Coordination of swarming motility, biosurfactant synthesis, and biofilm matrix exopolysaccharide production in Pseudomonas aeruginosa

Applied and Environmental Microbiology

Volumn 80, Issue 21, 2014, Pages 6724-6732

  Wang, Shiwei ^a   Yu, Shan ^a,b   Zhang, Zhenyin ^a   Wei, Qing ^a   Yan, Lu ^a   Ai, Guomin ^a   Liu, Hongsheng ^c   Ma, Luyan Z ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c LIAONING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOFILMS; BIOMOLECULES; BIOSYNTHESIS; COORDINATION REACTIONS; GENES; LIPIDS; METABOLITES; POLYSACCHARIDES; SURFACE ACTIVE AGENTS; TRANSCRIPTION;

BACTERIAL COMMUNITY; BACTERIAL MOTILITY; BIO SURFACTANT; BIOFILM FORMATION; BIOFILM MATRIX; COMPLEX PROCESSES; EXOPOLYSACCHARIDES; PSEUDOMONAS AERUGINOSA;

BACTERIA;

BIOFILM; COMPETITION (ECOLOGY); GENE EXPRESSION; LIPID; MORTALITY; PATHOGEN; PHENOTYPE; POLYSACCHARIDE; SURFACTANT; SWARMING;

PSEUDOMONAS AERUGINOSA;

BACTERIAL POLYSACCHARIDE; EXOPOLYSACCHARIDE, PSEUDOMONAS; GLYCOLIPID; RHAMNOLIPID; SURFACTANT;

BIOFILM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LOCOMOTION; METABOLISM; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA;

BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; GLYCOLIPIDS; LOCOMOTION; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS AERUGINOSA; SURFACE-ACTIVE AGENTS;

EID: 84914165779     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01237-14     Document Type: Article

References (46)

1. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318.
2. Wei Q, Ma L. 2013. Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int. J. Mol. Sci. 14:20983-21005. http://dx.doi.org/10.3390/ijms141020983.
3. Ma L-Y, Jackson K, 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. http://dx.doi.org/10.1128/JB.01202-06.
4. Ma L, Conover M, Lu H, Parsek MR, Bayles K, Wozniak DJ. 2009. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog. 5(3):e1000354. http://dx.doi.org/10.1371/journal.ppat.1000354.
5. Colvin KM, Irie Y, Tart CS, Urbano R, Whitney JC, Ryder C, Howell PL, Wozniak DJ, Parsek MR. 2012. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ. Microbiol. 14:1913-1928.
6. 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. http://dx.doi.org/10.1128/JB.186.14.4457-4465.2004.
7. 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.
8. Ma L, Wang S, Wang D, Parsek MR, Wozniak DJ. 2012. The roles of biofilm matrix polysaccharide Psl in mucoid Pseudomonas aeruginosa biofilms. FEMS Immunol. Med. Microbiol. 65:377-380. http://dx.doi.org/10.1111/j.1574-695X.2012.00934.x.
9. Byrd MS, Sadovskaya I, Vinogradov E, Lu H, Sprinkle AB, Richardson SH, Ma L, Ralston B, Parsek MR, Anderson EM, Lam JS, Wozniak DJ. 2009. Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol. Microbiol. 73:622-638. http://dx.doi.org/10.1111/j.1365-2958.2009.06795.x.
10. Irie Y, Borlee BR, O'Connor JR, Hill PJ, Harwood CS, Wozniak DJ, Parsek MR. 2012. Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 109:20632-20636. http://dx.doi.org/10.1073/pnas.1217993109.
11. Ma L, Wang J, Wang S, Anderson EM, Lam JS, Parsek MR, Wozniak DJ. 2012. Synthesis of multiple Pseudomonas aeruginosa biofilm matrix exopolysaccharides is post-transcriptionally regulated. Environ. Microbiol. 14:1995-2005. http://dx.doi.org/10.1111/j.1462-2920.2012.02753.x.
12. Rocchetta HL, Burrows LL, Lam JS. 1999. Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 63:523-553.
13. Ghafoor A, Jordens Z, Rehm BHA. 2013. Role of PelF in Pel polysaccharide biosynthesis in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 79:2968-2978. http://dx.doi.org/10.1128/AEM.03666-12.
14. 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.
15. Shrout JD, Chopp DL, Just CL, Hentzer M, Givskov M, Parsek MR. 2006. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol. Microbiol. 62:1264-1277. http://dx.doi.org/10.1111/j.1365-2958.2006.05421.x.
16. Köhler T, Curty LK, Barja F, van Delden C, Pechère J-C. 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.
17. Burrows LL. 2012. Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu. Rev. Microbiol. 66:493-520. http://dx.doi.org/10.1146/annurev-micro-092611-150055.
18. Leech AJ, Mattick JS. 2006. Effect of site-specific mutations in different phosphotransfer domains of the chemosensory protein ChpA on Pseudomonas aeruginosa motility. J. Bacteriol. 188:8479-8486. http://dx.doi.org/10.1128/JB.00157-06.
19. Déziel E, Lépine 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.
20. Soberón-Chávez G, Lépine F, Déziel E. 2005. Production of rhamnolipids by Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 68:718-725. http://dx.doi.org/10.1007/s00253-005-0150-3.
21. Zhu K, Rock CO. 2008. RhlA converts β-hydroxyacyl-acyl carrier protein intermediates in fatty acid synthesis to the β-hydroxydecanoyl-β-hydroxydecanoate component of rhamnolipids in Pseudomonas aeruginosa. J. Bacteriol. 190:3147-3154. http://dx.doi.org/10.1128/JB.00080-08.
22. Ochsner UA, Fiechter A, Reiser J. 1994. Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J. Biol. Chem. 269:19787-19795.
23. Ochsner UA, Reiser J. 1995. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 92:6424-6428. http://dx.doi.org/10.1073/pnas.92.14.6424.
24. Rahim R, Ochsner UA, Olvera C, Graninger M, Messner P, Lam JS, Soberón-Chávez G. 2001. Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol. Microbiol. 40:708-718. http://dx.doi.org/10.1046/j.1365-2958.2001.02420.x.
25. Olvera C, Goldberg JB, Sánchez R, Soberón-Chávez G. 1999. The Pseudomonas aeruginosa algC gene product participates in rhamnolipid biosynthesis. FEMS Microbiol. Lett. 179:85-90. http://dx.doi.org/10.1111/j.1574-6968.1999.tb08712.x.
26. Kuchma SL, Ballok AE, Merritt JH, Hammond JH, Lu W, Rabinowitz JD, O'Toole GA. 2010. Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. J. Bacteriol. 192:2950-2964. http://dx.doi.org/10.1128/JB.01642-09.
27. Römling U. 2013. Microbiology: bacterial communities as capitalist economies. Nature 497:321-322. http://dx.doi.org/10.1038/nature12103.
28. Baraquet C, Harwood CS. 2013. Cyclic diguanosine monophosphate represses bacterial flagella synthesis by interacting with the WalkerAmotif of the enhancer-binding protein FleQ. Proc. Natl. Acad. Sci. U. S. A. 110: 18478-18483. http://dx.doi.org/10.1073/pnas.1318972110.
29. Wang S, Parsek MR, Wozniak DJ, Ma LZ. 2013. A spider web strategy of type IV pili-mediated migration to build a fibre-like Psl polysaccharide matrix in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 15:2238-2253. http://dx.doi.org/10.1111/1462-2920.12095.
30. Rashid MH, Kornberg A. 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 97:4885-4890. http://dx.doi.org/10.1073/pnas.060030097.
31. Jensen SE, Fecycz IT, Campbell JN. 1980. Nutritional factors controlling exocellular protease production by Pseudomonas aeruginosa. J. Bacteriol. 144:844-847.
32. Hoang T, Kutchma A, Becher A, Schweizer H. 2000. Integrationproficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43:59-71. http://dx.doi.org/10.1006/plas.1999.1441.
33. Hoang T, Karkhoff-Schweizer R, Kutchma A, Schweizer H. 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 28:77-86.
34. Hassett DJ, Woodruff W, Wozniak DJ, Vasil ML, Cohen MS, Ohman DE. 1993. Cloning and characterization of the Pseudomonas aeruginosa sodA and sodB genes encoding iron-and manganese-cofactored superoxide dismutase: demonstration of increased manganese superoxide dismutase activity in alginate-producing bacteria. J. Bacteriol. 175:7658-7665.
35. Hori K, Marsudi S, Unno H. 2002. Simultaneous production of polyhydroxyalkanoates and rhamnolipids by Pseudomonas aeruginosa. Biotechnol. Bioeng. 78:699-707. http://dx.doi.org/10.1002/bit.10248.
36. Déziel E, Lépine F, Dennie D, Boismenu D, Mamer OA, Villemur R. 1999. Liquid chromatography/mass spectrometry analysis of mixtures of rhamnolipids produced by Pseudomonas aeruginosa strain 57RP grown on mannitol or naphthalene. Biochim. Biophys. Acta 1440:244-252. http://dx.doi.org/10.1016/S1388-1981(99)00129-8.
37. Jain DK, Collins-Thompson DL, Lee H, Trevors JT. 1991. A dropcollapsing test for screening surfactant-producing microorganisms. J. Microbiol. Methods 13:271-279. http://dx.doi.org/10.1016/0167-7012(91)90064-W.
38. Tremblay J, Richardson A-P, Lépine 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.
39. Starkey M, Hickman JH, Ma L, Zhang N, De Long S, Hinz A, Palacios S, Manoil C, Kirisits MJ, Starner TD, Wozniak DJ, Harwood CS, Parsek MR. 2009. Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J. Bacteriol. 191:3492-3503. http://dx.doi.org/10.1128/JB.00119-09.
40. Kirisits MJ, Prost L, Starkey M, Parsek MR. 2005. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 71:4809-4821. http://dx.doi.org/10.1128/AEM.71.8.4809-4821.2005.
41. Davey ME, Caiazza NC, O'Toole GA. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185:1027-1036. http://dx.doi.org/10.1128/JB.185.3.1027-1036.2003.
42. Boles BR, Thoendel M, Singh PK. 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol. Microbiol. 57:1210-1223. http://dx.doi.org/10.1111/j.1365-2958.2005.04743.x.
43. 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. http://dx.doi.org/10.1128/jb.184.4.1140-1154.2002.
44. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FSL, 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 GKS, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock REW, 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.
45. Coyne MJ, Russell KS, Coyle CL, Goldberg JB. 1994. The Pseudomonas aeruginosa algC gene encodes phosphoglucomutase required for the synthesis of a complete lipopolysaccharide core. J. Bacteriol. 176:3500-3507.
46. Schuster M, Greenberg EP. 2007. Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genomics 8:287. http://dx.doi.org/10.1186/1471-2164-8-287.