Sensor kinase PA4398 modulates swarming motility and biofilm formation in Pseudomonas aeruginosa PA14

Applied and Environmental Microbiology

Volumn 81, Issue 4, 2015, Pages 1274-1285

  Strehmel, Janine ^a   Neidig, Anke ^a   Nusser, Michael ^a   Geffers, Robert ^b   Brenner Weiss, Gerald ^a   Overhage, Joerg ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCHEMISTRY; BIOFILMS; ENZYMES; PLANTS (BOTANY); POLYMERASE CHAIN REACTION;

BIOFILM FORMATION; ENVIRONMENTAL STIMULI; EXOPOLYSACCHARIDES; MICROARRAY ANALYSIS; PSEUDOMONAS AERUGINOSA; SWARMING BEHAVIOR; TRANSCRIPTIONAL REGULATOR; TWO-COMPONENT REGULATORY SYSTEMS;

GENES;

BACTERIUM; BIOFILM; GENE EXPRESSION; GROWTH RATE; MOTILITY; MUTATION; PATHOGEN; SWARMING;

PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEIN; CYCLIC GMP; PROTEIN KINASE;

BIOFILM; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; BIOFILMS; CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN KINASES; PSEUDOMONAS AERUGINOSA;

EID: 84922021117     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02832-14     Document Type: Article

References (69)

