Flexible survival strategies of Pseudomonas aeruginosa in biofilms result in increased fitness compared with Candida albicans

Molecular and Cellular Proteomics

Volumn 11, Issue 12, 2012, Pages 1652-1669

  Purschke, Frauke Gina ^a   Hiller, Ekkehard ^b   Trick, Iris ^b   Rupp, Steffen ^b  

^a UNIVERSITY OF STUTTGART   (Germany)

^b FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EXOTOXIN; FUNGAL PROTEIN; IRON; PYOVERDINE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BINDING AFFINITY; BIOFILM; CANDIDA ALBICANS; FUNGUS GROWTH; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROBIAL DIVERSITY; MICROFLORA; MORPHOLOGY; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; SCANNING ELECTRON MICROSCOPY; YEAST CELL;

ADP RIBOSE TRANSFERASES; BACTERIAL TOXINS; BIOFILMS; CANDIDA ALBICANS; COLONY COUNT, MICROBIAL; EXOTOXINS; IRON; OLIGOPEPTIDES; PROTEOME; PSEUDOMONAS AERUGINOSA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); CANDIDA ALBICANS; FUNGI; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84870673207     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.017673     Document Type: Article

References (89)

1. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., and Lappin-Scott, H.M. (1995) Microbial biofilms. Annu. Rev. Microbiol. 49, 711-745
2. Miller, M. B., and Bassler, B. L. (2001) Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165-199 (Pubitemid 32978104)
3. De Sordi, L., and Muhlschlegel, F. A. (2009) Quorum sensing and fungal-bacterial interactions in Candida albicans: a communicative network regulating microbial coexistence and virulence. FEMS Yeast Res. 9, 990-999
4. Fux, C. A., Costerton, J. W., Stewart, P. S., and Stoodley, P. (2005) Survival strategies of infectious biofilms. Trends Microbiol. 13, 34-40 (Pubitemid 40082395)
5. Hermann, C., Hermann, J., Munzel, U., and Ruchel, R. (1999) Bacterial flora accompanying Candida yeasts in clinical specimens. Mycoses 42, 619-627 (Pubitemid 30053366)
6. Pierce, G. E. (2005) Pseudomonas aeruginosa, Candida albicans, and device-related nosocomial infections: implications, trends, and potential approaches for control. J. Ind. Microbiol. Biotechnol. 32, 309-318
7. Perlroth, J., Choi, B., and Spellberg, B. (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45, 321-346 (Pubitemid 46839802)
8. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322 (Pubitemid 29289651)
9. Kim, J., and Sudbery, P. (2011) Candida albicans, a major human fungal pathogen. J. Microbiol. 49, 171-177
10. Hornby, J. M., Jensen, E. C., Lisec, A. D., Tasto, J. J., Jahnke, B., Shoemaker, R., Dussault, P., and Nickerson, K. W. (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67, 2982-2992 (Pubitemid 33644762)
11. Ramage, G., VandeWalle, K., López-Ribot, J. L., and Wickes, B. L. (2002) The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol. Lett. 214, 95-100 (Pubitemid 35245528)
12. Hogan, D. A. (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot. Cell 5, 613-619
13. Martinez-Gomariz, M., Perumal, P., Mekala, S., Nombela, C., Chaffin, W. L., and Gil, C. (2009) Proteomic analysis of cytoplasmic and surface proteins from yeast cells, hyphae, and biofilms of Candida albicans. Proteomics 9, 2230-2252
14. Thomas, D. P., Bachmann, S. P., and Lopez-Ribot, J. L. (2006) Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics 6, 5795-5804 (Pubitemid 44764016)
15. Garcia-Sanchez, S., Aubert, S., Iraqui, I., Janbon, G., Ghigo, J. M., and d'Enfert, C. (2004) Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 3, 536-545 (Pubitemid 38497991)
16. Murillo, L. A., Newport, G., Lan, C. Y., Habelitz, S., Dungan, J., and Agabian, N. M. (2005) Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot. Cell 4, 1562-1573 (Pubitemid 41339111)
17. Yeater, K. M., Chandra, J., Cheng, G., Mukherjee, P. K., Zhao, X., Rodriguez- Zas, S. L., Kwast, K. E., Ghannoum, M. A., and Hoyer, L. L. (2007) Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 153, 2373-2385 (Pubitemid 47262027)
18. Enjalbert, B., and Whiteway, M. (2005) Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot. Cell 4, 1203-1210 (Pubitemid 41004133)
