Skip to main content
Log in

Composition and functions of the extracellular polymer matrix of bacterial biofilms

  • Reviews
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

The data on the composition and structure of the components comprising the extracellular polymer matrix of bacterial biofilms, the role of these components, and their functions in the biofilm are reviewed. The main biochemical mechanisms regulating the biosynthesis of biofilm matrix are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Nikolaev, Yu.A. and Plakunov, V.K., Biofilm—“City of microbes” or an analogue of multicellular organisms?, Microbiology (Moscow), 2007, vol. 76, no. 2, pp. 125–138.

    Article  CAS  Google Scholar 

  2. Flemming, H. and Wingender, J., The biofilm matrix, Nature Rev. Microbiol., 2010, vol. 8, pp. 623–633.

    CAS  Google Scholar 

  3. Flemming, H.-C., The perfect slime, Colloids Surf., 2011, vol. 86, pp. 251–259.

    Article  CAS  Google Scholar 

  4. Knirel, Y.A., Bystrova, O.V., Kocharova, N.A., Zähringer, U., and Pier, G., Review. Conserved and variable structural features in the lipopolysaccharide of Pseudomonas, J. Endotoxin Res., 2006, vol. 12, pp. 324–336.

    Article  CAS  PubMed  Google Scholar 

  5. Kocincova, D. and Lam, J.S., Structural diversity of the core oligosaccharide domain of Pseudomonas aeruginosa lipopolysaccharide, Biochemistry (Moscow), 2011, vol. 76, pp. 755–760.

    Article  CAS  Google Scholar 

  6. Ramsey, D.M. and Wozniak, D.J., Understanding the control of Pseudomonas aeruginosa alginate synthesis and the prospects for management of chronic infections in cystic fibrosis, Mol. Microbiol., 2005, vol. 56, pp. 309–322.

    Article  CAS  PubMed  Google Scholar 

  7. Branda, S.S., Vik, A., Friedman, L., and Kolter, R., Biofilms: the matrix revisited, Trends Microbiol., 2005, vol. 13, pp. 20–26.

    Article  CAS  PubMed  Google Scholar 

  8. Mann, E.E. and Wozniak, D.J., Pseudomonas biofilm matrix composition and niche biology, FEMS Microbiol. Rev., 2012, vol. 36, pp. 893–916.

    Article  CAS  PubMed  Google Scholar 

  9. Wozniak, D.J., Wyckoff, T.J.O., Starkey, M., Keyser, R., Azadi, P., O’Toole, G.A., and Parsek, M.R., Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms, Proc. Natl. Acad. Sci. U. S. A., 2003, vol. 100, pp. 7907–7912.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Orgad, O., Oren, Y., Walker, S.L., and Herzberg, M., The role of alginate in Pseudomonas aeruginosa EPS adherence, viscoelastic properties and cell attachment, Biofouling, 2011, vol. 27, pp. 787–798.

    Article  CAS  PubMed  Google Scholar 

  11. Wiens, J.R., Vasil, A.I., Schurr, M.J., and Vasil, M.L., Iron-regulated expression of alginate production, mucoid phenotype, and biofilm formation by Pseudomonas aeruginosa, MBio, 2014, vol. 5, no. 1. http://journals.asm.org/subscriptions

    Google Scholar 

  12. Lee, K., Lim, E.J., Kim, K.S., Huang, S-L., Veeranagouda, Y., and Rehm, B.H.A., An alginate-like exopolysaccharide biosynthesis gene cluster involved in biofilm aerial structure formation by Pseudomonas alkylphenolia, Appl. Microbiol. Biotechnol., 2014, vol. 98, pp. 4137–4148. http://link.springer.com/article/10.1007%2Fs00253-014-5529-6

