Essential Roles and Regulation of the Legionella pneumophila Collagen-Like Adhesin during Biofilm Formation

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Mallegol, Julia ^a,b,c   Duncan, Carla ^a   Prashar, Akriti ^d   So, Jannice ^a,b   Low, Donald E ^a,b,c   Terebeznik, Mauricio ^d   Guyard, Cyril ^a,b,c  

^a PUBLIC HEALTH ONTARIO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; COLLAGEN; HOMOSERINE; LACTONE; LCL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BIOFILM; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GROWTH CURVE; LCL GENE; LEGIONELLA PNEUMOPHILA; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; QUORUM SENSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

4-BUTYROLACTONE; ADHESINS, BACTERIAL; AMINO ACID MOTIFS; BACTERIAL ADHESION; BIOFILMS; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; LEGIONELLA PNEUMOPHILA; PROTEIN STRUCTURE, TERTIARY; QUORUM SENSING; TANDEM REPEAT SEQUENCES;

LEGIONELLA PNEUMOPHILA;

EID: 84866982452     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046462     Document Type: Article

References (65)

1. Stout JE, Yu VL, (1997) Eradicating Legionella from hospital water. Jama 278: 1404-1405.
2. Benin AL, Benson RF, Besser RE, (2002) Trends in legionnaires disease, 1980-1998: declining mortality and new patterns of diagnosis. Clin Infect Dis 35: 1039-1046.
3. Bartram J, Chartier Y, Lee JV, Pond K, Surman-Lee S (2007) Legionella and the prevention of legionellosis. In: Organization WH, editor. Geneva: WHO Press. 1-276.
4. Fields BS, Benson RF, Besser RE, (2002) Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 15: 506-526.
5. Fliermans CB, Cherry WB, Orrison LH, Smith SJ, Tison DL, et al. (1981) Ecological distribution of Legionella pneumophila. Appl Environ Microbiol 41: 9-16.
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. Luck CP, Jacobs E, Roske I, Schroter-Bobsin U, Dumke R, et al. (2009) Legionella dresdenensis sp. nov. isolated from the river Elbe near Dresden in Germany. Int J Syst Evol Microbiol: Epub ahead of print.
8. Hilbi H, Jarraud S, Hartland E, Buchrieser C, (2010) Update on Legionnaires' disease: pathogenesis, epidemiology, detection and control. Mol Microbiol 76: 1-11.
9. Piao Z, Sze CC, Barysheva O, Iida K, Yoshida S, (2006) Temperature-regulated formation of mycelial mat-like biofilms by Legionella pneumophila. Appl Environ Microbiol 72: 1613-1622.
10. Vervaeren H, Temmerman R, Devos L, Boon N, Verstraete W, (2006) Introduction of a boost of Legionella pneumophila into a stagnant-water model by heat treatment. FEMS Microbiol Ecol 58: 583-592.
11. Murga R, Forster TS, Brown E, Pruckler JM, Fields BS, et al. (2001) Role of biofilms in the survival of Legionella pneumophila in a model potable-water system. Microbiology 147: 3121-3126.
12. 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 Res 41: 3159-3167.
13. Declerck P, Behets J, van Hoef V, Ollevier F, (2007) Replication of Legionella pneumophila in floating biofilms. Curr Microbiol 55: 435-440.
14. Flemming HC, Wingender J, (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
15. Dunne WM Jr, Pinckard JK, Hooper LV, (2002) Clinical microbiology in the year 2025. J Clin Microbiol 40: 3889-3893.
16. Cooper IR, Hanlon GW, (2010) Resistance of Legionella pneumophila serotype 1 biofilms to chlorine-based disinfection. J Hosp Infect 74: 152-159.
17. Hall-Stoodley L, Stoodley P, (2009) Evolving concepts in biofilm infections. Cell Microbiol 11: 1034-1043.
18. Hoiby N, Ciofu O, Bjarnsholt T, (2010) Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 5: 1663-1674.
19. Anderson GG, O'Toole GA, (2008) Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol 322: 85-105.
20. Richards JJ, Melander C, (2009) Controlling bacterial biofilms. Chembiochem 10: 2287-2294.
21. Ueda A, Attila C, Whiteley M, Wood TK, (2009) Uracil influences quorum sensing and biofilm formation in Pseudomonas aeruginosa and fluorouracil is an antagonist. Microb Biotechnol 2: 62-74.
22. Camilli A, Bassler BL, (2006) Bacterial small-molecule signaling pathways. Science 311: 1113-1116.
23. Bassler BL, (2002) Small talk. Cell-to-cell communication in bacteria. Cell 109: 421-424.
24. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL, (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303-314.
25. Henke JM, Bassler BL, (2004) Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186: 3794-3805.
26. Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, et al. (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450: 883-886.
27. Tiaden A, Spirig T, Weber SS, Bruggemann H, Bosshard R, et al. (2007) 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 9: 2903-2920.
28. Spirig T, Tiaden A, Kiefer P, Buchrieser C, Vorholt JA, et al. (2008) The Legionella autoinducer synthase LqsA produces an alpha-hydroxyketone signaling molecule. J Biol Chem 283: 18113-18123.
29. Kimura S, Tateda K, Ishii Y, Horikawa M, Miyairi S, et al. (2009) Pseudomonas aeruginosa Las quorum sensing autoinducer suppresses growth and biofilm production in Legionella species. Microbiology 155: 1934-1939.