19. Cao, Y. Y., Cao, Y. B., Xu, Z., Ying, K., Li, Y., Xie, Y., Zhu, Z. Y., Chen, W. S., and Jiang, Y. Y. (2005) cDNA microarray analysis of differential gene expression in Candida albicans biofilm exposed to farnesol. Antimicrob. Agents Chemother. 49, 584-589 (Pubitemid 40175666)
20. Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., and Greenberg, E. P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298 (Pubitemid 28178075)
21. de Kievit, T. R. (2009) Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11, 279-288
22. Pesci, E. C., Milbank, J. B., Pearson, J. P., McKnight, S., Kende, A. S., Greenberg, E. P., and Iglewski, B. H. (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 96, 11229-11234 (Pubitemid 29487363)
23. Diggle, S. P., Matthijs, S., Wright, V. J., Fletcher, M. P., Chhabra, S. R., Lamont, I. L., Kong, X., Hider, R. C., Cornelis, P., Camara, M., and Williams, P. (2007) The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem. Biol. 14, 87-96 (Pubitemid 46138049)
24. Bredenbruch, F., Geffers, R., Nimtz, M., Buer, J., and Haussler, S. (2006) The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ. Microbiol. 8, 1318-1329 (Pubitemid 44025327)
25. 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
26. Banin, E., Vasil, M. L., and Greenberg, E. P. (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. U.S.A. 102, 11076-11081 (Pubitemid 41105995)
27. Sutak, R., Lesuisse, E., Tachezy, J., and Richardson, D.R. (2008) Crusade for iron: iron uptake in unicellular eukaryotes and its significance for virulence. Trends Microbiol. 16, 261-268
28. Schalk, I. J. (2008) Metal trafficking via siderophores in Gram-negative bacteria: specificities and characteristics of the pyoverdine pathway. J. Inorg. Biochem. 102, 1159-1169
29. Shirtliff, M. E., Peters, B. M., and Jabra-Rizk, M. A. (2009) Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol. Lett. 299, 1-8
30. Hogan, D. A., and Kolter, R. (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296, 2229-2232 (Pubitemid 34680309)
31. Bandara, H. M., Yau, J. Y., Watt, R. M., Jin, L. J., and Samaranayake, L. P. (2010) Pseudomonas aeruginosa inhibits in-vitro Candida biofilm development. BMC Microbiol. 10, 125
32. Hogan, D. A., Vik, A., and Kolter, R. (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol. 54, 1212-1223 (Pubitemid 39578266)
33. Holcombe, L. J., McAlester, G., Munro, C. A., Enjalbert, B., Brown, A. J., Gow, N. A., Ding, C., Butler, G., O'Gara, F., and Morrissey, J. P. (2010) Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans. Microbiology 156, 1476-1486
34. McAlester, G., O'Gara, F., and Morrissey, J. P. (2008) Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans. J. Med. Microbiol. 57, 563-569 (Pubitemid 351632902)
35. Cugini, C., Calfee, M. W., Farrow, J. M., 3rd, Morales, D. K., Pesci, E. C., and Hogan, D. A. (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol. Microbiol. 65, 896-906 (Pubitemid 47221077)
36. Kerr, J. R., Taylor, G. W., Rutman, A., Hoiby, N., Cole, P. J., and Wilson, R. (1999) Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. J. Clin. Pathol. 52, 385-387 (Pubitemid 29200034)
37. 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
38. Morales, D. K., Jacobs, N. J., Rajamani, S., Krishnamurthy, M., Cubillos-Ruiz, J. R., and Hogan, D. A. (2010) Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol. Microbiol. 78, 1379-1392
39. Gillum, A. M., Tsay, E. Y., and Kirsch, D. R. (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198, 179-182 (Pubitemid 15180998)
40. Holloway, B. W. (1955) Genetic recombination in Pseudomonas aeruginosa. J. Gen. Microbiol. 13, 572-581
41. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
42. Winsor, G. L., Van Rossum, T., Lo, R., Khaira, B., Whiteside, M. D., Hancock, R. E., and Brinkman, F. S. (2009) Pseudomonas Genome Database: facilitating user-friendly, comprehensive comparisons of microbial genomes. Nucleic Acids Res. 37, D483-D488
43. Liu, H., Sadygov, R. G., and Yates, J. R., 3rd (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201 (Pubitemid 38943698)
44. Saeed, A. I., Bhagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., Li, J., Thiagarajan, M., White, J. A., and Quackenbush, J. (2006) TM4 microarray software suite. Methods Enzymol. 411, 134-193
45. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378 (Pubitemid 36184095)
46. Hiller, E., Heine, S., Brunner, H., and Rupp, S. (2007) Candida albicans Sun41p, a putative glycosidase, is involved in morphogenesis, cell wall biogenesis, and biofilm formation. Eukaryot. Cell 6, 2056-2065 (Pubitemid 350221274)
47. Sheth, C. C., Hall, R., Lewis, L., Brown, A. J., Odds, F. C., Erwig, L. P., and Gow, N. A. (2011) Glycosylation status of the C. albicans cell wall affects the efficiency of neutrophil phagocytosis and killing but not cytokine signaling. Med. Mycol. 49, 513-524
48. Silverman, R. J., Nobbs, A. H., Vickerman, M. M., Barbour, M. E., and Jenkinson, H. F. (2010) Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect. Immun. 78, 4644-4652
49. 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
50. De Kievit, T. R., Gillis, R., Marx, S., Brown, C., and Iglewski, B. H. (2001) Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67, 1865-1873 (Pubitemid 33644961)
51. Hawser, S. P., and Douglas, L. J. (1994) Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect. Immun. 62, 915-921 (Pubitemid 24065575)
52. Blankenship, J. R., and Mitchell, A. P. (2006) How to build a biofilm: a fungal perspective. Curr. Opin. Microbiol. 9, 588-594 (Pubitemid 44791986)
53. Kendziorski, C., Irizarry, R. A., Chen, K. S., Haag, J. D., and Gould, M. N. (2005) On the utility of pooling biological samples in microarray experiments. Proc. Natl. Acad. Sci. U.S.A. 102, 4252-4257 (Pubitemid 40397098)
54. Karp, N. A., Spencer, M., Lindsay, H., O'Dell, K., and Lilley, K. S. (2005) Impact of replicate types on proteomic expression analysis. J. Proteome Res. 4, 1867-1871 (Pubitemid 41464817)
55. Booy, A., Lewis-Torpey, K., and Hunter, C. (2010) Effects of intelligent data acquisition and fast laser speed on analysis of complex protein digests. AB SCIEX. Technical Note, 0921810-01
56. Lewenza, S., Gardy, J. L., Brinkman, F. S., and Hancock, R. E. (2005) Genome-wide identification of Pseudomonas aeruginosa exported proteins using a consensus computational strategy combined with a laboratory-based PhoA fusion screen. Genome Res. 15, 321-329 (Pubitemid 40309397)
57. Nouwens, A. S., Willcox, M. D., Walsh, B. J., and Cordwell, S. J. (2002) Proteomic comparison of membrane and extracellular proteins from invasive (PAO1) and cytotoxic (6206) strains of. Pseudomonas aeruginosa. Proteomics 2, 1325-1346
58. Henderson, B., and Martin, A. (2011) Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect. Immun. 79, 3476-3491
59. Michel-Briand, Y., and Baysse, C. (2002) The pyocins of Pseudomonas aeruginosa. Biochimie (Paris) 84, 499-510 (Pubitemid 35350881)
60. Lee, S. A., Wormsley, S., Kamoun, S., Lee, A. F. S., Joiner, K., and Wong, B. (2003) An analysis of the Candida albicans genome database for soluble secreted proteins using computer-based prediction algorithms. Yeast 20, 595-610 (Pubitemid 36603567)
61. De Groot, P. W., Hellingwerf, K. J., and Klis, F. M. (2003) Genome-wide identification of fungal GPI proteins. Yeast 20, 781-796 (Pubitemid 36850044)
62. Urban, C., Xiong, X., Sohn, K., Schroppel, K., Brunner, H., and Rupp, S. (2005) The moonlighting protein Tsa1p is implicated in oxidative stress response and in cell wall biogenesis in Candida albicans. Mol. Microbiol. 57, 1318-1341 (Pubitemid 41176526)
63. Sorgo, A. G., Heilmann, C. J., Dekker, H. L., Brul, S., de Koster, C. G., and Klis, F. M. (2010) Mass spectrometric analysis of the secretome of Candida albicans. Yeast 27, 661-672
64. Lamont, I. L., Beare, P. A., Ochsner, U., Vasil, A. I., and Vasil, M. L. (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 99, 7072-7077 (Pubitemid 34526257)
65. Görisch, H. (2003) The ethanol oxidation system and its regulation in Pseudomonas aeruginosa. Biochim. Biophys. Acta 1647, 98-102
66. Visca, P., Colotti, G., Serino, L., Verzili, D., Orsi, N., and Chiancone, E. (1992) Metal regulation of siderophore synthesis in Pseudomonas aeruginosa and functional effects of siderophore-metal complexes. Appl. Environ. Microbiol. 58, 2886-2893
67. Wendenbaum, S., Demange, P., Dell, A., Meyer, J. M., and Abdallah, M. A. (1983) The structure of pyoverdine Pa, the siderophore of Pseudomonas aeruginosa. Tetrahedron Lett. 24, 4877-4880
