A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development

PLoS Pathogens

Volumn 5, Issue 11, 2009, Pages

  Petrova, Olga E ^a   Sauer, Karin ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BFISR PROTEIN; MIFSR PROTEIN; OUTER MEMBRANE PROTEIN REGULATOR; PHOSPHOPROTEIN; POLYSACCHARIDE; SIGMA FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIOPLANKTON; BIOFILM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME INACTIVATION; GENE EXPRESSION REGULATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; SURFACE PROPERTY; TRANSCRIPTION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; BIOFILMS; PHOSPHORYLATION; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

EID: 73549110327     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000668     Document Type: Article

References (86)

1. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annual Review of Microbiology 49: 711-745.
2. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: A common cause of persistent infection. Science 284: 1318-1322.
3. Gilligan PH (1991) Microbiology of airway disease in patients with cystic fibrosis. Clin Microbiol Rev 4: 35-51.
4. Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60: 539-574.
5. Pruitt JBA, McManus AT, Kim SH, Goodwin CW (1998) Burn Wound Infections: Current Status. World Journal of Surgery 22: 135-145.
6. Fleiszig SM, Evans DJ (2002) The pathogenesis of bacterial keratitis: studies with Pseudomonas aeruginosa. Clin Exp Optom 85: 271-278.
7. Takeyama K, Kunishima Y, Matsukawa M, Takahashi S, Hirose T, et al. (2002) Multidrug-resistant Pseudomonas aeruginosa isolated from the urine of patients with urinary tract infection. J Infect Chemother 8: 58-63.
8. Reinhardt A, Kohler T, Wood P, Rohner P, Dumas J-L, et al. (2007) Development and Persistence of Antimicrobial Resistance in Pseudomonas aeruginosa: a Longitudinal Observation in Mechanically Ventilated Patients. Antimicrob Agents Chemother 51: 1341-1350.
9. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annual Review of Microbiology 56: 187-209.
10. Sauer K (2003) The genomics and proteomics of biofilm formation. Genome Biology 4: 219.
11. Davey ME, O'Toole GA (2000) Microbial Biofilms: from Ecology to Molecular Genetics. Microbiol Mol Biol Rev 64: 847-867.
12. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm. J Bacteriol 184: 1140-1154.
13. Sauer K, Cullen MC, Rickard AH, Zeef LAH, Davies DG, et al. (2004) Characterization of Nutrient-Induced Dispersion in Pseudomonas aeruginosa PAO1 Biofilm. J Bacteriol 186: 7312-7326.
14. Vallet I, Diggle SP, Stacey RE, Camara M, Ventre I, et al. (2004) Biofilm Formation in Pseudomonas aeruginosa: Fimbrial cup Gene Clusters Are Controlled by the Transcriptional Regulator MvaT. J Bacteriol 186: 2880-2890.
15. O'Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Molecular Microbiology 30: 295-304.
16. O'Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Molecular Microbiology 28: 449-461.
17. Sauer K, Camper AK (2001) Characterization of Phenotypic Changes in Pseudomonas putida in Response to Surface-Associated Growth. J Bacteriol 183: 6579-6589.
18. Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, et al. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-281.
19. Ross P, Mayer R, Weinhouse H, Amikam D, Huggirat Y, et al. (1990) The cyclic diguanylic acid regulatory system of cellulose synthesis in Acetobacter xylinum. Chemical synthesis and biological activity of cyclic nucleotide dimer, trimer, and phosphothioate derivatives. J Biol Chem 265: 18933-18943.
20. Kuchma SL, Brothers KM, Merritt JH, Liberati NT, Ausubel FM, et al. (2007) BifA, a c-di-GMP phosphodiesterase, Inversely Regulates Biofilm Formation and Swarming Motility by Pseudomonas aeruginosa PA14. J Bacteriol: JB.00586-00507.
21. Merritt JH, Brothers KM, Kuchma SL, O'Toole GA (2007) SadC Reciprocally Influences Biofilm Formation and Swarming Motility via Modulation of Exopolysaccharide production and Flagellar Function. J Bacteriol: 585-507.
22. Morgan R, Kohn S, Hwang S-H, Hassett DJ, Sauer K (2006) BdlA, a Chemotaxis Regulator Essential for Biofilm Dispersion in Pseudomonas aeruginosa. J Bacteriol 188: 7335-7343.
23. Romling R, Amikam D (2006) Cyclic di-GMP as a second messenger Curr Opinion Microbiol 9: 218-228.
24. Simm R, Morr M, Kader A, Nimtz M, Romling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Molecular Microbiology 53: 1123-1134.
25. Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proceedings of the National Academy of Sciences 102: 14422-14427.
26. Paul R, Abel S, Wassmann P, Beck A, Heerklotz H, et al. (2007) Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J Biol Chem 282: 29170-29177.
27. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, et al. (2004) Cell cycledependent dynamic localization of a bacterial response regulator with a novel diguanylate cyclase output domain. Genes Dev 18: 715-727.