    Article  CAS  PubMed  Google Scholar 

  13. Pagès, D., Sanchez, L., Conrod, S., Gidrol, X., Fekete, A., Schmitt-Kopplin, P., Heulin, T., and Achouak, W., Exploration of intraclonal adaptation mechanisms of Pseudomonas brassicacearum facing cadmium toxicity, Environ. Microbiol., 2007, vol. 9, pp. 2820–2835.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Ma, L., Conover, M., Lu, H., Parsek, M.R., Bayles, K., and Wozniak, D.J., Assembly and development of the Pseudomonas aeruginosa biofilm matrix, PLoS Pathogens, 2009, vol. 5, no. 3. e1000354.6. www.plospathogens.org

    Article  Google Scholar 

  15. Byrd, M.S., Sadovskaya, I., Vinogradov, E., Lu, H., Sprinkle, A.B., Richardson, S.H., Ma, L., Ralston, B., Parsek, M.R., Anderson, E.M., Lam, J.S., and Wozniak, D.J., Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production, Mol. Microbiol., 2009, vol. 73, pp. 622–638.

    Article  CAS  PubMed  Google Scholar 

  16. Irie, Y., Starkey, M., Edwards, A.N., Wozniak, D.J., Romeo, T., and Parsek, M.R., Pseudomonas aeruginosa posttranscriptional regulator RsmA represses biofilm extracellular polysaccharide Psl synthesis, Mol. Microbiol., 2010, vol. 78, pp. 158–172.

    CAS  PubMed Central  PubMed  Google Scholar 

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

  18. Colvin, K.M, Gordon, V.D., Murakami, K., Borlee, B.R., Wozniak, D.J., Wong, G.C.L., and Parsek, M.R., The Pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa, PLoS Pathog., 2011, vol. 7. E.1. e001264. www.plospathogens.org

    Google Scholar 

  19. Ghafoor, A., Hay, I.D., and Rehm, B.H.A., Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture, Appl. Environ. Microbiol., 2011, vol. 77, pp. 5238–5246.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Cooley, B.J., Thatcher, T.W., Hashmi, S.M., L’Her, G., Le, H.H., Hurwitz, D.A., Provenzano, D., Touhami, A., and Gordon, V.D., The extracellular polysaccharide Pel makes the attachment of P. aeruginosa to surfaces symmetric and short-ranged, Soft Matter, 2013, vol. 9, pp. 3871–3876.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Serra, D.O., Richter, A.M., Klauck, G., Mika, F., and Hengge, R., Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm, Mbio. Asm. org., 2013, vol. 4 I.2. e00103–13

    Google Scholar 

  22. Spiers, A.J. and Rainey, P.B., The Pseudomonas fluorescens SBW25 wrinkley spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity, Microbiology (UK), 2005, vol. 151, pp. 2829–2839.

    Article  CAS  Google Scholar 

  23. Nielsen, L, Li, X. and Halverson, L.J., Cell-cell and cell-surface interactions mediated by cellulose and a novel exopolysaccharide contribute to Pseudomonas putida biofilm formation and fitness under water-limiting conditions, Environ. Microbiol., 2011, vol. 13, pp. 1342–1356.

    Article  CAS  PubMed  Google Scholar 

  24. Morgan, J.L., McNamara, J.T., and Zimmer, J., Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP, Nature Structur. Molec. Biol., 2014, vol. 21, pp. 489–498.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Dubeau, D., Deziel, E., Woods, D.E., and Lepine, F., Burkholderia thailandensis harbors two identical rhl gene clusters responsible for the biosynthesis of rhamnolipids, BMC Microbiol., 2009, vol. 9, p. 263. www.biomedcentral.com/1471-2180/9/263

    Article  PubMed Central  PubMed  Google Scholar 

  27. Müller, M.M., Kügler, J.H., Henkel, M., Gerlitzki, M., Hörmann, B., Pöhnlein, M., Syldatk, C., and Hausmann, R., Rhamnolipids-next generation surfactants?, J. Biotechnol., 2012, vol. 162, pp. 366–380.

