The role of biofilms and protozoa in legionella pathogenesis: Implications for drinking water

Journal of Applied Microbiology

Volumn 107, Issue 2, 2009, Pages 368-378

  Lau, H Y ^a   Ashbolt, N J ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Biofilm; Drinking water; Protozoa; Virulence; Water quality.

Indexed keywords

BIOFILMS; CELL CULTURE; MAMMALS; PROTOZOA; WATER DISTRIBUTION SYSTEMS; WATER QUALITY;

CELL LINES; CURRENT MODELING; DRINKING WATER SYSTEMS; FREE LIVINGS; LEGIONELLA SPP; LEGIONELLAE; MURINE MODEL; PATHOGENICS; VIRULENCE; WATER QUALITY.;

POTABLE WATER;

DRINKING WATER;

BACTERIUM; BIOFILM; DRINKING WATER; PATHOGENICITY; PNEUMONIA; PROTOZOAN; VIRULENCE; WATER QUALITY;

ACANTHAMOEBA; AMEBIASIS; AQUATIC ENVIRONMENT; BIOFILM; CELL MIGRATION; CELL PROLIFERATION; HUMAN; LEGIONELLA; LEGIONNAIRE DISEASE; MACROPHAGE; NONHUMAN; PHAGOCYTE; PROTOZOON; REVIEW; WATER CONTAMINATION; WATER SUPPLY;

ACANTHAMOEBA; BACTERIA (MICROORGANISMS); LEGIONELLA; MAMMALIA; MURINAE; PROTOZOA;

EID: 68049146040     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2009.04208.x     Document Type: Review

References (110)

