PA2663 (PpyR) increases biofilm formation in Pseudomonas aeruginosa PAO1 through the psl operon and stimulates virulence and quorum-sensing phenotypes

Applied Microbiology and Biotechnology

Volumn 78, Issue 2, 2008, Pages 293-307

  Attila, Can ^a   Ueda, Akihiro ^a   Wood, Thomas K ^a,b  

^a Texas AandM University   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Biofilm; Pseudomonas aeruginosa; psl operon; Pyoverdine

Indexed keywords

PYOVERDINE; SWIMMING MOTILITY; VIRULENCE FACTORS;

BACTERIA; GENE ENCODING; MICROBIOLOGY;

BIOFILMS;

ELASTASE; EXOPOLYSACCHARIDE; GALACTOSE; GLUCONIC ACID; GLUTAMIC ACID; MANNITOL; MANNOSE; MEMBRANE PROTEIN; PHTHALOYLGLUTAMIC ACID; PROTEIN PA2663; PYOVERDINE; UNCLASSIFIED DRUG;

BACTERIUM; BIOFILM; GENE; PHENOTYPE; POLYSACCHARIDE; VIRULENCE;

ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SYNTHESIS; GENE EXPRESSION; GENE MUTATION; NONHUMAN; OPERON; PHENOTYPE; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSPOSON; WILD TYPE;

BACTERIAL PROTEINS; BIOFILMS; BIOLOGICAL TRANSPORT; DNA TRANSPOSABLE ELEMENTS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; GLUCONATES; GLUTAMATES; LOCOMOTION; MANNITOL; METALLOENDOPEPTIDASES; MUTAGENESIS, INSERTIONAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OLIGOPEPTIDES; OPERON; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS AERUGINOSA; QUINOLONES; QUORUM SENSING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, MESSENGER; VIRULENCE;

ATTILA; POPULUS; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 38649101867     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-007-1308-y     Document Type: Article

References (62)

