1887

Abstract

The type II protein secretion (T2S) system of secretes over 25 proteins, including novel proteins that have no similarity to proteins of known function. T2S is also critical for the ability of to grow within its natural amoebal hosts, including , and . Thus, T2S has an important role in the natural history of legionnaires’ disease. Our previous work demonstrated that the novel T2S substrate NttA promotes intracellular infection of , whereas the secreted RNase SrnA, acyltransferase PlaC, and metalloprotease ProA all promote infection of and . In this study, we determined that another novel T2S substrate that is specific to , designated NttC, is unique in being required for intracellular infection of but not for infection of or . Expanding our repertoire of amoebal hosts, we determined that is susceptible to infection by strains 130b, Philadelphia-1 and Paris. Furthermore, T2S and, more specifically, NttA, NttC and PlaC were required for infection of . Taken together, these data demonstrate that the T2S system of is critical for infection of at least four types of aquatic amoebae and that the importance of the individual T2S substrates varies in a host cell-specific fashion. Finally, it is now clear that novel T2S-dependent proteins that are specific to the genus are particularly important for infection of key, environmental hosts.

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2014-12-01
2020-05-28
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References

  1. Alary M., Joly J. R.. ( 1991;). Risk factors for contamination of domestic hot water systems by legionellae. Appl Environ Microbiol57:2360–2367[PubMed]
    [Google Scholar]
  2. Amaro F., Gilbert J. A., Owens S., Trimble W., Shuman H. A.. ( 2012;). Whole-genome sequence of the human pathogen Legionella pneumophila serogroup 12 strain 570-CO-H. J Bacteriol194:1613–1614 [CrossRef][PubMed]
    [Google Scholar]
  3. Anand C. M., Skinner A. R., Malic A., Kurtz J. B.. ( 1983;). Interaction of L. pneumophilia and a free living amoeba (Acanthamoeba palestinensis). J Hyg (Lond)91:167–178 [CrossRef][PubMed]
    [Google Scholar]
  4. Aragon V., Kurtz S., Flieger A., Neumeister B., Cianciotto N. P.. ( 2000;). Secreted enzymatic activities of wild-type and pilD-deficient Legionella pneumophila . Infect Immun68:1855–1863 [CrossRef][PubMed]
    [Google Scholar]
  5. Aragon V., Kurtz S., Cianciotto N. P.. ( 2001;). Legionella pneumophila major acid phosphatase and its role in intracellular infection. Infect Immun69:177–185 [CrossRef][PubMed]
    [Google Scholar]
  6. Banerji S., Bewersdorff M., Hermes B., Cianciotto N. P., Flieger A.. ( 2005;). Characterization of the major secreted zinc metalloprotease-dependent glycerophospholipid : cholesterol acyltransferase, PlaC, of Legionella pneumophila . Infect Immun73:2899–2909 [CrossRef][PubMed]
    [Google Scholar]
  7. Barbaree J. M., Fields B. S., Feeley J. C., Gorman G. W., Martin W. T.. ( 1986;). Isolation of protozoa from water associated with a legionellosis outbreak and demonstration of intracellular multiplication of Legionella pneumophila . Appl Environ Microbiol51:422–424[PubMed]
    [Google Scholar]
  8. Berk S. G., Ting R. S., Turner G. W., Ashburn R. J.. ( 1998;). Production of respirable vesicles containing live Legionella pneumophila cells by two Acanthamoeba spp.. Appl Environ Microbiol64:279–286[PubMed]
    [Google Scholar]
