Biofilms: The stronghold of Legionella pneumophila

International Journal of Molecular Sciences

Volumn 14, Issue 11, 2013, Pages 21660-21675

  Abdel Nour, Mena ^a,b,c   Duncan, Carla ^a   Low, Donald E ^b,c   Guyard, Cyril ^a,b,c  

^a PUBLIC HEALTH ONTARIO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Amoeba; Legionella pneumophila; Legionellosis; Multispecies biofilms; Prozoa

Indexed keywords

BIOCIDE; CYCLIC DI GMP; CYCLIC GMP; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; IRON; LACTOFERRIN; UNCLASSIFIED DRUG;

AQUATIC ENVIRONMENT; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; BIOFOULING; ENVIRONMENTAL CHANGE; ENVIRONMENTAL STRESS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; NONHUMAN; PROTOZOON; REVIEW; WATER CONTAMINATION;

BIOFILMS; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONELLOSIS;

EID: 84887134409     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141121660     Document Type: Review

References (106)

1. Carratala, J.; Fernandez-Sabe, N.; Ortega, L.; Castellsague, X.; Roson, B.; Dorca, J.; Fernandez-Aguera, A.; Verdaguer, R.; Martinez, J.; Manresa, F.; et al. Outpatient care compared with hospitalization for community-acquired pneumonia: A randomized trial in low-risk patients. Ann. Intern. Med. 2005, 142, 165-172.
2. Yu, V. L.; Plouffe, J. F.; Pastoris, M. C.; Stout, J. E.; Schousboe, M.; Widmer, A.; Summersgill, J.; File, T.; Heath, C. M.; Paterson, D. L.; et al. Distribution of Legionella species and serogroups isolated by culture in patients with sporadic community-acquired Legionellosis: An international collaborative survey. J. Infect. Dis. 2002, 186, 127-128.
3. Bentham, R. H.; Broadbent, C. R. A model for autumn outbreaks of Legionnaires' disease associated with cooling towers, linked to system operation and size. Epidemiol. Infect. 1993, 111, 287-295.
4. Fields, B. S.; Benson, R. F.; Besser, R. E. Legionella and Legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 2002, 15, 506-526.
5. Feazel, L. M.; Baumgartner, L. K.; Peterson, K. L.; Frank, D. N.; Kirk Harris, J.; Pace, N. R. Opportunistic pathogens enriched in showerhead biofilms. Proc. Natl. Acad. Sci. USA 2009, 106, 16393-16398.
6. McEvoy, M.; Batchelor, N.; Hamilton, G.; MacDonald, A.; Faiers, M.; Sills, A.; Lee, J.; Harrison, T. A cluster of cases of Legionnaires' disease associated with exposure to a spa pool on display. Commun. Dis. Public Health 2000, 3, 43-45.
7. Wadowsky, R. M.; Yee, R. B.; Mezmar, L.; Wing, E. J.; Dowling, J. N. Hot water systems as sources of Legionella pneumophila in hospital and nonhospital plumbing fixtures. Appl. Environ. Microbiol. 1982, 43, 1104-1110.
8. Hindre, T.; Bruggemann, H.; Buchrieser, C.; Hechard, Y. Transcriptional profiling of Legionella Pneumophila biofilm cells and the influence of iron on biofilm formation. Microbiology 2008, 154, 30-41.
9. Pecastaings, S.; Berge, M.; Dubourg, K. M.; Roques, C. Sessile Legionella pneumophila is able to grow on surfaces and generate structured monospecies biofilms. Biofouling 2010, 26, 809-819.
10. Kwon, S.; Moon, E.; Kim, T.; Hong, S.; Park, H. Pyrosequencing demonstrated complex microbial communities in a membrane filtration system for a drinking water treatment plant. Microbes Environ. 2011, 26, 149-155.
11. Murga, R.; Forster, T. S.; Brown, E.; Pruckler, J. M.; Fields, B. S.; Donlan, R. M. Role of biofilms in the survival of Legionella pneumophila in a model potable-water system. Microbiology 2001, 147, 3121-3126.