30. O'Neill E, Pozzi C, Houston P, Humphreys H, Robinson DA, et al. (2008) A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol 190: 3835-3850.
31. Heilmann C, Niemann S, Sinha B, Herrmann M, Kehrel BE, et al. (2004) Staphylococcus aureus fibronectin-binding protein (FnBP)-mediated adherence to platelets, and aggregation of platelets induced by FnBPA but not by FnBPB. J Infect Dis 190: 321-329.
32. 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.
33. Vandersmissen L, De Buck E, Saels V, Coil DA, Anne J, (2010) 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 306: 168-176.
34. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
35. Towbin H, Staehelin T, Gordon J, (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76: 4350-4354.
36. Bijtenhoorn P, Mayerhofer H, Muller-Dieckmann J, Utpatel C, Schipper C, et al. (2011) A novel metagenomic short-chain dehydrogenase/reductase attenuates Pseudomonas aeruginosa biofilm formation and virulence on Caenorhabditis elegans. PLoS ONE 6: e26278.
37. Fishov I, Woldringh CL, (1999) Visualization of membrane domains in Escherichia coli. Mol Microbiol 32: 1166-1172.
38. Tchesnokova V, McVeigh AL, Kidd B, Yakovenko O, Thomas WE, et al. (2010) Shear-enhanced binding of intestinal colonization factor antigen I of enterotoxigenic Escherichia coli. Mol Microbiol 76: 489-502.
39. Stoodley P, Cargo R, Rupp CJ, Wilson S, Klapper I, (2002) Biofilm material properties as related to shear-induced deformation and detachment phenomena. J Ind Microbiol Biotechnol 29: 361-367.
40. 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.
41. Wood TK, (2009) Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ Microbiol 11: 1-15.
42. Hindre T, Bruggemann H, Buchrieser C, Hechard Y, (2008) Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. Microbiology 154: 30-41.
43. Carlson HK, Vance RE, Marletta MA (2010) H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Mol Microbiol.
44. Molofsky AB, Swanson MS, (2004) Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53: 29-40.
45. Byrne B, Swanson MS, (1998) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66: 3029-3034.
46. Pugsley AP, (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57: 50-108.
47. Lau HY, Ashbolt NJ, (2009) The role of biofilms and protozoa in Legionella pathogenesis: implications for drinking water. J Appl Microbiol 107: 368-378.
48. Declerck P, Behets J, Margineanu A, van Hoef V, De Keersmaecker B, et al. (2009) Replication of Legionella pneumophila in biofilms of water distribution pipes. Microbiol Res 164: 593-603.
49. De Buck E, Maes L, Meyen E, Van Mellaert L, Geukens N, et al. (2005) Legionella pneumophila Philadelphia-1 tatB and tatC affect intracellular replication and biofilm formation. Biochem Biophys Res Commun 331: 1413-1420.
50. DebRoy S, Dao J, Soderberg M, Rossier O, Cianciotto NP, (2006) Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc Natl Acad Sci U S A 103: 19146-19151.
51. Molofsky AB, Swanson MS, (2003) Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol Microbiol 50: 445-461.
52. Stoodley P, Sauer K, Davies DG, Costerton JW, (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56: 187-209.
53. Absalon C, Van Dellen K, Watnick PI, (2011) A communal bacterial adhesin anchors biofilm and bystander cells to surfaces. PLoS Pathog 7: e1002210.
54. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, et al. (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407: 762-764.
55. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, et al. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295-298.
56. Hentzer M, Eberl L, Nielsen J, Givskov M, (2003) Quorum sensing: a novel target for the treatment of biofilm infections. BioDrugs 17: 241-250.
57. Shrout JD, Nerenberg R, (2012) Monitoring bacterial twitter: does quorum sensing determine the behavior of water and wastewater treatment biofilms? Environ Sci Technol 46: 1995-2005.
58. Shiner EK, Rumbaugh KP, Williams SC, (2005) Inter-kingdom signaling: deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 29: 935-947.
59. Parsek MR, Greenberg EP, (2000) Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci U S A 97: 8789-8793.
60. Juhas M, Eberl L, Tummler B, (2005) Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7: 459-471.
61. Fuqua C, Greenberg EP, (2002) Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3: 685-695.
62. Henke JM, Bassler BL, (2004) Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186: 6902-6914.
63. Tiaden A, Spirig T, Sahr T, Walti MA, Boucke K, et al. (2010) The autoinducer synthase LqsA and putative sensor kinase LqsS regulate phagocyte interactions, extracellular filaments and a genomic island of Legionella pneumophila. Environ Microbiol 12: 1243-1259.
64. Tiaden A, Spirig T, Carranza P, Bruggemann H, Riedel K, et al. (2008) Synergistic contribution of the Legionella pneumophila lqs genes to pathogen-host interactions. J Bacteriol 190: 7532-7547.
65. Berger KH, Isberg RR, (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7: 7-19.