Parasitic growth of Pseudomonas aeruginosa in co-culture with the chitinolytic bacterium Aeromonas hydrophila

Environmental Microbiology

Volumn 12, Issue 6, 2010, Pages 1787-1802

  Jagmann, Nina ^a   Brachvogel, Hans Philipp ^a   Philipp, Bodo ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; ACONITATE HYDRATASE; CHITIN; PHENAZINE DERIVATIVE; PYOCYANINE; QUINOLONE DERIVATIVE;

AEROMONAS HYDROPHILA; ARTICLE; CHEMISTRY; COCULTURE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; METABOLISM; PATHOGENICITY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION;

ACETATES; ACONITATE HYDRATASE; AEROMONAS HYDROPHILA; CHITIN; COCULTURE TECHNIQUES; HOST-PARASITE INTERACTIONS; PHENAZINES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PYOCYANINE; QUINOLONES;

EID: 77957934751     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02271.x     Document Type: Article

References (78)

1. Aendekerk, S., Diggle, S.P., Song, Z., Høiby, N., Cornelis, P., Williams, P., and Cámara, M. (2005) The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151: 1113-1125
2. van Asperen, I.A., de Rover, C.M., Schijven, J.F., Oetomo, S.B., Schellekens, J.F., van Leeuwen, N.J., et al. (1995) Risk of otitis externa after swimming in recreational fresh water lakes containing Pseudomonas aeruginosa. BMJ 311: 1407-1410.
3. Baron, S.S., and Rowe, J.J. (1981) Antibiotic action of pyocyanin. Antimicrob Agents Chemother 20: 814-820.
4. Bazire, A., Dheilly, A., Diab, F., Morin, D., Jebbar, M., Haras, D., and Dufour, A. (2005) Osmotic stress and phosphate limitation alter production of cell-to-cell signal molecules and rhamnolipid biosurfactant by Pseudomonas aeruginosa. FEMS Microbiol Lett 253: 125-131.
5. Beatson, S.A., Whitchurch, C.B., Semmler, A.B.T., and Mattick, J.S. (2002) Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J Bacteriol 184: 3598-3604.
6. Biswas, L., Biswas, R., Schlag, M., Bertram, R., and Götz, F. (2009) Small-colony variant selection as a survival strategy for Staphylococcus aureus in the presence of Pseudomonas aeruginosa. Appl Environ Microbiol 75: 6910-6912.
7. Bollinger, N., Hassett, D.J., Iglewski, B.H., Costerton, J.W., and McDermott, T.R. (2001) Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J Bacteriol 183: 1990-1996.
8. Chayabutra, C., Wu, J., and Ju, L.K. (2001) Rhamnolipid production by Pseudomonas aeruginosa under denitrification: effects of limiting nutrients and carbon substrates. Biotechnol Bioeng 72: 25-33.
9. Chróst, R.J., and Rai, H. (1993) Ectoenzyme activity and bacterial secondary production in nutrient-impoverished and nutrient-enriched freshwater mesocosms. Microb Ecol 25: 131-150.
10. Clarke, P.H. (1982) The metabolic versatility of pseudomonads. Antonie Van Leeuwenhoek 48: 105-130.
11. Cox, C.D., and Adams, P. (1985) Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect Immun 48: 130-138.
12. van Delden, C., Comte, R., and Bally, A.M. (2001) Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J Bacteriol 183: 5376-5384.
13. Duan, K., and Surette, M.G. (2007) Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorumsensing systems. J Bacteriol 189: 4827-4836.
14. Dubern, J.-F., and Diggle, S.P. (2008) Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol Biosyst 4: 882-888.
15. Favero, M.S., Carson, L.A., Bond, W.W., and Petersen, N.J. (1971) Pseudomonas aeruginosa: growth in distilled water from hospitals. Science 173: 836-838.
16. Fletcher, M.P., Diggle, S.P., Cámara, M., and Williams, P. (2007) Biosensor-based assays for PQS, HHQ and related 2-alkyl-4-quinolone quorum sensing signal molecules. Nat Protoc 2: 1254-1262.