12. Rowbotham, T. J. Pontiac fever, ameobae and Legionllae. Lancet 1981, 317, 40-41.
13. Molmeret, M.; Horn, M.; Wagner, M.; Santic, M.; Abu Kwaik, Y. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 2005, 71, 20-28.
14. Steinert, M.; Hentschel, U.; Hacker, J. Legionella pneumophila: An aquatic microbe goes astray. FEMS Microbiol. Rev. 2002, 26, 149-162.
15. Yan, L.; Cerny, R. L.; Cirillo, J. D. Evidence that hsp90 is involved in the altered interactions of Acanthamoeba castellanii variants with bacteria. Eukaryotic Cell 2004, 3, 567-578.
16. Chaabna, Z.; Forey, F.; Reyrolle, M.; Jarraud, S.; Atlan, D.; Fontvieille, D.; Gilbert, C. Molecular diversity and high virulence of Legionella pneumophila strains isolated from biofilms developed within a warm spring of a thermal spa. BMC Microbiol. 2013, 13, 17.
17. Abu Khweek, A.; Fernandez Davila, N. S.; Caution, K.; Akhter, A.; Abdulrahman, B. A.; Tazi, M.; Hassan, H.; Novotny, L. A.; Bakaletz, L. O.; Amer, A. O. Biofilm-derived Legionella pneumophila evades the innate immune response in macrophages. Front. Cell Infect. Microbiol. 2013, 3, 18.
18. Barker, J.; Lambert, P. A.; Brown, M. R. Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila. Infect. Immun. 1993, 61, 3503-3510.
19. Newsome, A. L.; Farone, M. B.; Berk, S. G.; Gunderson, J. H. Free living amoebae as opportunistic hosts for intracellular bacterial parasites. J. Eukaryot. Microbiol. 2001, 48, 13S-14S.
20. Rowbotham, T. J. Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J. Clin. Pathol. 1983, 36, 978-986.
21. Skinner, A. R.; Anand, C. M.; Malic, A.; Kurtz, J. B. Acanthamoebae and environmental spread of Legionella pneumophila. Lancet 1983, 2, 289-290.
22. Taylor, M.; Ross, K.; Bentham, R. Legionella, protozoa, and biofilms: Interactions within complex microbial systems. Microb. Ecol. 2009, 58, 538-547.
23. Valster, R. M.; Wullings, B. A.; van der Kooij, D. Detection of protozoan hosts for Legionella pneumophila in engineered water systems by using a biofilm batch test. Appl. Environ. Microbiol. 2010, 76, 7144-7153.
24. Valster, R. M.; Wullings, B. A.; van den Berg, R.; van der Kooij, D. Relationships between free-living protozoa, cultivable Legionella spp., and water quality characteristics in three drinking water supplies in the caribbean. Appl. Environ. Microbiol. 2011, 77, 7321-7328.
25. Liu, R.; Yu, Z.; Guo, H.; Liu, M.; Zhang, H.; Yang, M. Pyrosequencing analysis of eukaryotic and bacterial communities in faucet biofilms. Sci. Total Environ. 2012, 435-436, 124-131.
26. Mampel, J.; Spirig, T.; Weber, S. S.; Haagensen, J. A.; Molin, S.; Hilbi, H. Planktonic replication is essential for biofilm formation by Legionella pneumophila in a complex medium under static and dynamic flow conditions. Appl. Environ. Microbiol. 2006, 72, 2885-2895.
27. Temmerman, R.; Vervaeren, H.; Noseda, B.; Boon, N.; Verstraete, W. Necrotrophic growth of Legionella pneumophila. Appl. Environ. Microbiol. 2006, 72, 4323-4328.
28. Declerck, P.; Behets, J.; van Hoef, V.; Ollevier, F. Replication of Legionella pneumophila in floating biofilms. Curr. Microbiol. 2007, 55, 435-440.