  9. Breiman R. F., Fields B. S., Sanden G. N., Volmer L., Meier A., Spika J. S.. ( 1990;). Association of shower use with Legionnaires’ disease. Possible role of amoebae. JAMA263:2924–2926 [CrossRef][PubMed]
    [Google Scholar]
  10. Brenner D. J., Steigerwalt A. G., McDade J. E.. ( 1979;). Classification of the Legionnaires’ disease bacterium: Legionella pneumophila, genus novum, species nova, of the family Legionellaceae, familia nova. Ann Intern Med90:656–658 [CrossRef][PubMed]
    [Google Scholar]
  11. Brenner D. J., Steigerwalt A. G., Gorman G. W., Wilkinson H. W., Bibb W. F., Hackel M., Tyndall R. L., Campbell J., Feeley J. C.. & other authors ( 1985;). Ten new species of Legionella . Int J Syst Bacteriol35:50–59 [CrossRef]
    [Google Scholar]
  12. Brieland J. K., Fantone J. C., Remick D. G., LeGendre M., McClain M., Engleberg N. C.. ( 1997;). The role of Legionella pneumophila-infected Hartmannella vermiformis as an infectious particle in a murine model of Legionnaire’s disease. Infect Immun65:5330–5333[PubMed]
    [Google Scholar]
  13. Brzuszkiewicz E., Schulz T., Rydzewski K., Daniel R., Gillmaier N., Dittmann C., Holland G., Schunder E., Lautner M.. & other authors ( 2013;). Legionella oakridgensis ATCC 33761 genome sequence and phenotypic characterization reveals its replication capacity in amoebae. Int J Med Microbiol303:514–528 [CrossRef][PubMed]
    [Google Scholar]
  14. Buse H. Y., Ashbolt N. J.. ( 2011;). Differential growth of Legionella pneumophila strains within a range of amoebae at various temperatures associated with in-premise plumbing. Lett Appl Microbiol53:217–224 [CrossRef][PubMed]
    [Google Scholar]
  15. Campbell J., Bibb W. F., Lambert M. A., Eng S., Steigerwalt A. G., Allard J., Moss C. W., Brenner D. J.. ( 1984;). Legionella sainthelensi: a new species of Legionella isolated from water near Mt. St. Helens. Appl Environ Microbiol47:369–373[PubMed]
    [Google Scholar]
  16. Cazalet C., Rusniok C., Brüggemann H., Zidane N., Magnier A., Ma L., Tichit M., Jarraud S., Bouchier C.. & other authors ( 2004;). Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet36:1165–1173 [CrossRef][PubMed]
    [Google Scholar]
  17. Cazalet C., Gomez-Valero L., Rusniok C., Lomma M., Dervins-Ravault D., Newton H. J., Sansom F. M., Jarraud S., Zidane N.. & other authors ( 2010;). Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires’ disease. PLoS Genet6:e1000851 [CrossRef][PubMed]
    [Google Scholar]
  18. Chatfield C. H., Cianciotto N. P.. ( 2007;). The secreted pyomelanin pigment of Legionella pneumophila confers ferric reductase activity. Infect Immun75:4062–4070 [CrossRef][PubMed]
    [Google Scholar]
  19. Chatfield C. H., Mulhern B. J., Burnside D. M., Cianciotto N. P.. ( 2011;). Legionella pneumophila LbtU acts as a novel, TonB-independent receptor for the legiobactin siderophore. J Bacteriol193:1563–1575 [CrossRef][PubMed]
    [Google Scholar]
  20. Chien M., Morozova I., Shi S., Sheng H., Chen J., Gomez S. M., Asamani G., Hill K., Nuara J.. & other authors ( 2004;). The genomic sequence of the accidental pathogen Legionella pneumophila . Science305:1966–1968 [CrossRef][PubMed]
    [Google Scholar]
  21. Cianciotto N. P.. ( 2005;). Type II secretion: a protein secretion system for all seasons. Trends Microbiol13:581–588 [CrossRef][PubMed]
    [Google Scholar]
  22. Cianciotto N. P.. ( 2009;). Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila . Future Microbiol4:797–805 [CrossRef][PubMed]
    [Google Scholar]
  23. Cianciotto N. P., Fields B. S.. ( 1992;). Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci U S A89:5188–5191 [CrossRef][PubMed]