68. El-Azizi, M. A., Starks, S. E., and Khardori, N. (2004) Interactions of Candida albicans with other Candida spp., and bacteria in the biofilms. J. Appl. Microbiol. 96, 1067-1073 (Pubitemid 38582153)
69. Klotz, S. A., Gaur, N. K., De Armond, R., Sheppard, D., Khardori, N., Edwards, J. E., Jr., Lipke, P. N., and El-Azizi, M. (2007) Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Med. Mycol. 45, 363-370 (Pubitemid 46839806)
70. Nailis, H., Vandenbroucke, R., Tilleman, K., Deforce, D., Nelis, H., and Coenye, T. (2009) Monitoring ALS1 and ALS3 gene expression during in vitro Candida albicans biofilm formation under continuous flow conditions. Mycopathologia 167, 9-17
71. O'Toole, G. A., and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295-304 (Pubitemid 28480181)
72. Whiteley, M., Bangera, M. G., Bumgarner, R. E., Parsek, M. R., Teitzel, G. M., Lory, S., and Greenberg, E. P. (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860-864 (Pubitemid 33026855)
73. Webb, J. S., Thompson, L. S., James, S., Charlton, T., Tolker-Nielsen, T., Koch, B., Givskov, M., and Kjelleberg, S. (2003) Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185, 4585-4592 (Pubitemid 36890507)
74. Rice, S. A., Tan, C. H., Mikkelsen, P. J., Kung, V., Woo, J., Tay, M., Hauser, A., McDougald, D., Webb, J. S., and Kjelleberg, S. (2009) The biofilm life-cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J. 3, 271-282
75. Rice, K. C., and Bayles, K. W. (2008) Molecular control of bacterial death and lysis. Microbiol. Mol. Biol. Rev. 72, 85-109 (Pubitemid 351398056)
76. Waite, R. D., and Curtis, M. A. (2009) Pseudomonas aeruginosa PAO1 pyocin production affects population dynamics within mixed-culture biofilms. J. Bacteriol. 191, 1349-1354
77. Goodwin, K., Levin, R. E., and Doggett, R. G. (1972) Autosensitivity of Pseudomonas aeruginosa to its own pyocin. Infect. Immun. 6, 889-892
78. Chang, W., Small, D. A., Toghrol, F., and Bentley, W. E. (2005) Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genomics 6, 115
79. Cox, C. D., and Adams, P. (1985) Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect. Immun. 48, 130-138 (Pubitemid 15111165)
80. Poole, K., Neshat, S., Krebes, K., and Heinrichs, D. E. (1993) Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J. Bacteriol. 175, 4597-4604 (Pubitemid 23220240)
81. Cox, C. D., and Graham, R. (1979) Isolation of an iron-binding compound from Pseudomonas aeruginosa. J. Bacteriol. 137, 357-364 (Pubitemid 9097580)
82. Letoffe, S., Redeker, V., and Wandersman, C. (1998) Isolation and characterization of an extracellular haem-binding protein from Pseudomonas aeruginosa that shares function and sequence similarities with the Serratia marcescens HasA haemophore. Mol. Microbiol. 28, 1223-1234 (Pubitemid 28293545)
83. Mao, F., Dam, P., Chou, J., Olman, V., and Xu, Y. (2009) DOOR: a database for prokaryotic operons. Nucleic Acids Res. 37, D459-D463
84. Winsor, G. L., Lam, D. K., Fleming, L., Lo, R., Whiteside, M. D., Yu, N. Y., Hancock, R. E., and Brinkman, F. S. (2011) Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39, D596-D600
85. Ghysels, B., Ochsner, U., Mollman, U., Heinisch, L., Vasil, M., Cornelis, P., and Matthijs, S. (2005) The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol. Lett. 246, 167-174 (Pubitemid 40724427)
86. Heymann, P., Gerads, M., Schaller, M., Dromer, F., Winkelmann, G., and Ernst, J. F. (2002) The siderophore iron transporter of Candida albicans (Sit1p/Arn1p) mediates uptake of ferrichrome-type siderophores and is required for epithelial invasion. Infect. Immun. 70, 5246-5255
87. Knight, S. A., and Dancis, A. (2006) Reduction of 2,3-bis(2-methoxy-4- nitro-5-sulfophenyl)-2H-tetrazolium-5-carboxanilide inner salt (XTT) is dependent on CaFRE10 ferric reductase for Candida albicans grown in unbuffered media. Microbiology 152, 2301-2308 (Pubitemid 44219639)
88. Weissman, Z., and Kornitzer, D. (2004) A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization. Mol. Microbiol. 53, 1209-1220 (Pubitemid 39120440)
89. Jagmann, N., Brachvogel, H. P., and Philipp, B. (2010) Parasitic growth of Pseudomonas aeruginosa in co-culture with the chitinolytic bacterium Aeromonas hydrophila. Environ. Microbiol. 12, 1787-1802