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Biofilm dispersion in Pseudomonas aeruginosa

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Abstract

In recent decades, many researchers have written numerous articles about microbial biofilms. Biofilm is a complex community of microorganisms and an example of bacterial group behavior. Biofilm is usually considered a sessile mode of life derived from the attached growth of microbes to surfaces, and most biofilms are embedded in self-produced extracellular matrix composed of extracellular polymeric substances (EPSs), such as polysaccharides, extracellular DNAs (eDNA), and proteins. Dispersal, a mode of biofilm detachment indicates active mechanisms that cause individual cells to separate from the biofilm and return to planktonic life. Since biofilm cells are cemented and surrounded by EPSs, dispersal is not simple to do and many researchers are now paying more attention to this active detachment process. Unlike other modes of biofilm detachment such as erosion or sloughing, which are generally considered passive processes, dispersal occurs as a result of complex spatial differentiation and molecular events in biofilm cells in response to various environmental cues, and there are many biological reasons that force bacterial cells to disperse from the biofilms. In this review, we mainly focus on the spatial differentiation of biofilm that is a prerequisite for dispersal, as well as environmental cues and molecular events related to the biofilm dispersal. More specifically, we discuss the dispersal-related phenomena and mechanisms observed in Pseudomonas aeruginosa, an important opportunistic human pathogen and representative model organism for biofilm study.

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References

  • Abdel-Mawgoud, A.M., Lepine, F., and Deziel, E. 2010. Rhamnolipids: diversity of structures, microbial origins and roles. Appl. Microbiol. Biotechnol. 86, 1323–1336.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Allesen-Holm, M., Barken, K.B., Yang, L., Klausen, M., Webb, J.S., Kjelleberg, S., Molin, S., Givskov, M., and Tolker-Nielsen, T. 2006. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59, 1114–1128.

    Article  PubMed  CAS  Google Scholar 

  • Allison, D.G., Ruiz, B., SanJose, C., Jaspe, A., and Gilbert, P. 1998. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol. Lett. 167, 179–184.

    Article  PubMed  CAS  Google Scholar 

  • An, S., Wu, J., and Zhang, L.H. 2010. Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-Di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl. Environ. Microbiol. 76, 8160–8173.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Applegate, D.H. and Bryers, J.D. 1991. Effects of carbon and oxygen limitations and calcium concentrations on biofilm removal processes. Biotechnol. Bioeng. 37, 17–25.

    Article  PubMed  CAS  Google Scholar 

  • Banin, E., Brady, K.M., and Greenberg, E.P. 2006. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl. Environ. Microbiol. 72, 2064–2069.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Barber, C.E., Tang, J.L., Feng, J.X., Pan, M.Q., Wilson, T.J., Slater, H., Dow, J.M., Williams, P., and Daniels, M.J. 1997. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol. Microbiol. 24, 555–566.

    Article  PubMed  CAS  Google Scholar 

  • Barraud, N., Hassett, D.J., Hwang, S.H., Rice, S.A., Kjelleberg, S., and Webb, J.S. 2006. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J. Bacteriol. 188, 7344–7353.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Barraud, N., Schleheck, D., Klebensberger, J., Webb, J.S., Hassett, D.J., Rice, S.A., and Kjelleberg, S. 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J. Bacteriol. 191, 7333–7342.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Basu Roy, A. and Sauer, K. 2014. Diguanylate cyclase NicD-based signalling mechanism of nutrient-induced dispersion by Pseudomonas aeruginosa. Mol. Microbiol. 94, 771–793.

    Article  PubMed  CAS  Google Scholar 

  • Bayles, K.W. 2014. Bacterial programmed cell death: making sense of a paradox. Nat. Rev. Microbiol. 12, 63–69.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Berk, R.S. 1965. Effect of antibacterial agents on the autoplaque phenomenon of Pseudomonas aeruginosa. Can. J. Microbiol. 11, 213–219.

    Article  PubMed  CAS  Google Scholar 

  • Bernier, S.P., Ha, D.G., Khan, W., Merritt, J.H., and O’Toole, G.A. 2011. Modulation of Pseudomonas aeruginosa surface-associated group behaviors by individual amino acids through c-di-GMP signaling. Res. Microbiol. 162, 680–688.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boles, B.R., Thoendel, M., and Singh, P.K. 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol. Microbiol. 57, 1210–1223.