    Article  PubMed  Google Scholar 

  28. Lopez, D., Vlamakis, H., and Kolter, R., Biofilms, Cold Spring Harb. Perspect. Biol., 2010. V. 2. a000398

    Article  PubMed Central  PubMed  Google Scholar 

  29. Marvasi, M., Visscher, P.T., and Martinez, L.C. Exopolymeric substances (EPS) from Bacillus subtilis: polymers and genes encoding their synthesis, FEMS Microbiol. Lett., 2010, vol. 313, pp. 1–9.

    Article  CAS  PubMed  Google Scholar 

  30. Branda, S.S., Gonzalez-Pastor, J. E., Dervyn, E., Ehrlich, S.D., Losick, R., and Kolter, R., Genes involved in formation of structured multicellular communities by Bacillus subtilis, J. Bacteriol., 2004, vol. 186, pp. 3970–3979.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Cue, D., Lei, M.G., and Lee, C.Y., Activation of sarX by Rbf is required for biofilm formation and icaADBC expression in Staphylococcus aureus, J. Bacteriol., 2013, vol. 195, pp. 1515–524.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Lembré, P., Vendrely, C., and Di Martino, P., Identification of an amyloidogenic peptide from the Bap protein of Staphylococcus epidermidis, Protein Peptide Lett., 2014, vol. 21, pp. 75–79.

    Article  Google Scholar 

  33. Romero, D., Vlamakis, H., Losick, R., and Kolter, R., Functional analysis of the accessory protein TapA in Bacillus subtilis amyloid fiber assembly, J. Bacteriol., 2014, vol. 196, pp. 1505–1513.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Koo, H., Falsetta, M.L., and Klein, M.I., The exopolysaccharide matrix: a virulence determinant of cariogenic biofilm, J. Dent. Res., 2013, vol. 92, pp. 1065–1073.

    Article  CAS  PubMed  Google Scholar 

  35. McSwain, B.S., Irvine, R.L., Hausner, M., and Wilderer, P.A., Composition and distribution of extracellular polymeric substances in aerobic flocs and granular sludge, Appl. Environ. Microbiol., 2005, vol. 71, pp. 1051–1057.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Kulp, A. and Kuehn, M.J., Biological functions and biogenesis of secreted bacterial outer membrane vesicles, Annu. Rev. Microbiol., 2010, vol. 64, pp. 163–184.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Tashiro, Y., Uchiyama, H., and Nomura, N., Multifunctional membrane vesicles in Pseudomonas aeruginosa, Environ. Microbiol., 2012, vol. 14, pp. 1349–1362.

    Article  CAS  PubMed  Google Scholar 

  38. Schooling, S.R. and Beveridge, T.J., Membrane vesicles: an overlooked component of the matrices of biofilms, J. Bacteriol., 2006, vol. 188, pp. 5945–5957.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Toyofuku, M., Roschitzki, B., Riedel, K., and Eberl, L., Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix, J. Proteom. Res., 2012, vol. 11, pp. 4906–4915.

    Article  CAS  Google Scholar 

  40. Bordeau, V. and Felden, B., Curli synthesis and biofilm formation in enteric bacteria are controlled by a dynamic small RNA module made up of a pseudoknot assisted by an RNA chaperone, Nucleic Acids Res., 2014, vol. 42, pp. 4682–4696.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Qin, Z., Ou, Y., Yang, L., Zhu, Y., Tolker-Nielsen, T., Molin, S., and Qu, D., Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis, Microbiology (UK), 2007, vol. 153, pp. 2083–2092.