1. 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 RE, Lory S, Olson MV. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964. http://dx.doi.org /10.1038/35023079.
2. Davies JC. 2002. Pseudomonas aeruginosa in cystic fibrosis: pathogenesis and persistence. Paediatr Respir Rev 3:128-134. http://dx.doi.org/10.1016 /S1526-0550(02)00003-3.
3. Gilligan PH. 1991. Microbiology of airway disease in patients with cystic fibrosis. Clin Microbiol Rev 4:35-51.
4. Hancock RE, Speert DP. 2000. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updat 3:247-255. http://dx.doi.org/10.1054/drup.2000.0152.
5. Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH, Quax WJ. 2012. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76:46-65. http://dx.doi.org/10.1128 /MMBR.05007-11.
6. Balasubramanian D, Schneper L, Kumari H, Mathee K. 2013. A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 41:1-20. http://dx.doi.org/10.1093/nar /gks1039.
7. O'Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304. http://dx.doi.org/10.1046/j.1365-2958.1998.01062.x.
8. Yeung AT, Bains M, Hancock RE. 2011. The sensor kinase CbrA is a global regulator that modulates metabolism, virulence, and antibiotic resistance in Pseudomonas aeruginosa. J Bacteriol 193:918-931. http://dx.doi.org/10.1128/JB.00911-10.
9. Darzins A. 1994. Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus. Mol Microbiol 11:137-153. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00296.x.
10. Harshey RM, Matsuyama T. 1994. Dimorphic transition in Escherichia coli and Salmonella typhimurium-surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci U S A 91:8631-8635. http://dx.doi.org/10.1073/pnas.91.18.8631.
11. Köhler T, Curty LK, Barja F, van Delden C, Pechere JC. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182:5990-5996. http://dx.doi.org/10.1128/JB.182.21.5990-5996.2000.
12. Fraser GM, Hughes C. 1999. Swarming motility. Curr Opin Microbiol 2:630-635. http://dx.doi.org/10.1016/S1369-5274(99)00033-8.
13. Lai S, Tremblay J, Déziel E. 2009. Swarming motility: a multicellular behaviour conferring antimicrobial resistance. Environ Microbiol 11: 126-136. http://dx.doi.org/10.1111/j.1462-2920.2008.01747.x.
14. Overhage J, Lewenza S, Marr AK, Hancock RE. 2007. Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol 189:2164-2169. http://dx.doi.org/10.1128/JB.01623-06.
15. Tremblay J, Richardson AP, Lepine F, Déziel E. 2007. Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour. Environ Microbiol 9:2622-2630. http://dx.doi.org/10.1111/j.1462-2920.2007.01396.x.
16. Overhage J, Bains M, Brazas MD, Hancock RE. 2008. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190: 2671-2679. http://dx.doi.org/10.1128/JB.01659-07.
17. Matilla MA, Ramos JL, Duque E, de Dios Alche J, Espinosa-Urgel M, Ramos-Gonzalez MI. 2007. Temperature and pyoverdine-mediated iron acquisition control surface motility of Pseudomonas putida. Environ Microbiol 9:1842-1850. http://dx.doi.org/10.1111/j.1462-2920.2007.01286.x.
18. Gooderham WJ, Hancock REW. 2009. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev 33:279-294. http://dx.doi.org/10.1111/j.1574-6976.2008.00135.x.
19. Rodrigue A, Quentin Y, Lazdunski A, Mejean V, Foglino M. 2000. Twocomponent systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8:498-504. http://dx.doi.org/10.1016/S0966-842X(00)01833-3.
20. Galperin MY. 2006. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188:4169-4182. http://dx.doi.org/10.1128/JB.01887-05.
21. Mikkelsen H, Sivaneson M, Filloux A. 2011. Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ Microbiol 13:1666-1681. http://dx.doi.org/10.1111/j.1462-2920.2011.02495.x.
22. 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. http://dx.doi.org/10.1073 /pnas.0511100103.
23. Yeung AT, Torfs EC, Jamshidi F, Bains M, Wiegand I, Hancock RE, Overhage J. 2009. Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including MetR. J Bacteriol 191:5592-5602. http://dx.doi.org/10.1128/JB.00157-09.
24. Neidig A, Yeung AT, Rosay T, Tettmann B, Strempel N, Rueger M, Lesouhaitier O, Overhage J. 2013. TypA is involved in virulence, antimicrobial resistance and biofilm formation in Pseudomonas aeruginosa.BMC Microbiol 13:77. http://dx.doi.org/10.1186/1471-2180-13-77.
25. 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. http: //dx.doi.org/10.1016/S0378-1119(98)00130-9.
26. Choi KH, Kumar A, Schweizer HP. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64:391-397. http://dx.doi.org/10.1016/j.mimet.2005.06.001.
27. Déziel E, Comeau Y, Villemur R. 2001. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183:1195-1204. http://dx.doi.org /10.1128/JB.183.4.1195-1204.2001.
28. O'Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449-461. http://dx.doi.org /10.1046/j.1365-2958.1998.00797.x.
29. Merritt JH, Kadouri DE, O'Toole GA. 2005. Growing and analyzing static biofilms. Curr Protoc Microbiol Chapter 1:Unit 1B.1. http://dx.doi.org/10.1002/9780471729259.mc01b01s00.
30. Friedman L, Kolter R. 2004. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675-690. http: //dx.doi.org/10.1046/j.1365-2958.2003.03877.x.
31. Spangler C, Bohm A, Jenal U, Seifert R, Kaever V. 2010. A liquid chromatography-coupled tandem mass spectrometry method for quantitation of cyclic di-guanosine monophosphate. J Microbiol Methods 81: 226-231. http://dx.doi.org/10.1016/j.mimet.2010.03.020.
32. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. 1985. Measurement of protein using bicinchoninic acid. Anal Biochem 150:76- 85. http://dx.doi.org/10.1016/0003-2697(85)90442-7.
33. Strempel N, Neidig A, Nusser M, Geffers R, Vieillard J, Lesouhaitier O, Brenner-Weiss G, Overhage J. 2013. Human host defense peptide LL-37 stimulates virulence factor production and adaptive resistance in Pseudomonas aeruginosa. PLoS One 8:e82240. http://dx.doi.org/10.1371 /journal.pone.0082240.
34. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. http://dx.doi.org/10.1093 /nar/29.9.e45.
35. Butler MT, Wang Q, Harshey RM. 2010. Cell density and mobility protect swarming bacteria against antibiotics. Proc Natl Acad Sci U S A 107:3776-3781. http://dx.doi.org/10.1073/pnas.0910934107.
36. 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. http://dx.doi.org/10.1128/JB.01685-06.
37. 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 189:8154-8164. http://dx.doi.org/10.1128/JB.00585-07.