    Article  PubMed  CAS  Google Scholar 

  • Borriello, G., Werner, E., Roe, F., Kim, A.M., Ehrlich, G.D., and Stewart, P.S. 2004. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 48, 2659–2664.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boyd, A. and Chakrabarty, A.M. 1994. Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 60, 2355–2359.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Boyd, C.D., Chatterjee, D., Sondermann, H., and O’Toole, G.A. 2012. LapG, required for modulating biofilm formation by Pseudomonas fluorescens Pf0-1, is a calcium-dependent protease. J. Bacteriol. 194, 4406–4414.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Brandenburg, K.S., Rodriguez, K.J., McAnulty, J.F., Murphy, C.J., Abbott, N.L., Schurr, M.J., and Czuprynski, C.J. 2013. Tryptophan inhibits biofilm formation by Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 57, 1921–1925.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chen, X. and Stewart, P.S. 2000. Biofilm removal caused by chemical treatments. Water Res. 34, 4229–4233.

    Article  CAS  Google Scholar 

  • Choi, Y., Park, H.Y., Park, S.J., Kim, S.K., Ha, C., Im, S.J., and Lee, J.H. 2011. Growth phase-differential quorum sensing regulation of anthranilate metabolism in Pseudomonas aeruginosa. Mol. Cells 32, 57–65.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cohen, D., Mechold, U., Nevenzal, H., Yarmiyhu, Y., Randall, T.E., Bay, D.C., Rich, J.D., Parsek, M.R., Kaever, V., Harrison, J.J., et al. 2015. Oligoribonuclease is a central feature of cyclic diguanylate signaling in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 112, 11359–11364.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Costaglioli, P., Barthe, C., Claverol, S., Brozel, V.S., Perrot, M., Crouzet, M., Bonneu, M., Garbay, B., and Vilain, S. 2012. Evidence for the involvement of the anthranilate degradation pathway in Pseudomonas aeruginosa biofilm formation. Microbiologyopen 1, 326–339.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Costerton, J.W., Cheng, K.J., Geesey, G.G., Ladd, T.I., Nickel, J.C., Dasgupta, M., and Marrie, T.J. 1987. Bacterial biofilms in nature and disease. Ann. Rev. Microbiol. 41, 435–464.

    Article  CAS  Google Scholar 

  • Costerton, J.W., Stewart, P.S., and Greenberg, E.P. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322.

    Article  PubMed  CAS  Google Scholar 

  • D’Argenio, D.A., Calfee, M.W., Rainey, P.B., and Pesci, E.C. 2002. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184, 6481–6489.

    Article  CAS  Google Scholar 

  • Davey, M.E., Caiazza, N.C., and O’Toole, G.A. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185, 1027–1036.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Davies, D.G. and Marques, C.N. 2009. A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J. Bacteriol. 191, 1393–1403.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • de Beer, D., Stoodley, P., Roe, F., and Lewandowski, Z. 1994. Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol. Bioeng. 43, 1131–1138.

    Article  PubMed  CAS  Google Scholar 

  • Diggle, S.P., Winzer, K., Chhabra, S.R., Worrall, K.E., Camara, M., and Williams, P. 2003. The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol. Microbiol. 50, 29–43.

    Article  PubMed  CAS  Google Scholar 

  • Dong, Y.H., Zhang, X.F., An, S.W., Xu, J.L., and Zhang, L.H. 2008. A novel two-component system BqsS-BqsR modulates quorum sensing-dependent biofilm decay in Pseudomonas aeruginosa. Commun. Integr. Biol. 1, 88–96.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dow, J.M., Crossman, L., Findlay, K., He, Y.Q., Feng, J.X., and Tang, J.L. 2003. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc. Natl. Acad. Sci. USA 100, 10995–11000.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Engelberg-Kulka, H., Amitai, S., Kolodkin-Gal, I., and Hazan, R. 2006. Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet. 2, e135.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Farrell, E.K. and Tipton, P.A. 2012. Functional characterization of AlgL, an alginate lyase from Pseudomonas aeruginosa. Biochemistry 51, 10259–10266.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Franklin, M.J., Nivens, D.E., Weadge, J.T., and Howell, P.L. 2011. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front. Microbiol. 2, 167.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fuqua, C. and Greenberg, E.P. 2002. Listening in on bacteria: acylhomoserine lactone signalling. Nat. Rev. Mol. Cell. Biol. 3, 685–695.

    Article  PubMed  CAS  Google Scholar 

  • Gacesa, P. 1987. Alginate-modifying enzymes - a proposed unified mechanism of action for the lyases and epimerases. FEBS Lett. 212, 199–202.