17. Folders, J., Tommassen, J., van Loon, L.C., and Bitter, W. (2000) Identification of a chitin-binding protein secreted by Pseudomonas aeruginosa. J Bacteriol 182: 1257-1263.
18. Folders, J., Algra, J., Roelofs, M.S., van Loon, L.C., Tommassen, J., and Bitter, W. (2001) Characterization of Pseudomonas aeruginosa chitinase, a gradually secreted protein. J Bacteriol 183: 7044-7052.
19. Fuqua, C., Parsek, M.R., and Greenberg, E.P. (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35: 439-468.
20. Gallagher, L.A., McKnight, S.L., Kuznetsova, M.S., Pesci, E.C., and Manoil, C. (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184: 6472-6480.
21. Ghysels, B., Dieu, B.T.M., Beatson, S.A., Pirnay, J.-P., Ochsner, U.A., Vasil, M.L., and Cornelis, P. (2004) FpvB, an alternative type I ferripyoverdine receptor of Pseudomonas aeruginosa. Microbiology 150: 1671-1680.
22. Gibson, J., Sood, A., and Hogan, D.A. (2009) Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl Environ Microbiol 75: 504-513.
23. Gooday, G.W. (1990) The ecology of chitin degradation. Adv Microb Ecol 11: 387-430.
24. von Graevenitz, A. (1987) Research on Aeromonas and Plesiomonas. Experentia 43: 348-358.
25. Haba, E., Pinazo, A., Jauregui, O., Espuny, M.J., Infante, M.R., and Manresa, A. (2003) Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotechnol Bioeng 81: 316-322.
26. Hardalo, C., and Edberg, S.C. (1997) Pseudomonas aeruginosa: assessment of risk from drinking water. Crit Rev Microbiol 23: 47-75.
27. Haruta, S., Kato, S., Yamamoto, K., and Igarashi, Y. (2009) Intertwined interspecies relationships: approaches to untangle the microbial network. Environ Microbiol 11: 2963-2969
28. Hassan, H.M., and Fridovich, I. (1980) Mechanism of the antibiotic action pyocyanine. J Bacteriol 141: 156-163.
29. Hassett, D.J., Charniga, L., Bean, K., Ohman, D.E., and Cohen, M.S. (1992) Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect Immun 60: 328-336.
30. Hausladen, A., and Fridovich, I. (1996) Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Methods Enzymol 269: 37-41.
31. Hibbing, M.E., Fuqua, C., Parsek, M.R., and Peterson, S.B. (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8: 15-25.
32. Hoben, H.J., and Somasegaran, P. (1982) Comparison of the pour, spread, and drop plate methods for enumeration of Rhizobium spp. in inoculants made from presterilized peat. Appl Environ Microbiol 44: 1246-1247.
33. Hoffman, L.R., Déziel, E., D'Argenio, D.A., Lépine, F., Emerson, J., McNamara, S., et al. (2006) Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 103: 19890-19895.
34. Hogan, D.A., and Kolter, R. (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 2229-2232.
35. Imlay, J.A. (2003) Pathways of oxidative damage. Annu Rev Microbiol 57: 395-418.
36. Janda, J.M. (1985) Biochemical and exoenzymatic properties of Aeromonas species. Diagn Microbiol Infect Dis 3: 223- 232.
37. Jensen, V., Löns, D., Zaoui, C., Bredenbruch, F., Meissner, A., Dieterich, G., et al. (2006) RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J Bacteriol 188: 8601-8606.
38. Kay, E., Humair, B., Dénervaud, V., Riedel, K., Spahr, S., Eberl, L., et al. (2006) Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188: 6026-6033.
39. Keyhani, N.O., and Roseman, S. (1999) Physiological aspects of chitin catabolism in marine bacteria. Biochim Biophys Acta 1473: 108-122.