    [Google Scholar]
  24. D’Auria G., Jiménez-Hernández N., Peris-Bondia F., Moya A., Latorre A.. ( 2010;). Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics11:181 [CrossRef][PubMed]
    [Google Scholar]
  25. DebRoy S., Aragon V., Kurtz S., Cianciotto N. P.. ( 2006a;). Legionella pneumophila Mip, a surface-exposed peptidylproline cis-trans-isomerase, promotes the presence of phospholipase C-like activity in culture supernatants. Infect Immun74:5152–5160 [CrossRef][PubMed]
    [Google Scholar]
  26. DebRoy S., Dao J., Söderberg M., Rossier O., Cianciotto N. P.. ( 2006b;). Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc Natl Acad Sci U S A103:19146–19151 [CrossRef][PubMed]
    [Google Scholar]
  27. Declerck P., Behets J., van Hoef V., Ollevier F.. ( 2007;). Detection of Legionella spp. and some of their amoeba hosts in floating biofilms from anthropogenic and natural aquatic environments. Water Res41:3159–3167 [CrossRef][PubMed]
    [Google Scholar]
  28. Dennis P. J., Brenner D. J., Thacker W. L., Wait R., Vesey G., Steigerwalt A. G., Benson R. F.. ( 1993;). Five new Legionella species isolated from water. Int J Syst Bacteriol43:329–337 [CrossRef][PubMed]
    [Google Scholar]
  29. Dey R., Bodennec J., Mameri M. O., Pernin P.. ( 2009;). Free-living freshwater amoebae differ in their susceptibility to the pathogenic bacterium Legionella pneumophila . FEMS Microbiol Lett290:10–17 [CrossRef][PubMed]
    [Google Scholar]
  30. Edelstein P. H., Cianciotto N. P.. ( 2010;). Legionella. Principles and Practice of Infectious Diseases, 7th edn.2969–2984 Mandell G. L., Bennett J. E., Dolin R.. Philadelphia: Elsevier Churchill Livingstone;
    [Google Scholar]
  31. Farhat M., Moletta-Denat M., Frère J., Onillon S., Trouilhé M. C., Robine E.. ( 2012;). Effects of disinfection on Legionella spp., Eukarya and biofilms in a hot water system. Appl Environ Microbiol78:6850–6858 [CrossRef][PubMed]
    [Google Scholar]
  32. Fields B. S.. ( 1996;). The molecular ecology of legionellae. Trends Microbiol4:286–290 [CrossRef][PubMed]
    [Google Scholar]
  33. Fields B. S., Sanden G. N., Barbaree J. M., Morrill W. E., Wadowsky R. M., White E. H., Feeley J. C.. ( 1989;). Intracellular multiplication of Legionella pneumophila in amoebae isolated from hospital hot water tanks. Curr Microbiol18:131–137 [CrossRef]
    [Google Scholar]
  34. Flieger A., Neumeister B., Cianciotto N. P.. ( 2002;). Characterization of the gene encoding the major secreted lysophospholipase A of Legionella pneumophila and its role in detoxification of lysophosphatidylcholine. Infect Immun70:6094–6106 [CrossRef][PubMed]
    [Google Scholar]
  35. Fliermans C. B., Cherry W. B., Orrison L. H., Smith S. J., Tison D. L., Pope D. H.. ( 1981;). Ecological distribution of Legionella pneumophila . Appl Environ Microbiol41:9–16[PubMed]
    [Google Scholar]
  36. Galka F., Wai S. N., Kusch H., Engelmann S., Hecker M., Schmeck B., Hippenstiel S., Uhlin B. E., Steinert M.. ( 2008;). Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun76:1825–1836 [CrossRef][PubMed]
    [Google Scholar]
  37. 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 Microbiol298:411–428 [CrossRef][PubMed]
    [Google Scholar]
  38. Grimm D., Ludwig W. F., Brandt B. C., Michel R., Schleifer K. H., Hacker J., Steinert M.. ( 2001;). Development of 18S rRNA-targeted oligonucleotide probes for specific detection of Hartmannella and Naegleria in Legionella-positive environmental samples. Syst Appl Microbiol24:76–82 [CrossRef][PubMed]