    Article  CAS  Google Scholar 

  • Galperin, M.Y., Gaidenko, T.A., Mulkidjanian, A.Y., Nakano, M., and Price, C.W. 2001. MHYT, a new integral membrane sensor domain. FEMS Microbiol. Lett. 205, 17–23.

    Article  PubMed  CAS  Google Scholar 

  • Galperin, M.Y. and Koonin, E.V. 2012. Divergence and convertgence in enzyme evolution. J. Biol. Chem. 287, 21–28.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gjermansen, M., Nilsson, M., Yang, L., and Tolker-Nielsen, T. 2010. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol. Microbiol. 75, 815–826.

    Article  PubMed  CAS  Google Scholar 

  • Gjermansen, M., Ragas, P., Sternberg, C., Molin, S., and Tolker-Nielsen, T. 2005. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ. Microbiol. 7, 894–906.

    Article  PubMed  CAS  Google Scholar 

  • Guerrasantos, L.H., Kappeli, O., and Fiechter, A. 1986. Dependence of Pseudomonas-aeruginosa continuous culture biosurfactant production on nutritional and environmental-factors. Appl. Microbiol. Biotechnol. 24, 443–448.

    CAS  Google Scholar 

  • Haagensen, J.A., Klausen, M., Ernst, R.K., Miller, S.I., Folkesson, A., Tolker-Nielsen, T., and Molin, S. 2007. Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. J. Bacteriol. 189, 28–37.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hancock, R.E. and Speert, D.P. 2000. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist. Updat. 3, 247–255.

    Article  PubMed  CAS  Google Scholar 

  • Harmsen, M., Yang, L., Pamp, S.J., and Tolker-Nielsen, T. 2010. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol. Med. Microbiol. 59, 253–268.

    PubMed  CAS  Google Scholar 

  • Heurlier, K., Denervaud, V., Haenni, M., Guy, L., Krishnapillai, V., and Haas, D. 2005. Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J. Bacteriol. 187, 4875–4883.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hickman, J.W. and Harwood, C.S. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69, 376–389.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hinsa, S.M., Espinosa-Urgel, M., Ramos, J.L., and O’Toole, G.A. 2003. Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol. Microbiol. 49, 905–918.

    Article  PubMed  CAS  Google Scholar 

  • Hunt, S.M., Werner, E.M., Huang, B., Hamilton, M.A., and Stewart, P.S. 2004. Hypothesis for the role of nutrient starvation in biofilm detachment. Appl. Environ. Microbiol. 70, 7418–7425.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Irie, Y., O’Toole G.A., and Yuk, M.H. 2005. Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol. Lett. 250, 237–243.

    Article  PubMed  CAS  Google Scholar 

  • Jackson, D.W., Suzuki, K., Oakford, L., Simecka, J.W., Hart, M.E., and Romeo, T. 2002. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184, 290–301.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jain, S. and Ohman, D.E. 2005. Role of an alginate lyase for alginate transport in mucoid Pseudomonas aeruginosa. Infect. Immun. 73, 6429–6436.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kalkowski, I. and Conrad, R. 1991. Metabolism of nitric oxide in denitrifying Pseudomonas aeruginosa and nitrate-respiring Bacillus cereus. FEMS Microbiol. Lett. 66, 107–111.

    Article  PubMed  CAS  Google Scholar 

  • Kaplan, J.B. 2010. Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J. Dent. Res. 89, 205–218.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kaplan, J.B., Meyenhofer, M.F., and Fine, D.H. 2003. Biofilm growth and detachment of Actinobacillus actinomycetemcomitans. J. Bacteriol. 185, 1399–1404.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim, S.K., Im, S.J., Yeom, D.H., and Lee, J.H. 2012. AntR-mediated bidirectional activation of antA and antR, anthranilate degradative genes in Pseudomonas aeruginosa. Gene 505, 146–152.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J. and Park, W. 2015. Indole: a signaling molecule or a mere metabolic byproduct that alters bacterial physiology at a high concentration? J. Microbiol. 53, 421–428.

    Article  PubMed  CAS  Google Scholar 

  • Kim, S.K., Park, H.Y., and Lee, J.H. 2015. Anthranilate deteriorates the structure of Pseudomonas aeruginosa biofilms and antagonizes the biofilm-enhancing indole effect. Appl. Environ. Microbiol. 81, 2328–2338.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kirov, S.M., Castrisios, M., and Shaw, J.G. 2004. Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infect. Immun. 72, 1939–1945.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Klausen, M., Aaes-Jorgensen, A., Molin, S., and Tolker-Nielsen, T. 2003a. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50, 61–68.