29. Hsu, B.; Huang, C.; Chen, J.; Chen, N.; Huang, J. Comparison of potentially pathogenic free-living amoeba hosts by Legionella spp. in substrate-associated biofilms and floating biofilms from spring environments. Water Res. 2011, 45, 5171-5183.
30. Atlas, R. M. Legionella: From environmental habitats to disease pathology, detection and control. Environ. Microbiol. 1999, 1, 283-293.
31. Hoffman, P. S. Invasion of eukaryotic cells by Legionella pneumophila: A common strategy for all hosts? Can. J. Infect. Dis. 1997, 8, 139-146.
32. Donlan, R. M.; Forster, T.; Murga, R.; Brown, E.; Lucas, C.; Carpenter, J.; Fields, B. Legionella pneumophila associated with the protozoan Hartmannella vermiformis in a model multi-species biofilm has reduced susceptibility to disinfectants. Biofouling 2005, 21, 1-7.
33. Thomas, V.; Bouchez, T.; Nicolas, V.; Robert, S.; Loret, J. F.; Levi, Y. Amoebae in domestic water systems: Resistance to disinfection treatments and implication in Legionella persistence. J. Appl. Microbiol. 2004, 97, 950-963.
34. Storey, M. V.; Winiecka-Krusnell, J.; Ashbolt, N. J.; Stenstrom, T. The efficacy of heat and chlorine treatment against thermotolerant Acanthamoebae and Legionellae. Scand. J. Infect. Dis. 2004, 36, 656-662.
35. Wright, J. B.; Ruseska, I.; Athar, M. A.; Corbett, S.; Costerton, J. W. Legionella pneumophila grows adherent to surfaces in vitro and in situ. Infect. Control Hosp. Epidemiol. 1989, 10, 408-415.
36. Rogers, J.; Dowsett, A. B.; Dennis, P. J.; Lee, J. V.; Keevil, C. W. Influence of plumbing materials on biofilm formation and growth of Legionella pneumophila in potable water systems. Appl. Environ. Microbiol. 1994, 60, 1842-1851.
37. Rogers, J.; Dowsett, A. B.; Dennis, P. J.; Lee, J. V.; Keevil, C. W. Influence of temperature and plumbing material selection on biofilm formation and growth of Legionella pneumophila in a model potable water system containing complex microbial flora. Appl. Environ. Microbiol. 1994, 60, 1585-1592.
38. Moritz, M. M.; Flemming, H.; Wingender, J. Integration of Pseudomonas aeruginosa and Legionella pneumophila in drinking water biofilms grown on domestic plumbing materials. Int. J. Hyg. Environ. Health 2010, 213, 190-197.
39. Geesey, G. G.; Wigglesworth-Cooksey, B.; Cooksey, K. E. Influence of calcium and other cations on surface adhesion of bacteria and diatoms: A review. Biofouling 2000, 15, 195-205.
40. Koubar, M.; Rodier, M. H.; Frere, J. Involvement of minerals in adherence of Legionella pneumophila to surfaces. Curr. Microbiol. 2013, 66, 437-442.
41. Yaradou, D. F.; Raze, D.; Ginevra, C.; Ader, F.; Doleans-Jordheim, A.; Vandenesch, F.; Menozzi, F. D.; Etienne, J.; Jarraud, S. Zinc-dependent cytoadherence of Legionella pneumophila to human alveolar epithelial cells in vitro. Microb. Pathog. 2007, 43, 234-242.
42. Bargellini, A.; Marchesi, I.; Righi, E.; Ferrari, A.; Cencetti, S.; Borella, P.; Rovesti, S. Parameters predictive of Legionella contamination in hot water systems: Association with trace elements and heterotrophic plate counts. Water Res. 2011, 45, 2315-2321.
43. Borella, P.; Montagna, M. T.; Romano-Spica, V.; Stampi, S.; Stancanelli, G.; Triassi, M.; Marchesi, I.; Bargellini, A.; Neglia, R.; Paglionico, N.; et al. Relationship between mineral content of domestic hot water and microbial contamination. J. Trace Elem. Med. Biol. 2003, 17, 37-43.