    [Google Scholar]
  39. Gunderson F. F., Cianciotto N. P.. ( 2013;). The CRISPR-associated gene cas2 of Legionella pneumophila is required for intracellular infection of amoebae. MBio4:e00074-13 [CrossRef][PubMed]
    [Google Scholar]
  40. Hales L. M., Shuman H. A.. ( 1999;). Legionella pneumophila contains a type II general secretion pathway required for growth in amoebae as well as for secretion of the Msp protease. Infect Immun67:3662–3666[PubMed]
    [Google Scholar]
  41. Harada E., Iida K., Shiota S., Nakayama H., Yoshida S.. ( 2010;). Glucose metabolism in Legionella pneumophila: dependence on the Entner-Doudoroff pathway and connection with intracellular bacterial growth. J Bacteriol192:2892–2899 [CrossRef][PubMed]
    [Google Scholar]
  42. Harf C., Monteil H.. ( 1988;). Interactions between free-living amoebae and Legionella in the environment. Water Sci Technol20:235–239
    [Google Scholar]
  43. Henke M., Seidel K. M.. ( 1986;). Association between Legionella pneumophila and amoebae in water. Isr J Med Sci22:690–695[PubMed]
    [Google Scholar]
  44. Herrmann V., Eidner A., Rydzewski K., Blädel I., Jules M., Buchrieser C., Eisenreich W., Heuner K.. ( 2011;). GamA is a eukaryotic-like glucoamylase responsible for glycogen- and starch-degrading activity of Legionella pneumophila . Int J Med Microbiol301:133–139 [CrossRef][PubMed]
    [Google Scholar]
  45. Hoffmann C., Harrison C. F., Hilbi H.. ( 2014;). The natural alternative: protozoa as cellular models for Legionella infection. Cell Microbiol16:15–26 [CrossRef][PubMed]
    [Google Scholar]
  46. Holden E. P., Winkler H. H., Wood D. O., Leinbach E. D.. ( 1984;). Intracellular growth of Legionella pneumophila within Acanthamoeba castellanii Neff. Infect Immun45:18–24[PubMed]
    [Google Scholar]
  47. Hsu B. M., Huang C. C., Chen J. S., Chen N. H., Huang J. T.. ( 2011;). Comparison of potentially pathogenic free-living amoeba hosts by Legionella spp. in substrate-associated biofilms and floating biofilms from spring environments. Water Res45:5171–5183 [CrossRef][PubMed]
    [Google Scholar]
  48. Korotkov K. V., Sandkvist M., Hol W. G.. ( 2012;). The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol10:336–351[PubMed]
    [Google Scholar]
  49. Kozak N. A., Buss M., Lucas C. E., Frace M., Govil D., Travis T., Olsen-Rasmussen M., Benson R. F., Fields B. S.. ( 2010;). Virulence factors encoded by Legionella longbeachae identified on the basis of the genome sequence analysis of clinical isolate D-4968. J Bacteriol192:1030–1044 [CrossRef][PubMed]
    [Google Scholar]
  50. Kuroki T., Sata S., Yamai S., Yagita K., Katsube Y., Endo T.. ( 1998a;). [Occurrence of free-living amoebae and Legionella in whirlpool baths]. Kansenshogaku Zasshi72:1056–1063[PubMed][CrossRef]
    [Google Scholar]
  51. Kuroki T., Yagita K., Yabuuchi E., Agata K., Ishima T., Katsube Y., Endo T.. ( 1998b;). [Isolation of Legionella and free-living amoebae at hot spring spas in Kanagawa, Japan]. Kansenshogaku Zasshi72:1050–1055[PubMed][CrossRef]
    [Google Scholar]
  52. La Scola B., Birtles R. J., Greub G., Harrison T. J., Ratcliff R. M., Raoult D.. ( 2004;). Legionella drancourtii sp. nov., a strictly intracellular amoebal pathogen. Int J Syst Evol Microbiol54:699–703 [CrossRef][PubMed]
    [Google Scholar]
  53. Lang C., Rastew E., Hermes B., Siegbrecht E., Ahrends R., Banerji S., Flieger A.. ( 2012;). Zinc metalloproteinase ProA directly activates Legionella pneumophila PlaC glycerophospholipid : cholesterol acyltransferase. J Biol Chem287:23464–23478 [CrossRef][PubMed]