    Article  PubMed  CAS  Google Scholar 

  • Klausen, M., Gjermansen, M., Kreft, J.U., and Tolker-Nielsen, T. 2006. Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol. Lett. 261, 1–11.

    Article  PubMed  CAS  Google Scholar 

  • Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes-Jorgensen, A., Molin, S., and Tolker-Nielsen, T. 2003b. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48, 1511–1524.

    Article  PubMed  CAS  Google Scholar 

  • Kohler, T., Curty, L.K., Barja, F., van Delden, C., and 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.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kolodkin-Gal, I., Romero, D., Cao, S., Clardy, J., Kolter, R., and Losick, R. 2010. D-amino acids trigger biofilm disassembly. Science 328, 627–629.

  • Landini, P., Antoniani, D., Burgess, J.G., and Nijland, R. 2010. Molecular mechanisms of compounds affecting bacterial biofilm formation and dispersal. Appl. Microbiol. Biotechnol. 86, 813–823.

    Article  PubMed  CAS  Google Scholar 

  • Lee, J.H., Lequette, Y., and Greenberg, E.P. 2006. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol. Microbiol. 59, 602–609.

    Article  PubMed  CAS  Google Scholar 

  • Lemon, K.P., Higgins, D.E., and Kolter, R. 2007. Flagellar motility is critical for Listeria monocytogenes biofilm formation. J. Bacteriol. 189, 4418–4424.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lequette, Y. and Greenberg, E.P. 2005. Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 37–44.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li, Y., Heine, S., Entian, M., Sauer, K., and Frankenberg-Dinkel, N. 2013. NO-induced biofilm dispersion in Pseudomonas aeruginosa is mediated by an MHYT domain-coupled phosphodiesterase. J. Bacteriol. 195, 3531–3542.

  • Li, Y., Petrova, O.E., Su, S., Lau, G.W., Panmanee, W., Na, R., Hassett, D.J., Davies, D.G., and Sauer, K. 2014. BdlA, DipA and induced dispersion contribute to acute virulence and chronic persistence of Pseudomonas aeruginosa. PLoS Pathog. 10, e1004168.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ma, L., Conover, M., Lu, H., Parsek, M.R., Bayles, K., and Wozniak, D.J. 2009. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog. 5, e1000354.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mashburn, L.M. and Whiteley, M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437, 422–425.

    Article  PubMed  CAS  Google Scholar 

  • McDougald, D., Rice, S.A., Barraud, N., Steinberg, P.D., and Kjelleberg, S. 2012. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat. Rev. Microbiol. 10, 39–50.

    CAS  Google Scholar 

  • Mikkelsen, H., Sivaneson, M., and Filloux, A. 2011. Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ. Microbiol. 13, 1666–1681.

    Article  PubMed  CAS  Google Scholar 

  • Morgan, R., Kohn, S., Hwang, S.H., Hassett, D.J., and Sauer, K. 2006. BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J. Bacteriol. 188, 7335–7343.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mulligan, C.N., Mahmourides, G., and Gibbs, B.F. 1989. The influence of phosphate-metabolism on biosurfactant production by Pseudomonas aeruginosa. J. Biotechnol. 12, 199–210.

    Article  CAS  Google Scholar 

  • Newell, P.D., Boyd, C.D., Sondermann, H., and O’Toole, G.A. 2011. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol. 9, e1000587.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Newell, P.D., Monds, R.D., and O’Toole, G.A. 2009. LapD is a bis- (3',5')-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc. Natl. Acad. Sci. USA 106, 3461–3466.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • O’Toole, G.A., Gibbs, K.A., Hager, P.W., Phibbs, P.V., Jr., and Kolter, R. 2000. The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 182, 425–431.

    Article  PubMed Central  PubMed  Google Scholar 

  • Orr, M.W., Donaldson, G.P., Severin, G.B., Wang, J.X., Sintim, H.O., Waters, C.M., and Lee, V.T. 2015. Oligoribonuclease is the primary degradative enzyme for pGpG in Pseudomonas aeruginosa that is required for cyclic-di-GMP turnover. Proc. Natl. Acad. Sci. USA 112, E5048–E5057.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ott, C.M., Day, D.F., Koenig, D.W., and Pierson, D.L. 2001. The release of alginate lyase from growing Pseudomonas syringae pathovar phaseolicola. Curr. Microbiol. 42, 78–81.