40. Kim, E.-J.,Wang,W., Deckwer,W.-D., and Zeng, A.-P. (2005) Expression of the quorum-sensing regulatory protein LasR is strongly affected by iron and oxygen concentrations in cultures of Pseudomonas aeruginosa irrespective of cell density. Microbiology 151: 1127-1138.
41. Klebensberger, J., Rui, O., Fritz, E., Schink, B., and Philipp, B. (2006) Cell aggregation of Pseudomonas aeruginosa strain PAO1 as an energy-dependent stress response during growth with sodium dodecyl sulfate. Arch Microbiol 185: 417-427.
42. Klebensberger, J., Lautenschlager, K., Bressler, D., Wingender, J., and Philipp, B. (2007) Detergent-induced cell aggregation in subpopulations of Pseudomonas aeruginosa as a preadaptive survival strategy. Environ Microbiol 9: 2247-2259.
43. van der Kooij, D., Oranje, J.P., and Hijnen, W.A. (1982) Growth of Pseudomonas aeruginosa in tap water in relation to utilization of substrates at concentrations of a few micrograms per liter. Appl Environ Microbiol 44: 1086- 1095.
44. Lan, X., Zhang, X., Kodaira, R., Zhou, Z., and Shimosaka, M. (2008) Gene cloning, expression, and characterization of a second beta-N-acetylglucosaminidase from the chitinolytic bacterium Aeromonas hydrophila strain SUWA-9. Biosci Biotechnol Biochem 72: 492-498.
45. Lau, G.W., Hassett, D.J., Ran, H., and Kong, F. (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10: 599-606.
46. Li, Q., Xiao, X., and Wang, F. (2007) Screening of genes involved in chitinase production in Aeromonas caviae CB101 via transposon mutagenesis. J Appl Microbiol 102: 640-649.
47. Lynch, M.J., Swift, S., Kirke, D.F., Keevil, C.W., Dodd, C.E.R., and Williams, P. (2002) The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ Microbiol 4: 18-28.
48. Lynd, L.R., Weimer, P.J., van Zyl, W.H., and Pretorius, I.S. (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66: 506-577.
49. Manos, J., Arthur, J., Rose, B., Bell, S., Tingpej, P., Hu, H., et al. (2009) Gene expression characteristics of a cystic fibrosis epidemic strain of Pseudomonas aeruginosa during biofilm and planktonic growth. FEMS Microbiol Lett 292: 107-114.
50. Mena, K.D., and Gerba, C.P. (2009) Risk assessment of Pseudomonas aeruginosa in water. Rev Environ Contam Toxicol 201: 71-115.
51. Namdari, H., and Cabelli, V.J. (1990) Glucose-mediated catabolite repression of the tricarboxylic acid cycle as an explanation for increased acetic acid production in suicidal Aeromonas strains. J Bacteriol 172: 4721-4724.
52. Norman, R.S., Moeller, P., McDonald, T.J., and Morris, P.J. (2004) Effect of pyocyanin on a crude-oil-degrading microbial community. Appl Environ Microbiol 70: 4004-4011.
53. Nouwens, A.S., Beatson, S.A., Whitchurch, C.B.,Walsh, B.J., Schweizer, H.P., Mattick, J.S., and Cordwell, S.J. (2003) Proteome analysis of extracellular proteins regulated by the las and rhl quorum sensing systems in Pseudomonas aeruginosa PAO1. Microbiology 149: 1311-1322.
54. Ohman, D.E., Cryz, S.J., and Iglewski, B.H. (1980) Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase. J Bacteriol 142: 836-842.
55. O'Malley, Y.Q., Abdalla, M.Y., McCormick, M.L., Reszka, K.J., Denning, G.M., and Britigan, B.E. (2003) Subcellular localization of Pseudomonas pyocyanin cytotoxicity in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 284: L420-L430.
56. Philipp, B., and Schink, B. (1998) Evidence of two oxidative reaction steps initiating anaerobic degradation of resorcinol (1,3-dihydroxybenzene) by the denitrifying bacterium Azoarcus anaerobius. J Bacteriol 180: 3644-3649.
57. Pinzon, N.M., and Ju, L.-K. (2009) Analysis of rhamnolipid biosurfactants by methylene blue complexation. Appl Microbiol Biotechnol 82: 975-981.