    [Google Scholar]
  54. Lau H. Y., Ashbolt N. J.. ( 2009;). The role of biofilms and protozoa in Legionella pathogenesis: implications for drinking water. J Appl Microbiol107:368–378 [CrossRef][PubMed]
    [Google Scholar]
  55. Liles M. R., Edelstein P. H., Cianciotto N. P.. ( 1999;). The prepilin peptidase is required for protein secretion by and the virulence of the intracellular pathogen Legionella pneumophila . Mol Microbiol31:959–970 [CrossRef][PubMed]
    [Google Scholar]
  56. Livak K. J., Schmittgen T. D.. ( 2001;). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔ C T method. Methods25:402–408 [CrossRef][PubMed]
    [Google Scholar]
  57. McCoy-Simandle K., Stewart C. R., Dao J., DebRoy S., Rossier O., Bryce P. J., Cianciotto N. P.. ( 2011;). Legionella pneumophila type II secretion dampens the cytokine response of infected macrophages and epithelia. Infect Immun79:1984–1997 [CrossRef][PubMed]
    [Google Scholar]
  58. Michel R., Müller K. D., Amann R., Schmid E. N.. ( 1998;). Legionella-like slender rods multiplying within a strain of Acanthamoeba sp. isolated from drinking water. Parasitol Res84:84–88 [CrossRef][PubMed]
    [Google Scholar]
  59. Miyamoto H., Taniguchi H., Yoshida S.. ( 2003;). [A simple qualitative assay for intracellular growth of Legionella pneumophila within Acanthamoeba culbertsoni.]. Kansenshogaku Zasshi77:343–345[PubMed][CrossRef]
    [Google Scholar]
  60. Moffat J. F., Edelstein P. H., Regula D. P. Jr, Cirillo J. D., Tompkins L. S.. ( 1994;). Effects of an isogenic Zn-metalloprotease-deficient mutant of Legionella pneumophila in a guinea-pig pneumonia model. Mol Microbiol12:693–705 [CrossRef][PubMed]
    [Google Scholar]
  61. Molmeret M., Jarraud S., Mori J. P., Pernin P., Forey F., Reyrolle M., Vandenesch F., Etienne J., Farge P.. ( 2001;). Different growth rates in amoeba of genotypically related environmental and clinical Legionella pneumophila strains isolated from a thermal spa. Epidemiol Infect126:231–239 [CrossRef][PubMed]
    [Google Scholar]
  62. Mouchtouri V., Velonakis E., Tsakalof A., Kapoula C., Goutziana G., Vatopoulos A., Kremastinou J., Hadjichristodoulou C.. ( 2007;). Risk factors for contamination of hotel water distribution systems by Legionella species. Appl Environ Microbiol73:1489–1492 [CrossRef][PubMed]
    [Google Scholar]
  63. Newsome A. L., Baker R. L., Miller R. D., Arnold R. R.. ( 1985;). Interactions between Naegleria fowleri and Legionella pneumophila . Infect Immun50:449–452[PubMed]
    [Google Scholar]
  64. Newton H. J., Ang D. K., van Driel I. R., Hartland E. L.. ( 2010;). Molecular pathogenesis of infections caused by Legionella pneumophila . Clin Microbiol Rev23:274–298 [CrossRef][PubMed]
    [Google Scholar]
  65. Pagnier I., Merchat M., La Scola B.. ( 2009;). Potentially pathogenic amoeba-associated microorganisms in cooling towers and their control. Future Microbiol4:615–629 [CrossRef][PubMed]
    [Google Scholar]
  66. Pagnier I., Boughalmi M., Croce O., Robert C., Raoult D., La Scola B.. ( 2012;). Genome sequence of Legionella tunisiensis strain LegMT, a new Legionella species isolated from hypersaline lake water. J Bacteriol194:5978 [CrossRef][PubMed]
    [Google Scholar]
  67. Paszko-Kolva C., Yamamoto H., Shahamat M., Sawyer T. K., Morris G., Colwell R. R.. ( 1991;). Isolation of amoebae and Pseudomonas and Legionella spp. from eyewash stations. Appl Environ Microbiol57:163–167[PubMed]