28. Thormann KM, Duttler S, Saville RM, Hyodo M, Shukla S, et al. (2006) Control of Formation and Cellular Detachment from Shewanella oneidensis MR-1 Biofilms by Cyclic di-GMP. J Bacteriol 188: 2681-2691.
29. Romling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Molecular Microbiology 57: 629-639.
30. Kirillina O, Fetherston JD, Bobrov AG, Abney J, Perry RD (2004) HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Molecular Microbiology 54:75-88.
31. Tischler AD, Camilli A (2005) Cyclic Diguanylate Regulates Vibrio cholerae Virulence Gene Expression. Infect Immun 73: 5873-5882.
32. Kulesekara H, Lee V, Brencic A, Liberati N, Urbach J, et al. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(39-59)-cyclic-GMP in virulence. Proceedings of the National Academy of Sciences 103: 2839-2844.
33. 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.
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. Rydera C, Byrda M, Wozniak DJ (2007) Role of polysaccharides in Pseudomonas aeruginosa biofilm development Current Opinion in Microbiology 10: 644-648.
36. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, et al. (2004) A Signaling Network Reciprocally Regulates Genes Associated with Acute Infection and Chronic Persistence in Pseudomonas aeruginosa. Developmental Cell 7: 745-754.
37. Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C, et al. (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. PNAS 103: 171-176.
38. Goodman AL, Merighi M, Hyodo M, Ventre I, Filloux A, et al. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen Genes Dev 23: 249-259.
39. O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54: 49-79.
40. Trapphoff T, Beutner C, Niehaus K, Colditz F (2009) Induction of distinct defense-associated protein patterns in Aphanomyces euteiches (Oomycota)-elicited and -inoculated Medicago truncatula cell-suspension cultures: a proteome and phosphoproteome approach. Mol Plant Microbe Interact 22: 421-436.
41. Soufi B, Gnad F, Jensen PR, Petranovic D, Mann M, et al. (2008) The Ser/Thr/ Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins. PROTEOMICS 8: 3486-3493.
42. Voisin S, Watson DC, Tessier L, Ding W, Foote S, et al. (2007) The cytoplasmic phosphoproteome of the Gram-negative bacterium Campylobacter jejuni: Evidence for modification by unidentified protein kinases. PROTEOMICS 7: 4338-4348.
43. Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, et al. (2008) Phosphoproteome Analysis of E. coli Reveals Evolutionary Conservation of Bacterial Ser/Thr/Tyr Phosphorylation. Mol Cell Proteomics 7: 299-307.
44. Eymann C, Becher D, Bernhardt J, Gronau K, Klutzny A, et al. (2007) Dynamics of protein phosphorylation on Ser/Thr/Tyr in Bacillus subtilis. PROTEOMICS 7: 3509-3526.
45. Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, et al. (2007) The Serine/ Threonine/Tyrosine Phosphoproteome of the Model Bacterium Bacillus subtilis. Mol Cell Proteomics 6: 697-707.
46. Le´vine A, Vannier F, Absalon C, Kuhn L, Jackson P, et al. (2006) Analysis of the dynamic Bacillus subtilis Ser/Thr/Tyr phosphoproteome implicated in a wide variety of cellular processes. PROTEOMICS 6: 2157-2173.
47. Nova´kova´ L, Saskova´ L, Pallova´ P, Janecek J, Novotna´ J, et al. (2005) Characterization of a eukaryotic type serine/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates. FEBS Journal 272: 1243-1254.
48. Bendt AK, Burkovski A, Schaffer S, Bott M, Farwick M, et al. (2003) Towards a phosphoproteome map of Corynebacterium glutamicum. PROTEOMICS 3: 1637-1646.
49. Ravichandran A, Sugiyama N, Tomita M, Swarup S, Ishihama Y (2009) Ser/ Thr/Tyr phosphoproteome analysis of pathogenic and non-pathogenic Pseudomonas species. PROTEOMICS 9: 2764-2775.
50. Southey-Pillig CJ, Davies DG, Sauer K (2005) Characterization of Temporal Protein Production in Pseudomonas aeruginosa Biofilms. J Bacteriol 187: 8114-8126.
51. Wolschin F, Wienkoop S, Weckwerth W (2005) Enrichment of phosphorylated proteins and peptides from complex mixtures using metal oxide/hydroxide affinity chromatography (MOAC). PROTEOMICS 5: 4389-4397.
52. Krüger R, Wolschin F, Weckwerth W, Bettmer J, Lehmann WD (2007) Plant protein phosphorylation monitored by capillary liquid chromatography- element mass spectrometry. Biochem Biophys Res Commun 355: 89-96.
53. Winsor GL, Van Rossum T, Lo R, Khaira B, Whiteside MD, et al. (2009) Pseudomonas Genome Database: facilitating user-friendly, comprehensive comparisons of microbial genomes. Nucl Acids Res 37: D483-488.
54. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
55. De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH (2001) Quorum-Sensing Genes in Pseudomonas aeruginosa Biofilms: Their Role and Expression Patterns. Appl Environ Microbiol 67: 1865-1873.
56. Mikkel K, Arne H, Paula R, Lotte L, Anders A-J, et al. (2003) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Molecular Microbiology 48: 1511-1524.