58. Pruzzo, C., Vezzulli, L., and Colwell, R.R. (2008) Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10: 1400-1410.
59. Ramana, K.V., and Karanth, N.G. (1989) Factors affecting biosurfactant production using Pseudomonas aeruginosa CFTR-6 under submerged conditions. J Chem Technol Biotechnol 45: 249-257.
60. Reichenbach, H. (2006) The genus Lysobacter. In The Prokaryotes. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E. (eds). New York, NY, USA: Springer, pp. 939-957.
61. Römling, U., Wingender, J., Müller, H., and Tümmler, B. (1994) A major Pseudomonas aeruginosa clone common to patients and aquatic habitats. Appl Environ Microbiol 60
62. Ryan, R.P., and Dow, J.M. (2008) Diffusible signals and interspecies communication in bacteria. Microbiology 154: 1845-1858.
63. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1: 784-791.
64. Straight, P.D., and Kolter, R. (2009) Interspecies chemical communication in bacterial development. Annu Rev Microbiol 63: 99-118.
65. Styp von Rekowski, K., Hempel, M., and Philipp, B. (2008) Quorum sensing by N-acylhomoserine lactones is not required for Aeromonas hydrophila during growth with organic particles in lake water microcosms. Arch Microbiol 189: 475-482.
66. Swift, S., Lynch, M.J., Fish, L., Kirke, D.F., Tomás, J.M., Stewart, G.S., and Williams, P. (1999) Quorum sensingdependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect Immun 67: 5192- 5199.
67. Unanue, M., Ayo, B., Agis, M., Slezak, D., Herndl, G.J., and Iriberri, J. (1999) Ectoenzymatic activity and uptake of monomers in marine bacterioplankton described by a biphasic kinetic model. Microb Ecol 37: 36-48.
68. Visca, P., Serino, L., and Orsi, N. (1992) Isolation and characterization of Pseudomonas aeruginosa mutants blocked in the synthesis of pyoverdin. J Bacteriol 174: 5727-5731.
69. Wagner, V.E., Bushnell, D., Passador, L., Brooks, A.I., and Iglewski, B.H. (2003) Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185: 2080-2095.
70. Whooley, M.A., and McLoughlin, A.J. (1983) The regulation of pyocyanin production in Pseudomonas aeruginosa. Eur J Appl Microbiol Biotechnol 15: 161-166.
71. Widdel, F., Kohring, G.W., and Mayer, F. (1983) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. III. Characterization of the Filamentous Gliding Desulfonema limicola gen. nov. sp. nov., and Desulfonema magnum sp. nov. Arch Microbiol 134: 286-294.
72. Williams, P., and Cámara, M. (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12: 182-191.
73. Windgassen, M., Urban, A., and Jaeger, K.E. (2000) Rapid gene inactivation in Pseudomonas aeruginosa. FEMS Microbiol Lett 193: 201-205.
74. Winson, M.K., Swift, S., Fish, L., Throup, J.P., Jørgensen, F., Chhabra, S.R., et al. (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163: 185-192.
75. Xiao, G., Déziel, E., He, J., Lépine, F., Lesic, B., Castonguay, M.-H., et al. (2006) MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62: 1689-1699.
76. Yates, E.A., Philipp, B., Buckley, C., Atkinson, S., Chhabra, S.R., Sockett, R.E., et al. (2002) N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70: 5635-5646.
77. Zaborin, A., Romanowski, K., Gerdes, S., Holbrook, C., Lepine, F., Long, J., et al. (2009) Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. Proc Natl Acad Sci USA 106: 6327-6332.
78. Zhu, X., Cai, J., Yang, J., and Su, Q. (2005) Determination of glucosamine in impure chitin samples by high-performance liquid chromatography. Carbohydr Res 340: 1732-1738.