    [Google Scholar]
  68. Pearce M. M., Cianciotto N. P.. ( 2009;). Legionella pneumophila secretes an endoglucanase that belongs to the family-5 of glycosyl hydrolases and is dependent upon type II secretion. FEMS Microbiol Lett300:256–264 [CrossRef][PubMed]
    [Google Scholar]
  69. Pearce M. M., Theodoropoulos N., Mandel M. J., Brown E., Reed K. D., Cianciotto N. P.. ( 2012;). Legionella cardiaca sp. nov., isolated from a case of native valve endocarditis in a human heart. Int J Syst Evol Microbiol62:2946–2954 [CrossRef][PubMed]
    [Google Scholar]
  70. Polesky A. H., Ross J. T., Falkow S., Tompkins L. S.. ( 2001;). Identification of Legionella pneumophila genes important for infection of amoebas by signature-tagged mutagenesis. Infect Immun69:977–987 [CrossRef][PubMed]
    [Google Scholar]
  71. Qin T., Cui Y., Cen Z., Liang T., Ren H., Yang X., Zhao X., Liu Z., Xu L.. & other authors ( 2012;). Draft genome sequences of two Legionella dumoffii strains, TEX-KL and NY-23. J Bacteriol194:1251–1252 [CrossRef][PubMed]
    [Google Scholar]
  72. Rossier O., Cianciotto N. P.. ( 2001;). Type II protein secretion is a subset of the PilD-dependent processes that facilitate intracellular infection by Legionella pneumophila . Infect Immun69:2092–2098 [CrossRef][PubMed]
    [Google Scholar]
  73. Rossier O., Cianciotto N. P.. ( 2005;). The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect Immun73:2020–2032 [CrossRef][PubMed]
    [Google Scholar]
  74. Rossier O., Starkenburg S. R., Cianciotto N. P.. ( 2004;). Legionella pneumophila type II protein secretion promotes virulence in the A/J mouse model of Legionnaires’ disease pneumonia. Infect Immun72:310–321 [CrossRef][PubMed]
    [Google Scholar]
  75. Rossier O., Dao J., Cianciotto N. P.. ( 2008;). The type II secretion system of Legionella pneumophila elaborates two aminopeptidases, as well as a metalloprotease that contributes to differential infection among protozoan hosts. Appl Environ Microbiol74:753–761 [CrossRef][PubMed]
    [Google Scholar]
  76. Rossier O., Dao J., Cianciotto N. P.. ( 2009;). A type II secreted ribonuclease of Legionella pneumophila facilitates optimal intracellular infection of Hartmannella vermiformis . Microbiology155:882–890 [CrossRef]
    [Google Scholar]
  77. Rowbotham T. J.. ( 1980;). Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol33:1179–1183 [CrossRef][PubMed]
    [Google Scholar]
  78. Rowbotham T. J.. ( 1986;). Current views on the relationships between amoebae, legionellae and man. Isr J Med Sci22:678–689[PubMed]
    [Google Scholar]
  79. Sahr T., Rusniok C., Dervins-Ravault D., Sismeiro O., Coppee J. Y., Buchrieser C.. ( 2012;). Deep sequencing defines the transcriptional map of L. pneumophila and identifies growth phase-dependent regulated ncRNAs implicated in virulence. RNA Biol9:503–519 [CrossRef][PubMed]
    [Google Scholar]
  80. Schroeder G. N., Petty N. K., Mousnier A., Harding C. R., Vogrin A. J., Wee B., Fry N. K., Harrison T. G., Newton H. J.. & other authors ( 2010;). Legionella pneumophila strain 130b possesses a unique combination of type IV secretion systems and novel Dot/Icm secretion system effector proteins. J Bacteriol192:6001–6016 [CrossRef][PubMed]
    [Google Scholar]
  81. Söderberg M. A., Dao J., Starkenburg S., Cianciotto N. P.. ( 2008;). Importance of type II secretion for survival of Legionella pneumophila in tap water and in amoebae at low temperatures. Appl Environ Microbiol74:5583–5588 [CrossRef][PubMed]
