.
134. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, et al. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100-3108.
135. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
136. Rice P, Longden I, Bleasby A, (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
137. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-222.
138. Haft DH, Selengut JD, White O, (2003) The TIGRFAMs database of protein families. Nucleic Acids Res 31: 371-373.
139. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M, (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40: D109-114.
140. Sonnhammer EL, von Heijne G, Krogh A, (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6: 175-182.
141. Nielsen H, Brunak S, von Heijne G, (1999) Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng 12: 3-9.
142. Petkau A, Stuart-Edwards M, Stothard P, Van Domselaar G, (2010) Interactive microbial genome visualization with GView. Bioinformatics 26: 3125-3126.
143. McKinney RM, Thomason BM, Harris PP, Thacker L, Lewallen KR, et al. (1979) Recognition of a new serogroup of Legionnaires disease bacterium. J Clin Microbiol 9: 103-107.