57. Joshua DS, David LC, Collin LJ, Morten H, Michael G, et al. (2006) The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Molecular Microbiology 62: 1264-1277.
58. Palmer KL, Aye LM, Whiteley M (2007) Nutritional Cues Control Pseudomonas aeruginosa Multicellular Behavior in Cystic Fibrosis Sputum. J Bacteriol 189: 8079-8087.
59. Kohler T, Curty LK, Barja F, van Delden C, Pechere J-C (2000) Swarming of Pseudomonas aeruginosa Is Dependent on Cell-to-Cell Signaling and Requires Flagella and Pili. J Bacteriol 182: 5990-5996.
60. Farrow JM III, Pesci EC (2007) Two Distinct Pathways Supply Anthranilate as a Precursor of the Pseudomonas Quinolone Signal. J Bacteriol 189: 3425-3433.
61. Palmer KL, Mashburn LM, Singh PK, Whiteley M (2005) Cystic Fibrosis Sputum Supports Growth and Cues Key Aspects of Pseudomonas aeruginosa Physiology. J Bacteriol 187: 5267-5277.
62. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH (2003) Microarray Analysis of Pseudomonas aeruginosa Quorum-Sensing Regulons: Effects of Growth Phase and Environment. J Bacteriol 185: 2080-2095.
63. Shrout JD, Chopp DL, Just CL, Hentzer M, Givskov M, et al. (2006) The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Molecular Microbiology 62: 1264-1277.
64. Schweizer HP (1991) The agmR gene, an environmentally responsive gene, complements defective glpR, which encodes the putative activator for glycerol metabolism in Pseudomonas aeruginosa. J Bacteriol 173: 6798-6806.
65. Parkins MD, Ceri H, Storey DG (2001) Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Molecular Microbiology 40: 1215-1226.
66. Kuchma SL, Connolly JP, O'Toole GA (2005) A Three-Component Regulatory System Regulates Biofilm Maturation and Type III Secretion in Pseudomonas aeruginosa. J Bacteriol 187: 1441-1454.
67. Kirby J, Zusman D (2003) Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proceedings of the National Academy of Sciences of the United States of America 100: 2008-2013.
68. Kroos L (2007) The Bacillus and Myxococcus Developmental Networks and Their Transcriptional Regulators. Annual Review of Genetics 41: 13-39.
69. Caberoy NB, Welch RD, Jakobsen JS, Slater SC, Garza AG (2003) Global Mutational Analysis of NtrC-Like Activators in Myxococcus xanthus: Identifying Activator Mutants Defective for Motility and Fruiting Body Development. J Bacteriol 185: 6083-6094.
70. Diodati ME, Ossa F, Caberoy NB, Jose IR, Hiraiwa W, et al. (2006) Nla18, a Key Regulatory Protein Required for Normal Growth and Development of Myxococcus xanthus. J Bacteriol 188: 1733-1743.
71. Ossa F, Diodati ME, Caberoy NB, Giglio KM, Edmonds M, et al. (2007) The Myxococcus xanthus Nla4 Protein Is Important for Expression of Stringent Response-Associated Genes, ppGpp Accumulation, and Fruiting Body Development. J Bacteriol 189: 8474-8483.
72. Gorski L, Kaiser D (1998) Targeted Mutagenesis of sigma 54 Activator Proteins in Myxococcus xanthus. J Bacteriol 180: 5896-5905.
73. Haldenwang WG (1995) The sigma factors of Bacillus subtilis. Microbiol Rev 59:1-30.
74. Gruber TM, Bryant DA (1997) Molecular systematic studies of eubacteria, using sigma70-type sigma factors of group 1 and group 2. J Bacteriol 179: 1734-1747.
75. Buck M, Gallegos M-T, Studholme DJ, Guo Y, Gralla JD (2000) The Bacterial Enhancer-Dependent sigma 54 (sigma N) Transcription Factor. J Bacteriol 182: 4129-4136.
76. Kulasekara H, Ventre I, Kulasekara B, LazdunskiAe, Filloux A, et al. (2005) A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Molecular Microbiology 55: 368-380.
77. Brencic A, Lory S (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Molecular Microbiology 72: 612-632.
78. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, et al. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395-2407.
79. Schweizer HP, Hoang TT (1995) An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158: 15-22.
80. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
81. Newman JR, Fuqua C (1999) Broad-host-range expression vectors that carry the-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227: 197-203.
82. Shrout J, Chopp D, Just C, Hentzer M, Givskov M, et al. (2006) The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Molecular Microbiology 62: 1264-1277.
83. Allegrucci M, Sauer K (2007) Characterization of Colony Morphology Variants Isolated from Streptococcus pneumoniae Biofilms. J Bacteriol 189: 2030-2038.
84. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, et al. (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. PNAS 100:14339-14344.
85. Figurski DH, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proceedings of the National Academy of Sciences of the United States of America 76:1648-1652.
86. Choi KH, Schweizer HP (2006) mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nature Protocol 1: 153-161.