    [Google Scholar]
  82. Steinert M., Hentschel U., Hacker J.. ( 2002;). Legionella pneumophila: an aquatic microbe goes astray. FEMS Microbiol Rev26:149–162 [CrossRef][PubMed]
    [Google Scholar]
  83. Stewart C. R., Rossier O., Cianciotto N. P.. ( 2009;). Surface translocation by Legionella pneumophila: a form of sliding motility that is dependent upon type II protein secretion. J Bacteriol191:1537–1546 [CrossRef][PubMed]
    [Google Scholar]
  84. Stewart C. R., Burnside D. M., Cianciotto N. P.. ( 2011;). The surfactant of Legionella pneumophila is secreted in a TolC-dependent manner and is antagonistic toward other Legionella species. J Bacteriol193:5971–5984 [CrossRef][PubMed]
    [Google Scholar]
  85. Taylor M., Ross K., Bentham R.. ( 2009;). Legionella, protozoa, and biofilms: interactions within complex microbial systems. Microb Ecol58:538–547 [CrossRef][PubMed]
    [Google Scholar]
  86. Thacker W. L., Benson R. F., Hawes L., Gidding H., Dwyer B., Mayberry W. R., Brenner D. J.. ( 1991;). Legionella fairfieldensis sp. nov. isolated from cooling tower waters in Australia. J Clin Microbiol29:475–478[PubMed]
    [Google Scholar]
  87. Thacker W. L., Dyke J. W., Benson R. F., Havlichek D. H. Jr, Robinson-Dunn B., Stiefel H., Schneider W., Moss C. W., Mayberry W. R., Brenner D. J.. ( 1992;). Legionella lansingensis sp. nov. isolated from a patient with pneumonia and underlying chronic lymphocytic leukemia. J Clin Microbiol30:2398–2401[PubMed]
    [Google Scholar]
  88. Thomas V., McDonnell G., Denyer S. P., Maillard J. Y.. ( 2010;). Free-living amoebae and their intracellular pathogenic microorganisms: risks for water quality. FEMS Microbiol Rev34:231–259 [CrossRef][PubMed]
    [Google Scholar]
  89. Tyndall R. L., Domingue E. L.. ( 1982;). Cocultivation of Legionella pneumophila and free-living amoebae. Appl Environ Microbiol44:954–959[PubMed]
    [Google Scholar]
  90. Tyson J. Y., Pearce M. M., Vargas P., Bagchi S., Mulhern B. J., Cianciotto N. P.. ( 2013;). Multiple Legionella pneumophila Type II secretion substrates, including a novel protein, contribute to differential infection of the amoebae Acanthamoeba castellanii, Hartmannella vermiformis, and Naegleria lovaniensis . Infect Immun81:1399–1410 [CrossRef][PubMed]
    [Google Scholar]
  91. Valster R. M., Wullings B. A., van der Kooij D.. ( 2010;). Detection of protozoan hosts for Legionella pneumophila in engineered water systems by using a biofilm batch test. Appl Environ Microbiol76:7144–7153 [CrossRef][PubMed]
    [Google Scholar]
  92. Verma U. K., Brenner D. J., Thacker W. L., Benson R. F., Vesey G., Kurtz J. B., Dennis P. J., Steigerwalt A. G., Robinson J. S., Moss C. W.. ( 1992;). Legionella shakespearei sp. nov., isolated from cooling tower water. Int J Syst Bacteriol42:404–407 [CrossRef][PubMed]
    [Google Scholar]
  93. Wadowsky R. M., Wilson T. M., Kapp N. J., West A. J., Kuchta J. M., States S. J., Dowling J. N., Yee R. B.. ( 1991;). Multiplication of Legionella spp. in tap water containing Hartmannella vermiformis . Appl Environ Microbiol57:1950–1955[PubMed]
    [Google Scholar]
  94. Wilkinson H. W., Drasar V., Thacker W. L., Benson R. F., Schindler J., Potuznikova B., Mayberry W. R., Brenner D. J.. ( 1988;). Legionella moravica sp. nov. and Legionella brunensis sp. nov. isolated from cooling-tower water. Ann Inst Pasteur Microbiol139:393–402 [CrossRef][PubMed]
    [Google Scholar]
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