38. 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. Mol Microbiol 53:1123-1134. http://dx.doi.org/10.1111/j.1365-2958.2004.04206.x.
39. Jenal U, Malone J. 2006. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40:385-407. http://dx.doi.org/10.1146/annurev.genet.40.110405.090423.
40. Sutherland IW. 2001. The biofilm matrix-an immobilized but dynamic microbial environment. Trends Microbiol 9:222-227. http://dx.doi.org /10.1016/S0966-842X(01)02012-1.
41. Hickman JW, Tifrea DF, Harwood CS. 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102:14422-14427. http://dx.doi.org/10.1073/pnas.0507170102.
42. Kuchma SL, Brothers KM, Merritt JH, Liberati NT, Ausubel FM, O'Toole GA. 2007. BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:8165-8178. http://dx.doi.org/10.1128/JB.00586-07.
43. Guillon L, El Mecherki M, Altenburger S, Graumann PL, Schalk IJ. 2012. High cellular organization of pyoverdine biosynthesis in Pseudomonas aeruginosa: clustering of PvdA at the old cell pole. Environ Microbiol 14:1982-1994. http://dx.doi.org/10.1111/j.1462-2920.2012.02741.x.
44. Jimenez PN, Koch G, Papaioannou E, Wahjudi M, Krzeslak J, Coenye T, Cool RH, Quax WJ. 2010. Role of PvdQ in Pseudomonas aeruginosa virulence under iron-limiting conditions. Microbiology 156:49-59. http: //dx.doi.org/10.1099/mic.0.030973-0.
45. Youard ZA, Wenner N, Reimmann C. 2011. Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals 24:513-522. http://dx.doi.org/10.1007 /s10534-010-9399-9.
46. Kulasekara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3=-5=)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103:2839 -2844. http://dx.doi.org/10.1073 /pnas.0511090103.
47. Merritt JH, Ha DG, Cowles KN, Lu W, Morales DK, Rabinowitz J, Gitai Z, O'Toole GA. 2010. Specific control of Pseudomonas aeruginosa surfaceassociated behaviors by two c-di-GMP diguanylate cyclases. mBio 1(4): e00183-10. http://dx.doi.org/10.1128/mBio.00183-10.
48. Hengge R. 2009. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263-273. http://dx.doi.org/10.1038/nrmicro2109.
49. Düvel J, Bertinetti D, Moller S, Schwede F, Morr M, Wissing J, Radamm L, Zimmermann B, Genieser HG, Jansch L, Herberg FW, Haussler S. 2012. A chemical proteomics approach to identify c-di-GMP binding proteins in Pseudomonas aeruginosa. J Microbiol Methods 88:229-236. http://dx.doi.org/10.1016/j.mimet.2011.11.015.
50. Ha DG, Merritt JH, Hampton TH, Hodgkinson JT, Janecek M, Spring DR, Welch M, O'Toole GA. 2011. 2-Heptyl-4-quinolone, a precursor of the Pseudomonas quinolone signal molecule, modulates swarming motility in Pseudomonas aeruginosa. J Bacteriol 193:6770-6780. http://dx.doi.org/10.1128/JB.05929-11.
51. Kazmierczak BI, Lebron MB, Murray TS. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol Microbiol 60:1026-1043. http://dx.doi.org/10.1111/j.1365 -2958.2006.05156.x.
52. Kulasekara HD, Ventre I, Kulasekara BR, Lazdunski A, Filloux A, Lory S. 2005. A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55:368-380. http: //dx.doi.org/10.1111/j.1365-2958.2004.04402.x.
53. Mikkelsen H, Ball G, Giraud C, Filloux A. 2009. Expression of Pseudomonas aeruginosa CupD fimbrial genes is antagonistically controlled by RcsB and the EAL-containing PvrR response regulators. PLoS One 4:e6018. http://dx.doi.org/10.1371/journal.pone.0006018.
54. Tremblay J, Déziel E. 2010. Gene expression in Pseudomonas aeruginosa swarming motility. BMC Genomics 11:587. http://dx.doi.org/10.1186 /1471-2164-11-587.
55. Déziel E, Lepine F, Milot S, Villemur R. 2003. rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149:2005-2013. http://dx.doi.org/10.1099/mic.0.26154-0.
56. Imperi F, Tiburzi F, Visca P. 2009. Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 106:20440-20445. http://dx.doi.org/10.1073/pnas.0908760106.
57. Sio CF, Otten LG, Cool RH, Diggle SP, Braun PG, Bos R, Daykin M, Camara M, Williams P, Quax WJ. 2006. Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74:1673-1682. http://dx.doi.org/10.1128/IAI.74.3.1673 -1682.2006.
58. Hannauer M, Yeterian E, Martin LW, Lamont IL, Schalk IJ. 2010. An efflux pump is involved in secretion of newly synthesized siderophore by Pseudomonas aeruginosa. FEBS Lett 584:4751-4755. http://dx.doi.org/10.1016/j.febslet.2010.10.051.
59. Schalk IJ, Guillon L. 2013. Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol 15:1661-1673. http://dx.doi.org/10.1111/1462-2920.12013.
60. Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2010. The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection. J Bacteriol 192:117-126. http://dx.doi.org/10.1128/JB.00689-09.
61. Alibaud L, Kohler T, Coudray A, Prigent-Combaret C, Bergeret E, Perrin J, Benghezal M, Reimmann C, Gauthier Y, van Delden C, Attree I, Fauvarque MO, Cosson P. 2008. Pseudomonas aeruginosa virulence genes identified in a Dictyostelium host model. Cell Microbiol 10:729-740. http://dx.doi.org/10.1111/j.1462-5822.2007.01080.x.
62. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, Lory S. 2004. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7:745-754. http://dx.doi.org/10.1016/j.devcel.2004.08.020.
63. Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C, Molin S, Bleves S, Lazdunski A, Lory S, Filloux A. 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci U S A 103:171-176. http://dx.doi.org/10.1073/pnas.0507407103.
64. Furukawa S, Kuchma SL, O'Toole GA. 2006. Keeping their options open: acute versus persistent infections. J Bacteriol 188:1211-1217. http://dx.doi.org/10.1128/JB.188.4.1211-1217.2006.
65. Matz C, Moreno AM, Alhede M, Manefield M, Hauser AR, Givskov M, Kjelleberg S. 2008. Pseudomonas aeruginosa uses type III secretion system to kill biofilm-associated amoebae. ISME J 2:843-852. http://dx.doi.org /10.1038/ismej.2008.47.
66. Drenkard E, Ausubel FM. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740- 743. http://dx.doi.org/10.1038/416740a.
67. Yahr TL, Wolfgang MC. 2006. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 62:631-640. http://dx.doi.org/10.1111/j.1365-2958.2006.05412.x.
68. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat Biotechnol 1:784-791. http://dx.doi.org/10.1038 /nbt1183-784.
69. West SE, Schweizer HP, Dall C, Sample AK, Runyen-Janecky LJ. 1994. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148:81-86. http://dx.doi.org/10.1016/0378-1119(94)90237-2.