1. Albert-Weissenberger, C., Cazalet, C. Buchrieser, C. (2007) Legionella pneumophila- a human pathogen that co-evolved with fresh water protozoa. Cell Mol Life Sci 64, 432 448.
2. Allen, P.G. Dawidowicz, E.A. (1990a) Phagocytosis in Acanthamoeba: I. A mannose receptor is responsible for the binding and phagocytosis of yeast. J Cell Physiol 145, 508 513.
3. Allen, P.G. Dawidowicz, E.A. (1990b) Phagocytosis in Acanthamoeba: II. Soluble and insoluble mannose-rich ligands stimulate phosphoinositide metabolism. J Cell Physiol 145, 514 521.
4. Armstrong, T.W. Haas, C.N. (2008) Legionnaires' disease: evaluation of a quantitative microbial risk assessment model. J Water Health 6, 149 166.
5. Azara, A., Piana, A., Sotgiu, G., Dettori, M., Deriu, M.G., Masia, M.D., Are, B.M. Muresu, E. (2006) Prevalence study of Legionella spp. contamination in ferries and cruise ships. BMC Public Health 6, 100.
6. 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 Microbiol 51, 422 424.
7. Barbeau, J. Buhler, T. (2001) Biofilms augment the number of free-living amoebae in dental unit waterlines. Res Microbiol 152, 753 760.
8. Barker, J., Brown, M.R., Collier, P.J., Farrell, I. Gilbert, P. (1992) Relationship between Legionella pneumophila and Acanthamoeba polyphaga: physiological status and susceptibility to chemical inactivation. Appl Environ Microbiol 58, 2420 2425.
9. Barker, J., Lambert, P.A. Brown, M.R. (1993) Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila. Infect Immun 61, 3503 3510.
10. Bartram, J., Chartlier, Y., Lee, J.V., Pond, K. Surman-Lee, S. (2007) Legionella and the Prevention of Legionellosis. Geneva : World Health Organization.
11. Benin, A.L., Benson, R.F. Besser, R.E. (2002) Trends in legionnaires disease, 1980-1998: declining mortality and new patterns of diagnosis. Clin Infect Dis 35, 1039 1046.
12. 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 Microbiol 64, 279 286.
13. Bhan, U., Trujillo, G., Lyn-Kew, K., Newstead, M.W., Zeng, X., Hogaboam, C.M., Krieg, A.M. Standiford, T.J. (2008) Toll-like receptor 9 regulates the lung macrophage phenotype and host immunity in murine pneumonia caused by Legionella pneumophila. Infect Immun 76, 2895 2904.
14. Borella, P., Montagna, M.T., Romano-Spica, V., Stampi, S., Stancanelli, G., Triassi, M., Neglia, R., Marchesi, I. et al. (2004) Legionella infection risk from domestic hot water. Emerg Infect Dis 10, 457 464.
15. Bornstein, N., Vieilly, C., Nowicki, M., Paucod, J.C. Fleurette, J. (1986) Epidemiological evidence of legionellosis transmission through domestic hot water supply systems and possibilities of control. Isr J Med Sci 22, 655 661.
16. Bouyer, S., Imbert, C., Rodier, M.H. Hechard, Y. (2007) Long-term survival of Legionella pneumophila associated with Acanthamoeba castellanii vesicles. Environ Microbiol 9, 1341 1344.
17. Bozue, J.A. Johnson, W. (1996) Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect Immun 64, 668 673.
18. Breiman, R.F., Cozen, W., Fields, B.S., Mastro, T.D., Carr, S.J., Spika, J.S. Mascola, L. (1990a) Role of air sampling in investigation of an outbreak of legionnaires' disease associated with exposure to aerosols from an evaporative condenser. J Infect Dis 161, 1257 1261.
19. Breiman, R.F., Fields, B.S., Sanden, G.N., Volmer, L., Meier, A. Spika, J.S. (1990b) Association of shower use with Legionnaires' disease. Possible role of amoebae. JAMA 263, 2924 2926.
20. 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 Med 90, 656 658.
21. Brooks, S.E. Schneider, D.L. (1985) Oxidative metabolism associated with phagocytosis in Acanthamoeba castellanii. J Protozool 32, 330 333.
22. Brown, R.C., Bass, H. Coombs, J.P. (1975) Carbohydrate binding proteins involved in phagocytosis by Acanthamoeba. Nature 254, 434 435.
23. Byrne, B. Swanson, M.S. (1998) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66, 3029 3034.
24. Cao, Z., Jefferson, D.M. Panjwani, N. (1998) Role of carbohydrate- mediated adherence in cytopathogenic mechanisms of Acanthamoeba. J Biol Chem 273, 15838 15845.