44. Boyd, C. D.; Chatterjee, D.; Sondermann, H.; O'Toole, G. A. LapG, required for modulating biofilm formation by Pseudomonas fluorescens Pf0-1, is a calcium-dependent protease. J. Bacteriol. 2012, 194, 4406-4414.
45. Chatterjee, D.; Boyd, C. D.; O'Toole, G. A.; Sondermann, H. Structural characterization of a conserved, calcium-dependent periplasmic protease from Legionella pneumophila. J. Bacteriol. 2012, 194, 4415-4425.
46. Giao, M. S.; Wilks, S. A.; Azevedo, N. F.; Vieira, M. J.; Keevil, C. W. Comparison between standard culture and peptide nucleic acid 16S rRNA hybridization quantification to study the influence of physico-chemical parameters on Legionella pneumophila survival in drinking water biofilms. Biofouling 2009, 25, 343-351.
47. Pang, C. M.; Liu, W. Biological filtration limits carbon availability and affects downstream biofilm formation and community structure. Appl. Environ. Microbiol. 2006, 72, 5702-5712.
48. Van der Kooij, D. K.; Veenendaal, H. R.; Scheffer, W. J. H. Biofilm formation and multiplication of Legionella in a model warm water system with pipes of copper, stainless steel and cross-linked polyethylene. Water Res. 2005, 39, 2789-2798.
49. Martinelli, F.; Caruso, A.; Moschini, L.; Turano, A.; Scarcella, C.; Speziani, F. A comparison of Legionella pneumophila occurrence in hot water tanks and instantaneous devices in domestic, nosocomial, and community environments. Curr. Microbiol. 2000, 41, 374-376.
50. Ciesielski, C. A.; Blaser, M. J.; Wang, W. L. Role of stagnation and obstruction of water flow in isolation of Legionella pneumophila from hospital plumbing. Appl. Environ. Microbiol. 1984, 48, 984-987.
51. Fisher-Hoch, S.; Bartlett, C. L.; Tobin, J. O.; Gillett, M. B.; Nelson, A. M.; Pritchard, J. E.; Smith, M. G.; Swann, R. A.; Talbot, J. M.; Thomas, J. A. Investigation and control of an outbreaks of Legionnaires' disease in a district general hospital. Lancet 1981, 1, 932-936.
52. Makin, T.; Pride, M. Venturi system could be major breakthrough. Health Estate 2010, 64, 27-33.
53. Storey, M. V.; Langmark, J.; Ashbolt, N. J.; Stenstrom, T. A. The fate of Legionellae within distribution pipe biofilms: Measurement of their persistence, inactivation and detachment. Water Sci. Technol. 2004, 49, 269-275.
54. Lehtola, M. J.; Torvinen, E.; Kusnetsov, J.; Pitkanen, T.; Maunula, L.; von Bonsdorff, C.; Martikainen, P. J.; Wilks, S. A.; Keevil, C. W.; Miettinen, I. T. Survival of Mycobacterium avium, Legionella pneumophila, Escherichia coli, and caliciviruses in drinking water-associated biofilms grown under high-shear turbulent flow. Appl. Environ. Microbiol. 2007, 73, 2854-2859.
55. Liu, Z.; Lin, Y. E.; Stout, J. E.; Hwang, C. C.; Vidic, R. D.; Yu, V. L. Effect of flow regimes on the presence of Legionella within the biofilm of a model plumbing system. J. Appl. Microbiol. 2006, 101, 437-442.
56. Fliermans, C. B.; Cherry, W. B.; Orrison, L. H.; Smith, S. J.; Tison, D. L.; Pope, D. H. Ecological distribution of Legionella pneumophila. Appl. Environ. Microbiol. 1981, 41, 9-16.
57. Stout, J. E.; Yu, V. L.; Best, M. G. Ecology of Legionella pneumophila within water distribution systems. Appl. Environ. Microbiol. 1985, 49, 221-228.