1. Attila C, Ueda, A, Cirillo, SLG, Cirillo, JD, Chen, W, Wood, TK (2008) Pseudomonas aeruginosa PAO1 virulence factors and poplar tree response in the rhizosphere. Microb Biotechnol 1:17-29
2. Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188:7344-7353
3. Breedveld MW, Zevenhuizen LPTM, Zehnder AJB (1991) Osmotically-regulated trehalose accumulation and cyclic β-(1,2)-glucan excretion by Rhizobium leguminosarum biovar trifolii TA-1. Arch Microbiol 156:501-506
4. Caiazza NC, O'Toole GA (2004) SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol 186:4476-4485
5. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:3603-3612
6. Campisano A, Schroeder C, Schemionek M, Overhage J, Rehm BH (2006) PslD is a secreted protein required for biofilm formation by Pseudomonas aeruginosa. Appl Environ Microbiol 72:3066-3068
7. Cho EJ, Oh JY, Chang HY, Yun JW (2006) Production of exopolysaccharides by submerged mycelial culture of a mushroom Tremella fuciformis. J Biotechnol 127:129-140
8. Claassen PA, Kortstee GJ, Oosterveld-van Vliet WM, van Neerven AR (1986) Colonial heterogeneity of Thiobacillus versutus. J Bacteriol 168:791-794
9. Costerton B (2004) Microbial ecology comes of age and joins the general ecology community. Proc Natl Acad Sci U S A 101:16983-16984
10. q /Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123:17-24
11. Diggle SP, Cornelis P, Williams P, Cámara M (2006) 4-Quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 296:83-91
12. Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207-210
13. Ezzell JW Jr., Abshire TG, Little SF, Lidgerding BC, Brown C (1990) Identification of Bacillus anthracis by using monoclonal antibody to cell wall galactose-N-acetylglucosamine polysaccharide. J Clin Microbiol 28:223-231
14. Filiatrault MJ, Picardo KF, Ngai H, Passador L, Iglewski BH (2006) Identification of Pseudomonas aeruginosa genes involved in virulence and anaerobic growth. Infect Immun 74:4237-4245
15. Firoved AM, Wood SR, Ornatowski W, Deretic V, Timmins GS (2004) Microarray analysis and functional characterization of the nitrosative stress response in nonmucoid and mucoid Pseudomonas aeruginosa. J Bacteriol 186:4046-4050
16. Friedman L, Kolter R (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186:4457-4465
17. Fux CA, Costerton JW, Stewart PS, Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13:34-40
18. Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184:6472-6480
19. Gillam DE, Bishop PL, Love NG (2005) A study of glutathione-gated potassium efflux in biofilms using potassium microelectrodes. Environ Eng Sci 22:489-495
20. Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378-379
21. Izano EA, Sadovskaya I, Vinogradov E, Mulks MH, Velliyagounder K, Ragunath C, Kher WB, Ramasubbu N, Jabbouri S, Perry MB, Kaplan JB (2007) Poly-N-acetylglucosamine mediates biofilm formation and antibiotic resistance in Actinobacillus pleuropneumoniae. Microb Pathog 43:1-9
22. Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ (2004) Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186:4466-4475
23. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenthner D, Bovee D, Olson MV, Manoil C (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100:14339-14344
24. Junker LM, Clardy J (2007) High-throughput screens for small-molecule inhibitors of Pseudomonas aeruginosa biofilm development. Antimicrob Agents Chemother 51:3582-3590
25. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117:877-888
26. Keshk S, Sameshima K (2006) Influence of lignosulfonate on crystal structure and productivity of bacterial cellulose in a static culture. Enzyme Microb Technol 40:4-8
27. Kropec A, Maira-Litran T, Jefferson KK, Grout M, Cramton SE, Gotz F, Goldmann DA, Pier GB (2005) Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect Immun 73:6868-6876
28. Kuchma SL, Brothers KM, Merritt JH, Liberati NT, Ausubel FM, O'Toole GA (2007) BifA, a c-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:8165-8178
29. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 99:7072-7077
30. Lamont IL, Martin LW (2003) Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology 149:833-842
31. Lee J, Bansal T, Jayaraman A, Bentley WE, Wood TK (2007) Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microbiol 73:4100-4109
32. Lewenza S, Falsafi RK, Winsor G, Gooderham WJ, McPhee JB, Brinkman FS, Hancock REW (2005) Construction of a mini-Tn5-luxCDABE mutant library in Pseudomonas aeruginosa PAO1: a tool for identifying differentially regulated genes. Genome Res 15:583-589
33. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, Wu G, Villanueva J, Wei T, Ausubel FM (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A 103:2833-2838
34. Ma L, Jackson KD, Landry RM, Parsek MR, Wozniak DJ (2006) Analysis of Pseudomonas aeruginosa conditional Psl variants reveals roles for the Psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188:8213-8221
35. Ma L, Lu H, Sprinkle A, Parsek MR, Wozniak D (2007) Pseudomonas aeruginosa Psl is a galactose- and mannose-rich exopolysaccharide. J Bacteriol 189:8353-8356
36. Matsukawa M, Greenberg EP (2004) Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186:4449-4456
37. Merriman TR, Merriman ME, Lamont IL (1995) Nucleotide sequence of pvdD, a pyoverdine biosynthetic gene from Pseudomonas aeruginosa: PvdD has similarity to peptide synthetases. J Bacteriol 177:252-258
38. Michel L, González N, Jagdeep S, Nguyen-Ngoc T, Reimmann C (2005) PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Mol Microbiol 58:495-509
39. Moraes TF, Bains M, Hancock REW, Strynadka NCJ (2007) An arginine ladder in OprP mediates phosphate-specific transfer across the outer membrane. Nature Struct Biol 14:85-87
40. Nicolaus B, Lama L, Panico A, Moriello VS, Romano I, Gambacorta A (2002) Production and characterization of exopolysaccharides excreted by thermophilic bacteria from shallow, marine hydrothermal vents of Flegrean Ares (Italy). Syst Appl Microbiol 25:319-325
41. Ohman DE, Cryz SJ, Iglewski BH (1980) Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase. J Bacteriol 142:836-842
42. Parkins MD, Ceri H, Storey DG (2001) Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 40:1215-1226
43. Parvatiyar K, Alsabbagh EM, Ochsner UA, Stegemeyer MA, Smulian AG, Hwang SH, Jackson CR, McDermott TR, Hassett DJ (2005) Global analysis of cellular factors and responses involved in Pseudomonas aeruginosa resistance to arsenite. J Bacteriol 187:4853-4864
44. Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96:11229-11234
45. Pratt LA, Kolter R (1998) Genetic analysis of Escherichia coli biofilm formation: Roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30:285-293
46. Ren D, Bedzyk LA, Thomas SM, Ye RW, Wood TK (2004) Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64:515-524
47. Ren D, Zuo R, González Barrios AF, Bedzyk LA, Eldridge GR, Pasmore ME, Wood TK (2005a) Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl Environ Microbiol 71:4022-4034
48. Ren D, Zuo R, Wood TK (2005b) Quorum-sensing antagonist (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone influences siderophore biosynthesis in Pseudomonas putida and Pseudomonas aeruginosa. Appl Microbiol Biotechnol 66:689-695
49. Rodriguez RL, Tait RC (1983) Recombinant DNA techniques: an introduction. Benjamin/Cummings, Menlo Park, CA
50. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA
51. Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312-7326
52. Sperandio V, Torres AG, Kaper JB (2002) Quorum-sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43:809-821
53. Stintzi A, Evans K, Meyer J-M, Poole K (1998) Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol Lett 166:341-345
54. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock REW, Lory S, Olson MV (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406:959-964
55. Urata M, Miyakoshi M, Kai S, Maeda K, Habe H, Omori T, Yamane H, Nojiri H (2004) Transcriptional regulation of the ant operon, encoding two-component anthranilate 1,2-dioxygenase, on the carbazole-degradative plasmid pCAR1 of Pseudomonas resinovorans strain CA10. J Bacteriol 186:6815-6823
56. 5-oxygenase in Pseudomonas aeruginosa. J Bacteriol 176:1128-1140
57. von Heijne G (2006) Membrane-protein topology. Nat Rev Mol Cell Biol 7:909-918
58. Waite RD, Paccanaro A, Papakonstantinopoulou A, Hurst JM, Saqi M, Littler E, Curtis MA (2006) Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles. BMC Genomics 7:162
59. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860-864
60. Wilhelm S, Gdynia A, Tielen P, Rosenau F, Jaeger KE (2007) The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation. J Bacteriol 189:6695-6703
61. Winsor GL, Lo R, Ho Sui SJ, Ung KSE, Huang S, Cheng D, Ho Ching WK, Hancock REW, Brinkman FSL (2005) Pseudomonas aeruginosa Genome Database and PseudoCAP: facilitating community-based, continually updated, genome annotation. Nucleic Acids Res 33:D338-D343
62. Yokochi T, Inoue Y, Kimura Y, Kato N (1990) Strong interaction of lipopolysaccharides possessing the mannose homopolysaccharides with complement and its relation to adjuvant action. J Immunol 144:3106-3110