    Article  PubMed  CAS  Google Scholar 

  • Pamp, S.J. and Tolker-Nielsen, T. 2007. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 189, 2531–2539.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Percival, S.L., Hill, K.E., Williams, D.W., Hooper, S.J., Thomas, D.W., and Costerton, J.W. 2012. A review of the scientific evidence for biofilms in wounds. Wound Repair Regen. 20, 647–657.

    Article  PubMed  Google Scholar 

  • Petrova, O.E., Cherny, K.E., and Sauer, K. 2014. The Pseudomonas aeruginosa diguanylate cyclase GcbA, a homolog of P. fluorescens GcbA, promotes initial attachment to surfaces, but not biofilm formation, via regulation of motility. J. Bacteriol. 196, 2827–2841.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Petrova, O.E., Cherny, K.E., and Sauer, K. 2015. The diguanylate cyclase GcbA facilitates Pseudomonas aeruginosa biofilm dispersion by activating BdlA. J. Bacteriol. 197, 174–187.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Petrova, O.E. and Sauer, K. 2012a. Dispersion by Pseudomonas aeruginosa requires an unusual posttranslational modification of BdlA. Proc. Natl. Acad. Sci. USA 109, 16690–16695.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Petrova, O.E. and Sauer, K. 2012b. PAS domain residues and prosthetic group involved in BdlA-dependent dispersion response by Pseudomonas aeruginosa biofilms. J. Bacteriol. 194, 5817–5828.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Purevdorj-Gage, B., Costerton, W.J., and Stoodley, P. 2005. Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiology 151, 1569–1576.

    Article  PubMed  CAS  Google Scholar 

  • Reis, R.S., Pereira, A.G., Neves, B.C., and Freire, D.M. 2011. Gene regulation of rhamnolipid production in Pseudomonas aeruginosa-a review. Bioresour. Technol. 102, 6377–6384.

    Article  PubMed  CAS  Google Scholar 

  • Renelli, M., Matias, V., Lo, R.Y., and Beveridge, T.J. 2004. DNAcontaining membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150, 2161–2169.

    Article  PubMed  CAS  Google Scholar 

  • Rice, K.C. and Bayles, K.W. 2008. Molecular control of bacterial death and lysis. Microbiol. Mol. Biol. Rev. 72, 85–109. table of contents.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Romling, U., Galperin, M.Y., and Gomelsky, M. 2013. Cyclic di- GMP: the first 25 years of a universal bacterial second messenger. Microbiol. Mol. Biol. Rev. 77, 1–52.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Roy, A.B., Petrova, O.E., and Sauer, K. 2012. The phosphodiesterase DipA (PA5017) is essential for Pseudomonas aeruginosa biofilm dispersion. J. Bacteriol. 194, 2904–2915.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sauer, K., Camper, A.K., Ehrlich, G.D., Costerton, J.W., and Davies, D.G. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184, 1140–1154.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sauer, K., Cullen, M.C., Rickard, A.H., Zeef, L.A., Davies, D.G., and Gilbert, P. 2004. Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J. Bacteriol. 186, 7312–7326.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schleheck, D., Barraud, N., Klebensberger, J., Webb, J.S., McDougald, D., Rice, S.A., and Kjelleberg, S. 2009. Pseudomonas aeruginosa PAO1 preferentially grows as aggregates in liquid batch cultures and disperses upon starvation. PLoS One 4, e5513.

  • Sekhon Randhawa, K.K. and Rahman, P.K. 2014. Rhamnolipid biosurfactants-past, present, and future scenario of global market. Front. Microbiol. 5, 454.

    Article  PubMed Central  PubMed  Google Scholar 

  • Shrout, J.D., Tolker-Nielsen, T., Givskov, M., and Parsek, M.R. 2011. The contribution of cell-cell signaling and motility to bacterial biofilm formation. MRS Bull. 36, 367–373.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Soberon-Chavez, G., Lepine, F., and Deziel, E. 2005. Production of rhamnolipids by Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 68, 718–725.

    Article  PubMed  CAS  Google Scholar 

  • Sotirova, A., Spasova, D., Vasileva-Tonkova, E., and Galabova, D. 2009. Effects of rhamnolipid-biosurfactant on cell surface of Pseudomonas aeruginosa. Microbiol. Res. 164, 297–303.