25. Carlesso, A.M., Simonetti, A.B., Artuso, G.L. Rott, M.B. (2007) Isolation and identification of potentially pathogenic free-living amoebae in samples from environments in a public hospital in the city of Porto Alegre, Rio Grande do Sul. Rev Soc Bras Med Trop 40, 316 320.
26. Chen, J., de Felipe, K.S., Clarke, M., Lu, H., Anderson, O.R., Segal, G. Shuman, H.A. (2004) Legionella effectors that promote nonlytic release from protozoa. Science 303, 1358 1361.
27. Chen, J., Reyes, M., Clarke, M. Shuman, H.A. (2007) Host cell-dependent secretion and translocation of the LepA and LepB effectors of Legionella pneumophila. Cell Microbiol 9, 1660 1671.
28. Cirillo, J.D., Falkow, S. Tompkins, L.S. (1994) Growth of Legionella pneumophila in Acanthamoeba castellanii enhances invasion. Infect Immun 62, 3254 3261.
29. Cirillo, J.D., Cirillo, S.L., Yan, L., Bermudez, L.E., Falkow, S. Tompkins, L.S. (1999) Intracellular growth in Acanthamoeba castellanii affects monocyte entry mechanisms and enhances virulence of Legionella pneumophila. Infect Immun 67, 4427 4434.
30. Colbourne, J.S. Dennis, P.J. (1985) Distribution and persistence of Legionella in water systems. Microbiol Sci 2, 40 43.
31. Corsaro, D., Feroldi, V., Saucedo, G., Ribas, F., Loret, J.F. Greub, G. (2009) Novel Chlamydiales strains isolated from a water treatment plant. Environ Microbiol 11, 188 200.
32. Davies, B. Edwards, S.W. (1991) Chemiluminescence and superoxide production in Acanthamoeba castellanii: free radicals generated during oxidative stress. J Gen Microbiol 137, 1021 1027.
33. Davies, B., Chattings, L.S. Edwards, S.W. (1991) Superoxide generation during phagocytosis by Acanthamoeba castellanii: similarities to the respiratory burst of immune phagocytes. J Gen Microbiol 137, 705 710.
34. Declerck, P., Behets, J., De Keersmaecker, B. Ollevier, F. (2007a) Receptor-mediated uptake of Legionella pneumophila by Acanthamoeba castellanii and Naegleria lovaniensis. J Appl Microbiol 103, 2697 2703.
35. Declerck, P., Behets, J., Margineanu, A., van Hoef, V., De Keersmaecker, B. Ollevier, F. (2007b) Replication of Legionella pneumophila in biofilms of water distribution pipes. Microbiol Res
36. Declerck, P., Behets, J., van Hoef, V. Ollevier, F. (2007c) Detection of Legionella spp. and some of their amoeba hosts in floating biofilms from anthropogenic and natural aquatic environments. Water Res 41, 3159 3167.
37. Doyle, R.M. Heuzenroeder, M.W. (2002) A mutation in an ompR-like gene on a Legionella longbeachae serogroup 1 plasmid attenuates virulence. Int J Med Microbiol 292, 227 239.
38. Doyle, R.M., Cianciotto, N.P., Banvi, S., Manning, P.A. Heuzenroeder, M.W. (2001) Comparison of virulence of Legionella longbeachae strains in guinea pigs and U937 macrophage-like cells. Infect Immun 69, 5335 5344.
39. Fields, B.S., Shotts, E.B., Jr., Feeley, J.C., Gorman, G.W. Martin, W.T. (1984) Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated protozoan Tetrahymena pyriformis. Appl Environ Microbiol 47, 467 471.
40. 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 Microbiol 18, 131 137.
41. 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 Microbiol 41, 9 16.
42. Gao, L.Y. Abu Kwaik, Y. (1999) Apoptosis in macrophages and alveolar epithelial cells during early stages of infection by Legionella pneumophila and its role in cytopathogenicity. Infect Immun 67, 862 870.
43. Gao, L.Y. Abu Kwaik, Y. (2000) The mechanism of killing and exiting the protozoan host Acanthamoeba polyphaga by Legionella pneumophila. Environ Microbiol 2, 79 90.
44. Gao, L.Y., Susa, M., Ticac, B. Abu Kwaik, Y. (1999) Heterogeneity in intracellular replication and cytopathogenicity of Legionella pneumophila and Legionella micdadei in mammalian and protozoan cells. Microb Pathog 27, 273 287.
45. Garcia, M.T., Jones, S., Pelaz, C., Millar, R.D. Abu Kwaik, Y. (2007) Acanthamoeba polyphaga resuscitates viable non-culturable Legionella pneumophila after disinfection. Environ Microbiol 9, 1267 1277.