    Article  CAS  Google Scholar 

  42. Thomas, V.C. and Hancock, L.E., Suicide and fratricide in bacterial biofilms, Int. J. Artif. Organs, 2009, vol.32, pp. 537–544.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  44. Okshevsky, M. and Meyer, R.L., The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms, Crit. Rev. Microbiol., 2013. Informa Healthcare USA http://informahealth-care.com/mby

    Google Scholar 

  45. Schmidt, J., Musken, M., Becker, T., Magnowska, Z., Bertinetti, D., Moller, S., Zimmermann, B., Herberg, F. W., Jansch, L., and Haussler, S., The Pseudomonas aeruginosa chemotaxis methyltransferase CheR1 impacts on bacterial surface sampling, PLoS One, 2011, vol. 6. I.3. e18184

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Nickzad, A. and Deziel, E., The involvement of rhamnolipids in microbial cell adhesion and biofilm development—an approach for control?, Lett. Appl. Microbiol., 2014, vol. 58, pp. 447–453.

    Article  CAS  PubMed  Google Scholar 

  47. Strelkova, E.A., Zhurina, M.V., Plakunov, V.K., and Belyaev, S.S., Stimulation of biofilm formation by antibiotics, Microbiology (Moscow), 2012, vol. 81, no. 2, pp. 259–262.

    Article  CAS  Google Scholar 

  48. Haussler, S. and Fuqua, C., Biofilms: new discoveries and significant wrinkles in a dynamic field, J. Bacteriol., 2012, vol. 195, pp. 2947–2958.

    Article  Google Scholar 

  49. An, S., Wu, J., and Zhang, L.H., Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclicdi-GMP phosphodiesterase with a putative hypoxiasensing domain, Appl. Environ. Microbiol., 2010, vol. 76, pp. 8160–8173.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Ferreira, A.S., Silva, I.N., Oliveira, V.H., Cunha, R., and Moreira, L.M., Insights into the role of extracellular polysaccharides in Burkholderia adaptation to different environments, Front. Cell. Infect. Microbiol., 2011, vol. 1 A. 16. www.frontiersin.org

  51. Strelkova, E.A., Pozdnyakova, N.V., Zhurina, M.V., Plakunov, V.K., and Belyaev, S.S., Role of the extracellular polymer matrix in resistance of bacterial biofilms to extreme environmental factors, Microbiology (Moscow), 2013, vol. 82, no. 2, pp. 119–125.

    Article  CAS  Google Scholar 

  52. Zhurina, M.V., Kostrikina, N.A., Parshina, E.Yu., Strelkova, E.A., Yusipovich, A.I., Maksimov, G.V., and Plakunov, V.K., Visualization of the extracellular polymeric matrix of Chromobacterium violaceum biofilms by microscopic methods, Microbiology (Moscow), 2013, vol. 82, no. 4, pp. 517–524.

    Article  CAS  Google Scholar 

  53. Mart’yanov, S.V., Zhurina, M.V., El’-Registan, G.I., and Plakunov, V.K., Activation of formation of bacterial biofilms by azithromycin and countering this effect, Microbiology (Moscow), 2014, vol. 83, no. 6, pp. 723- 731.

    Google Scholar 

  54. Madsen, J.S., Burmølle, M., Hansen, L.H., and Sørensen, S.J., The interconnection between biofilm formation and horizontal gene transfer, FEMS Immunol. Med. Microbiol., 2012, vol. 65, pp. 183–195.

    Article  CAS  PubMed  Google Scholar 

  55. Fazli, M., Almblad, H., Rybtke, M. L., Givskov, M., Eberl, L., and Tolker-Nielsen, T., Regulation of biofilm formation in Pseudomonas and Burkholderia species, Environ. Microbiol., 2014. doi: 10.1111/1462-2920.12448

    Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  57. O’Connor, J.R., Kuwada, N.J., Huangyutitham, V., Wiggins, P.A., and Harwood, C.S. Surface sensing and lateral subcellular localization of WspA, the receptor in a chemosensory-like system leading to c-di-GMP production, Mol. Microbiol., 2012, vol. 86, pp. 720–729.