58. Tiaden, A.; Spirig, T.; Sahr, T.; Walti, M. A.; Boucke, K.; Buchrieser, C.; Hilbi, H. The autoinducer synthase LqsA and putative sensor kinase lqss regulate phagocyte interactions, extracellular filaments and a genomic island of Legionella pneumophila. Environ. Microbiol. 2010, 12, 1243-1259.
59. Kessler, A.; Schell, U.; Sahr, T.; Tiaden, A.; Harrison, C.; Buchrieser, C.; Hilbi, H. The Legionella pneumophila orphan sensor kinase LqsT regulates competence and pathogen-host interactions as a component of the LAI-1 circuit. Environ. Microbiol. 2013, 15, 646-662.
60. Vandersmissen, L.; de Buck, E.; Saels, V.; Coil, D. A.; Anne, J. A Legionella pneumophila collagen-like protein encoded by a gene with a variable number of tandem repeats is involved in the adherence and invasion of host cells. FEMS Microbiol. Lett. 2010, 306, 168-176.
61. Duncan, C.; Prashar, A.; So, J.; Tang, P.; Low, D. E.; Terebiznik, M.; Guyard, C. 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. 2011, 6, 2168-2181.
62. Mallegol, J.; Duncan, C.; Prashar, A.; So, J.; Low, D. E.; Terebeznik, M.; Guyard, C. Essential roles and regulation of the Legionella pneumophila collagen-like adhesin during biofilm formation. PLoS One 2012, 7, e46462.
63. Stone, B. J.; Kwaik, Y. A. Expression of multiple pili by Legionella pneumophila: Identification and characterization of a type IV pilin gene and its role in adherence to mammalian and protozoan cells. Infect. Immun. 1998, 66, 1768-1775.
64. Lucas, C. E.; Brown, E.; Fields, B. S. Type IV Pili and Type II secretion play a limited role in Legionella pneumophila biofilm colonization and retention. Microbiology 2006, 152, 3569-3573.
65. De Buck, E.; Maes, L.; Meyen, E.; van Mellaert, L.; Geukens, N.; Anne, J.; Lammertyn, E. Legionella pneumophila Philadelphia-1 tatB and tatC affect intracellular replication and biofilm formation. Biochem. Biophys. Res. Commun. 2005, 331, 1413-1420.
66. Cianciotto, N. P. Iron acquisition by Legionella pneumophila. Biometals 2007, 20, 323-331.
67. Orsi, N. The antimicrobial activity of lactoferrin: Current status and perspectives. Biometals 2004, 17, 189-196.
68. Robey, M.; Cianciotto, N. P. Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect. Immun. 2002, 70, 5659-5669.
69. Tiaden, A.; Hilbi, H. A-hydroxyketone synthesis and sensing by Legionella and Vibrio. Sensors 2012, 12, 2899-2919.
70. Spirig, T.; Tiaden, A.; Kiefer, P.; Buchrieser, C.; Vorholt, J. A.; Hilbi, H. The Legionella autoinducer synthase LqsA produces an α-hydroxyketone signaling molecule. J. Biol. Chem. 2008, 283, 18113-18123.
71. Tiaden, A.; Spirig, T.; Hilbi, H. Bacterial gene regulation by α-hydroxyketone signaling. Trends Microbiol. 2010, 18, 288-297.
72. Tiaden, A.; Spirig, T.; Carranza, P.; Bruggemann, H.; Riedel, K.; Eberl, L.; Buchrieser, C.; Hilbi, H. Synergistic contribution of the Legionella pneumophila Lqs genes to pathogen-host interactions. J. Bacteriol. 2008, 190, 7532-7547.
73. McDonough, K. A.; Rodriguez, A. The myriad roles of cyclic AMP in microbial pathogens: From signal to sword. Nat. Rev. Microbiol. 2011, 10, 27-38.
74. Levi, A.; Folcher, M.; Jenal, U.; Shuman, H. A. Cyclic diguanylate signaling proteins control intracellular growth of Legionella pneumophila. mBio 2011, 2, e00316-10.