46. Gebran, S.J., Yamamoto, Y., Newton, C., Klein, T.W. Friedman, H. (1994) Inhibition of Legionella pneumophila growth by gamma interferon in permissive A/J mouse macrophages: role of reactive oxygen species, nitric oxide, tryptophan, and iron(III). Infect Immun 62, 3197 3205.
47. Gerhardt, H., Walz, M.J., Faigle, M., Northoff, H., Wolburg, H. Neumeister, B. (2000) Localization of Legionella bacteria within ribosome-studded phagosomes is not restricted to Legionella pneumophila. FEMS Microbiol Lett 192, 145 152.
48. Glick, T.H., Gregg, M.B., Berman, B., Mallison, G., Rhodes, W.W., Jr. Kassanoff, I. (1978) Pontiac fever. An epidemic of unknown etiology in a health department: I. Clinical and epidemiologic aspects. Am J Epidemiol 107, 149 160.
49. Greub, G. Raoult, D. (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17, 413 433.
50. Hagele, S., Kohler, R., Merkert, H., Schleicher, M., Hacker, J. Steinert, M. (2000) Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2, 165 171.
51. Halablab, M.A., Bazin, M., Richards, L. Pacy, J. (1990) Ultra-structure and localisation of formazan formed by human neutrophils and amoebae phagocytosing virulent and avirulent Legionella pneumophila. FEMS Microbiol Immunol 2, 295 301.
52. Harb, O.S., Venkataraman, C., Haack, B.J., Gao, L.Y. Kwaik, Y.A. (1998) Heterogeneity in the attachment and uptake mechanisms of the Legionnaires' disease bacterium, Legionella pneumophila, by protozoan hosts. Appl Environ Microbiol 64, 126 132.
53. Hay, J., Seal, D.V., Billcliffe, B. Freer, J.H. (1995) Non-culturable Legionella pneumophila associated with Acanthamoeba castellanii: detection of the bacterium using DNA amplification and hybridization. J Appl Bacteriol 78, 61 65.
54. Horwitz, M.A. (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158, 2108 2126.
55. Horwitz, M.A. (1984) Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36, 27 33.
56. Horwitz, M.A. Maxfield, F.R. (1984) Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J Cell Biol 99, 1936 1943.
57. Huws, S.A., McBain, A.J. Gilbert, P. (2005) Protozoan grazing and its impact upon population dynamics in biofilm communities. J Appl Microbiol 98, 238 244.
58. Jacobs, R.F., Locksley, R.M., Wilson, C.B., Haas, J.E. Klebanoff, S.J. (1984) Interaction of primate alveolar macrophages and Legionella pneumophila. J Clin Invest 73, 1515 1523.
59. Kikuhara, H., Ogawa, M., Miyamoto, H., Nikaido, Y. Yoshida, S. (1994) Intracellular multiplication of Legionella pneumophila in Tetrahymena thermophila. J UOEH 16, 263 275.
60. Kilvington, S. Price, J. (1990) Survival of Legionella pneumophila within cysts of Acanthamoeba polyphaga following chlorine exposure. J Appl Bacteriol 68, 519 525.
61. Kirby, J.E., Vogel, J.P., Andrews, H.L. Isberg, R.R. (1998) Evidence for pore-forming ability by Legionella pneumophila. Mol Microbiol 27, 323 336.
62. 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 Microbiol 54, 699 703.
63. Lammertyn, E. Anne, J. (2004) Protein secretion in Legionella pneumophila and its relation to virulence. FEMS Microbiol Lett 238, 273 279.
64. Lehtola, M.J., Torvinen, E., Kusnetsov, J., Pitkanen, T., Maunula, L., von Bonsdorff, C.H., Martikainen, P.J., Wilks, S.A. et al. (2007) Survival of Mycobacterium avium, Legionella pneumophila, Escherichia coli, and caliciviruses in drinking water-associated biofilms grown under high-shear turbulent flow. Appl Environ Microbiol 73, 2854 2859.
65. Liang, J.L., Dziuban, E.J., Craun, G.F., Hill, V., Moore, M.R., Gelting, R.J., Calderon, R.L., Beach, M.J. et al. (2006) Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking - United States, 2003-2004. MMWR Surveill Summ 55, 31 65.
66. Linehan, S.A., Martinez-Pomares, L. Gordon, S. (2000) Macrophage lectins in host defence. Microbes Infect 2, 279 288.
67. Lock, R., Ohman, L. Dahlgren, C. (1987) Phagocytic recognition mechanisms in human granulocytes and Acanthamoeba castellanii using type 1 fimbriated Escherichia coli as phagocytic prey. FEMS Microbiol Lett 44, 135 140.
68. Loret, J.F., Jousset, M., Robert, S., Saucedo, G., Ribas, F., Thomas, V. Greub, G. (2008) Amoebae-resisting bacteria in drinking water: risk assessment and management. Water Sci Technol 58, 571 577.