    Article  PubMed  CAS  Google Scholar 

  • Stelitano, V., Giardina, G., Paiardini, A., Castiglione, N., Cutruzzola, F., and Rinaldo, S. 2013. C-di-GMP hydrolysis by Pseudomonas aeruginosa HD-GYP phosphodiesterases: analysis of the reaction mechanism and novel roles for pGpG. PLoS One 8, e74920.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stoodley, P., Lewandowski, Z., Boyle, J.D., and Lappin-Scott, H.M. 1999. The formation of migratory ripples in a mixed species bacterial biofilm growing in turbulent flow. Environ. Microbiol. 1, 447–455.

    Article  PubMed  CAS  Google Scholar 

  • Sudarsan, N., Lee, E.R., Weinberg, Z., Moy, R.H., Kim, J.N., Link, K.H., and Breaker, R.R. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321, 411–413.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, B.L. and Zhulin, I.B. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63, 479–506.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Thormann, K.M., Saville, R.M., Shukla, S., and Spormann, A.M. 2005. Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J. Bacteriol. 187, 1014–1021.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tolker-Nielsen, T., Brinch, U.C., Ragas, P.C., Andersen, J.B., Jacobsen, C.S., and Molin, S. 2000. Development and dynamics of Pseudomonas sp. biofilms. J. Bacteriol. 182, 6482–6489.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Turakhia, M.H., Cooksey, K.E., and Characklis, W.G. 1983. Influence of a calcium-specific chelant on biofilm removal. Appl. Environ. Microbiol. 46, 1236–1238.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ueda, A. and Wood, T.K. 2009. Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog. 5, e1000483.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vakulskas, C.A., Potts, A.H., Babitzke, P., Ahmer, B.M., and Romeo, T. 2015. Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol. Mol. Biol. Rev. 79, 193–224.

    Article  PubMed  Google Scholar 

  • van Gestel, J., Vlamakis, H., and Kolter, R. 2015. Division of labor in biofilms: the ecology of cell differentiation. Microbiol. Spectr. 3, MB-0002-2014.

  • Walters, M.C., Roe, F., Bugnicourt, A., Franklin, M.J., and Stewart, P.S. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47, 317–323.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang, J., Yu, B., Tian, D., and Ni, M. 2013. Rhamnolipid but not motility is associated with the initiation of biofilm seeding dispersal of Pseudomonas aeruginosa strain PA17. J. Biosci. 38, 149–156.

    Article  PubMed  CAS  Google Scholar 

  • Watnick, P. and Kolter, R. 2000. Biofilm, city of microbes. J. Bacteriol. 182, 2675–2679.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wei, Q. and Ma, L.Z. 2013. Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int. J. Mol. Sci. 14, 20983–21005.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C., and Mattick, J.S. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, S., Hamilton, M.A., Hamilton, G.C., Schumann, M.R., and Stoodley, P. 2004. Statistical quantification of detachment rates and size distributions of cell clumps from wild-type (PAO1) and cell signaling mutant (JP1) Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 70, 5847–5852.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wood, T.K. 2014. Biofilm dispersal: deciding when it is better to travel. Mol. Microbiol. 94, 747–750.

    Article  PubMed  CAS  Google Scholar 

  • Yang, N., Ding, S., Chen, F., Zhang, X., Xia, Y., Di, H., Cao, Q., Deng, X., Wu, M., Wong, C.C., et al. 2015. The Crc protein participates in down-regulation of the Lon gene to promote rhamnolipid production and rhl quorum sensing in Pseudomonas aeruginosa. Mol. Microbiol. 96, 526–547.

    Article  PubMed  CAS  Google Scholar 

  • Yoon, S.S., Hennigan, R.F., Hilliard, G.M., Ochsner, U.A., Parvatiyar, K., Kamani, M.C., Allen, H.L., DeKievit, T.R., Gardner, P.R., Schwab, U., et al. 2002. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell 3, 593–603.

    Article  PubMed  CAS  Google Scholar 

  • Zumft, W.G. 2002. Nitric oxide signaling and NO dependent transcriptional control in bacterial denitrification by members of the FNR-CRP regulator family. J. Mol. Microbiol. Biotechnol. 4, 277–286.

    PubMed  CAS  Google Scholar 

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Kim, SK., Lee, JH. Biofilm dispersion in Pseudomonas aeruginosa . J Microbiol. 54, 71–85 (2016). https://doi.org/10.1007/s12275-016-5528-7

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