75. Carlson, H. K.; Vance, R. E.; Marletta, M. A. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Mol. Microbiol. 2010, 77, 930-942.
76. Hammer, B. K.; Swanson, M. S. Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 1999, 33, 721-731.
77. Bachman, M. A.; Swanson, M. S. RpoS co-operates with other factors to induce Legionella pneumophila virulence in the stationary phase. Mol. Microbiol. 2001, 40, 1201-1214.
78. Tiaden, A.; Spirig, T.; Weber, S. S.; Bruggemann, H.; Bosshard, R.; Buchrieser, C.; Hilbi, H. The Legionella pneumophila response regulator LqsR promotes host cell interactions as an element of the virulence regulatory network controlled by RpoS and LetA. Cell. Microbiol. 2007, 9, 2903-2920.
79. Hammer, B. K.; Tateda, E. S.; Swanson, M. S. A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol. Microbiol. 2002, 44, 107-118.
80. Molofsky, A. B.; Swanson, M. S. Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol. Microbiol. 2003, 50, 445-461.
81. Piao, Z.; Sze, C. C.; Barysheva, O.; Iida, K.; Yoshida, S. Temperature-regulated formation of mycelial mat-like biofilms by Legionella pneumophila. Appl. Environ. Microbiol. 2006, 72, 1613-1622.
82. Konishi, T.; Yamashiro, T.; Koide, M.; Nishizono, A. Influence of temperature on growth of Legionella pneumophila biofilm determined by precise temperature gradient incubator. J. Biosci. Bioeng. 2006, 101, 478-484.
83. Justice, S. S.; Hunstad, D. A.; Cegelski, L.; Hultgren, S. J. Morphological plasticity as a bacterial survival strategy. Nat. Rev. Microbiol. 2008, 6, 162-168.
84. Prashar, A.; Bhatia, S.; Tabatabaeiyazdi, Z.; Duncan, C.; Garduno, R. A.; Tang, P.; Low, D. E.; Guyard, C.; Terebiznik, M. R. Mechanism of invasion of lung epithelial cells by filamentous Legionella pneumophila. Cell. Microbiol. 2012, 14, 1632-1655.
85. Liles, M. R.; Viswanathan, V. K.; Cianciotto, N. P. Identification and temperature regulation of Legionella pneumophila genes involved in type IV pilus biogenesis and type II protein secretion. Infect. Immun. 1998, 66, 1776-1782.
86. Messi, P.; Anacarso, I.; Bargellini, A.; Bondi, M.; Marchesi, I.; de Niederhausern, S.; Borella, P. Ecological behaviour of three serogroups of Legionella pneumophila within a model plumbing system. Biofouling 2011, 27, 165.
87. Tison, D. L.; Pope, D. H.; Cherry, W. B.; Fliermans, C. B. Growth of Legionella pneumophila in association with blue-green algae (Cyanobacteria). Appl. Environ. Microbiol. 1980, 39, 456-459.
88. Wadowsky, R. M.; Yee, R. B. Satellite growth of Legionella pneumophila with an environmental isolate of Flavobacterium breve. Appl. Environ. Microbiol. 1983, 46, 1447-1449.
89. Wery, N.; Bru-Adan, V.; Minervini, C.; Delgenes, J.; Garrelly, L.; Godon, J. Dynamics of Legionella spp. and bacterial populations during the proliferation of L. pneumophila in a cooling tower facility. Appl. Environ. Microbiol. 2008, 74, 3030-3037.
90. Stewart, C. R.; Burnside, D. M.; Cianciotto, N. P. The surfactant of Legionella pneumophila is secreted in a TolC-dependent manner and is antagonistic toward other Legionella species. J. Bacteriol. 2011, 193, 5971-5984.
91. Stewart, C. R.; Muthye, V.; Cianciotto, N. P. Legionella pneumophila persists within biofilms formed by Klebsiella pneumoniae, Flavobacterium sp., and Pseudomonas fluorescens under dynamic flow conditions. PLoS One 2012, 7, e50560.