69. Marston, B.J., Plouffe, J.F., File, T.M., Jr., Hackman, B.A., Salstrom, S.J., Lipman, H.B., Kolczak, M.S. Breiman, R.F. (1997) Incidence of community-acquired pneumonia requiring hospitalization. Results of a population-based active surveillance Study in Ohio. The Community-Based Pneumonia Incidence Study Group. Arch Intern Med 157, 1709 1718.
70. Miyamoto, M., Yamaguchi, Y. Sasatsu, M. (2000) Disinfectant effects of hot water, ultraviolet light, silver ions and chlorine on strains of Legionella and nontuberculous mycobacteria. Microbios 101, 7 13.
71. Molmeret, M., Alli, O.A., Zink, S., Flieger, A., Cianciotto, N.P. Kwaik, Y.A. (2002) icmT is essential for pore formation-mediated egress of Legionella pneumophila from mammalian and protozoan cells. Infect Immun 70, 69 78.
72. Molmeret, M., Bitar, D.M., Han, L. Kwaik, Y.A. (2004) Disruption of the phagosomal membrane and egress of Legionella pneumophila into the cytoplasm during the last stages of intracellular infection of macrophages and Acanthamoeba polyphaga. Infect Immun 72, 4040 4051.
73. Murga, R., Forster, T.S., Brown, E., Pruckler, J.M., Fields, B.S. Donlan, R.M. (2001) Role of biofilms in the survival of Legionella pneumophila in a model potable-water system. Microbiology 147, 3121 3126. (Pubitemid 33077000)
74. Nagl, M., Starlinger, R. Tiefenbrunner, F. (2000) Influence of sequential cultivation on virulence of Legionella pneumophila and Staphylococcus aureus. Int J Hyg Environ Health 203, 165 167.
75. Neil, K. Berkelman, R. (2008) Increasing incidence of legionellosis in the United States, 1990-2005: changing epidemiologic trends. Clin Infect Dis 47, 591 599.
76. 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.
77. Neumeister, B., Reiff, G., Faigle, M., Dietz, K., Northoff, H. Lang, F. (2000) Influence of Acanthamoeba castellanii on intracellular growth of different Legionella species in human monocytes. Appl Environ Microbiol 66, 914 919.
78. Newsome, A.L., Baker, R.L., Miller, R.D. Arnold, R.R. (1985) Interactions between Naegleria fowleri and Legionella pneumophila. Infect Immun 50, 449 452.
79. Ohno, A., Kato, N., Yamada, K. Yamaguchi, K. (2003) Factors influencing survival of Legionella pneumophila serotype 1 in hot spring water and tap water. Appl Environ Microbiol 69, 2540 2547.
80. Park, M., Yun, S.T., Kim, M.S., Chun, J. Ahn, T.I. (2004) Phylogenetic characterization of Legionella-like endosymbiotic X-bacteria in Amoeba proteus: a proposal for 'Candidatus Legionella jeonii' sp. nov. Environ Microbiol 6, 1252 1263.
81. Pryor, M., Springthorpe, S., Riffard, S., Brooks, T., Huo, Y., Davis, G. Sattar, S.A. (2004) Investigation of opportunistic pathogens in municipal drinking water under different supply and treatment regimes. Water Sci Technol 50, 83 90.
82. Rechnitzer, C. Blom, J. (1989) Engulfment of the Philadelphia strain of Legionella pneumophila within pseudopod coils in human phagocytes. Comparison with other Legionella strains and species. APMIS 97, 105 114.
83. Reingold, A.L., Thomason, B.M., Brake, B.J., Thacker, L., Wilkinson, H.W. Kuritsky, J.N. (1984) Legionella pneumonia in the United States: the distribution of serogroups and species causing human illness. J Infect Dis 149, 819.
84. Rogers, J. Keevil, C.W. (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.
85. Roig, J., Sabria, M. Pedro-Botet, M.L. (2003) Legionella spp.: community acquired and nosocomial infections. Curr Opin Infect Dis 16, 145 151.
86. Rowbotham, T.J. (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33, 1179 1183.
87. Rowbotham, T.J. (1983) Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J Clin Pathol 36, 978 986.
88. Rowbotham, T.J. (1986) Current views on the relationships between amoebae, legionellae and man. Isr J Med Sci 22, 678 689.
89. Schopf, R.E., Mattar, J., Meyenburg, W., Scheiner, O., Hammann, K.P. Lemmel, E.M. (1984) Measurement of the respiratory burst in human monocytes and polymorphonuclear leukocytes by nitro blue tetrazolium reduction and chemiluminescence. J Immunol Methods 67, 109 117.