92. Kimura, S.; Tateda, K.; Ishii, Y.; Horikawa, M.; Miyairi, S.; Gotoh, N.; Ishiguro, M.; Yamaguchi, K. Pseudomonas aeruginosa las quorum sensing autoinducer suppresses growth and biofilm production in Legionella species. Microbiology 2009, 155, 1934-1939.
93. Declerck, P.; Behets, J.; Delaedt, Y.; Margineanu, A.; Lammertyn, E.; Ollevier, F. Impact of non-Legionella bacteria on the uptake and intracellular replication of Legionella pneumophila in Acanthamoeba castellanii and Naegleria lovaniensis. Microb. Ecol. 2005, 50, 536-549.
94. Emtiazi, F.; Schwartz, T.; Marten, S. M.; Krolla-Sidenstein, P.; Obst, U. Investigation of natural biofilms formed during the production of drinking water from surface water embankment filtration. Water Res. 2004, 38, 1197-1206.
95. Giao, M. S.; Wilks, S.; Azevedo, N. F.; Vieira, M. J.; Keevil, C. W. Incorporation of natural uncultivable Legionella pneumophila into potable water biofilms provides a protective niche against chlorination stress. Biofouling 2009, 25, 335-341.
96. Alleron, L.; Merlet, N.; Lacombe, C.; Frere, J. Long-term survival of Legionella pneumophila in the viable but nonculturable state after monochloramine treatment. Curr. Microbiol. 2008, 57, 497-502.
97. Raftery, T. D.; Lindler, H.; McNealy, T. L. Altered host cell-bacteria interaction due to nanoparticle interaction with a bacterial biofilm. Microb. Ecol. 2013, 65, 496-503.
98. Stojak, A. R.; Raftery, T.; Klaine, S. J.; McNealy, T. L. Morphological responses of Legionella pneumophila biofilm to nanoparticle exposure. Nanotoxicology 2011, 5, 730-742.
99. Rogers, J.; Dowsett, A. B.; Keevil, C. W. A paint incorporating silver to control mixed biofilms containing Legionella pneumophila. J. Ind. Microbiol. 1995, 15, 377-383.
100. Liu, Z.; Stout, J. E.; Boldin, M.; Rugh, J.; Diven, W. F.; Yu, V. L. Intermittent use of copper-silver ionization for Legionella control in water distribution systems: A potential option in buildings housing individuals at low risk of infection. Clin. Infect Dis. 1998, 26, 138-140.
101. Schwartz, T.; Hoffmann, S.; Obst, U. Formation of natural biofilms during chlorine dioxide and u. v. disinfection in a public drinking water distribution system. J. Appl. Microbiol. 2003, 95, 591-601.
102. Walker, J. T.; Mackerness, C. W.; Mallon, D.; Makin, T.; Williets, T.; Keevil, C. W. Control of Legionella pneumophila in a hospital water system by chlorine dioxide. J. Ind. Microbiol. 1995, 15, 384-390.
103. Pryor, M.; Springthorpe, S.; Riffard, S.; Brooks, T.; Huo, Y.; Davis, G.; Sattar, S. A. Investigation of opportunistic pathogens in municipal drinking water under different supply and treatment regimes. Water Sci. Technol. 2004, 50, 83-90.
104. Williams, M. M.; Braun-Howland, E. Growth of Escherichia coli in model distribution system biofilms exposed to hypochlorous acid or monochloramine. Appl. Environ. Microbiol. 2003, 69, 5463-5471.
105. Kusnetsov, J. M.; Keskitalo, P. J.; Ahonen, H. E.; Tulkki, A. I.; Miettinen, I. T.; Martikainen, P. J. Growth of Legionella and other heterotrophic bacteria in a circulating cooling water system exposed to ultraviolet irradiation. J. Appl. Microbiol. 1994, 77, 461-466.
106. Cargill, K. L.; Pyle, B. H.; Sauer, R. L.; McFeters, G. A. Effects of culture conditions and biofilm formation on the iodine susceptibility of Legionella pneumophila. Can. J. Microbiol. 1992, 38, 423-429.