90. Seno, M., Sakaki, M., Ogawa, H., Matsuda, H. Takeda, Y. (2006) Effective proliferation of low level Legionella pneumophila serogroup 1 cells using coculture procedure with Acanthamoeba castellanii. J Microbiol Methods 66, 564 567.
91. Shoff, M.E., Rogerson, A., Kessler, K., Schatz, S. Seal, D.V. (2008) Prevalence of Acanthamoeba and other naked amoebae in South Florida domestic water. J Water Health 6, 99 104.
92. Singh, T. Coogan, M.M. (2005) Isolation of pathogenic Legionella species and legionella-laden amoebae in dental unit waterlines. J Hosp Infect 61, 257 262.
93. Steinert, M., Emody, L., Amann, R. Hacker, J. (1997) Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl Environ Microbiol 63, 2047 2053.
94. Storey, M.V., Winiecka-Krusnell, J., Ashbolt, N.J. Stenstrom, T.A. (2004) The efficacy of heat and chlorine treatment against thermotolerant Acanthamoebae and Legionellae. Scand J Infect Dis 36, 656 662.
95. Swanson, M.S. Isberg, R.R. (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63, 3609 3620.
96. Temmerman, R., Vervaeren, H., Noseda, B., Boon, N. Verstraete, W. (2006) Necrotrophic growth of Legionella pneumophila. Appl Environ Microbiol 72, 4323 4328.
97. Thomas, V., Herrera-Rimann, K., Blanc, D.S. Greub, G. (2006) Biodiversity of amoebae and amoeba-resisting bacteria in a hospital water network. Appl Environ Microbiol 72, 2428 2438.
98. Thomas, V., Casson, N. Greub, G. (2007) New Afipia and Bosea strains isolated from various water sources by amoebal co-culture. Syst Appl Microbiol 30, 572 579.
99. Thomas, V., Loret, J.F., Jousset, M. Greub, G. (2008) Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Environ Microbiol 10, 2728 2745.
100. Tilney, L.G., Harb, O.S., Connelly, P.S., Robinson, C.G. Roy, C.R. (2001) How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J Cell Sci 114, 4637 4650.
101. Tsai, T.F., Finn, D.R., Plikaytis, B.D., McCauley, W., Martin, S.M. Fraser, D.W. (1979) Legionnaires' disease: clinical features of the epidemic in Philadelphia. Ann Intern Med 90, 509 517.
102. Tyndall, R.L. Domingue, E.L. (1982) Cocultivation of Legionella pneumophila and free-living amoebae. Appl Environ Microbiol 44, 954 959.
103. USEPA (2000) The History of Drinking Water Treatment, EPA-816-F-00-006. Washington, DC : US Environmental Protection Agency, Office of Water.
104. Wadowsky, R.M., Yee, R.B., Mezmar, L., Wing, E.J. Dowling, J.N. (1982) Hot water systems as sources of Legionella pneumophila in hospital and nonhospital plumbing fixtures. Appl Environ Microbiol 43, 1104 1110.
105. Wadowsky, R.M., Butler, L.J., Cook, M.K., Verma, S.M., Paul, M.A., Fields, B.S., Keleti, G., Sykora, J.L. et al. (1988) Growth-supporting activity for Legionella pneumophila in tap water cultures and implication of hartmannellid amoebae as growth factors. Appl Environ Microbiol 54, 2677 2682.
106. Weinbaum, D.L., Benner, R.R., Dowling, J.N., Alpern, A., Pasculle, A.W. Donowitz, G.R. (1984) Interaction of Legionella micdadei with human monocytes. Infect Immun 46, 68 73.
107. Williams, M.M., Santo Domingo, J.W. Meckes, M.C. (2005) Population diversity in model potable water biofilms receiving chlorine or chloramine residual. Biofouling 21, 279 288.
108. Winn, W.C., Jr. Myerowitz, R.L. (1981) The pathology of the Legionella pneumonias. A review of 74 cases and the literature. Hum Pathol 12, 401 422.
109. Yoder, J., Roberts, V., Craun, G.F., Hill, V., Hicks, L., Alexander, N.T., Radke, V., Calderon, R.L., Hlavsa, M.C., Beach, M.J. Roy, S.L. (2008) Surveillance for waterborne disease and outbreaks associated with recreational water use and other aquatic facility-associated health events - United States, 2005-2006 and surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking - United States, 2005-2006. Morbid Mortal Wkly Rep Surv Summ 57, 1 69.
110. Yu, V.L., Plouffe, J.F., Pastoris, M.C., Stout, J.E., Schousboe, M., Widmer, A., Summersgill, J., File, T. 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.