    Article  PubMed Central  PubMed  Google Scholar 

  58. Nilsson, M., Chiang, W.C., Fazli, M., Gjermansen, M., Givskov, M., and Tolker-Nielsen, T., Influence of putative exopolysaccharide genes on Pseudomonas putida KT2440 biofilm stability, Environ. Microbiol., 2011, vol. 13, pp. 1357–1369.

    Article  CAS  PubMed  Google Scholar 

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

  60. Irie, Y., Borlee, B.R., O’Connor, J.R., Hill, P.J., Harwood, C.S., Wozniak, D.J., and Parsek, M.R., Selfproduced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa, Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, no. 50. www.pnas.org/cgi/doi/10.1073/pnas.1217993109

    Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Khmel’, I.A., Quorum-sensing regulation of gene expression: fundamental and applied aspects and the role in bacterial communication, Microbiology (Moscow), 2006, vol. 75, no. 4, pp. 390–397.

    Article  Google Scholar 

  63. Li, Z. and Nair, S.K., Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals?, Protein Sci., 2012, vol. 21, pp. 1403–1417.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Gupta, R. and Schuster, M., Quorum sensing modulates colony morphology through alkyl quinolones in Pseudomonas aeruginosa, BMC Microbiol., 2012, vol. 12, no. 30. www.biomedcentral.com/14712180/12/30

    Google Scholar 

  65. Mika, F. and Hengge, R., Small regulatory RNAs in the control of motility and biofilm formation in E. coli and Salmonella, Int. J. Mol. Sci., 2013, vol. 14, pp. 4560–4579.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Thomason, M.K., Fontaine, F., De Lay, N., and Storz, G., A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli, Mol. Microbiol., 2012, vol. 84, pp. 17–35.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Jørgensen, M.G., Nielsen, J.S., Boysen, A., Franch, T., Møller-Jensen, J., and Valentin-Hansen, P., Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli, Mol. Microbiol., 2012, vol. 84, pp. 36–50.

    Article  PubMed  Google Scholar 

  68. De Lay, N. and Gottesman, S., A complex network of small non-coding RNAs regulate motility in Escherichia coli, Mol. Microbiol., 2012, vol. 86, pp. 524–538.

    Article  PubMed  Google Scholar 

  69. Marden, J.N., Diaz, M.R., Walton, W.G., Gode, C.J., Betts, L., and Urbanowski, M.L., An unusual CsrA family member operates in series with RsmA to amplify posttranscriptional responses in Pseudomonas aeruginosa, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, pp. 15055–15060.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Duque, E., de la Torre, J., Bernal, P., Molina-Henares, M.A., Alaminos, M., and Espinosa-Urgel, M., Identification of reciprocal adhesion genes in pathogenic and non-pathogenic Pseudomonas, Environ. Microbiol., 2013, vol. 15, pp. 36–48.

    Article  CAS  PubMed  Google Scholar 

  71. Wood, T.K., Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling, Environ. Microbiol., 2009, vol. 11, pp. 1–15.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  72. Lee, J., Jayaraman, A., and Wood, T.K., Indole is an inter-species biofilm signal mediated by SdiA, BMC Microbiol., 2007. 7:42. http://www.biomedcentral.com/1471-2180/7/42.

    Article  PubMed Central  PubMed  Google Scholar 

  73. Hochbaum, A.I., Kolodkin-Gal, I., and Foulston, L., Inhibitory effects of D-amino acids on Staphylococcus aureus biofilm development, J. Bacteriol., 2011, vol. 193, pp. 5616–5622.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Romero, D., Vlamakis, H., and Losick, R., An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms, Mol. Microbiol., 2011, vol. 80, pp. 1155–1168.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Oppenheimer-Shaanan, Y., Steinberg N., and Kolodkin-Gal, I., Small molecules are natural triggers for the disassembly of biofilms, Trends Microbiol., 2013, vol. 11, pp. 594–601.

    Article  Google Scholar 

  76. Bottcher, T., Kolodkin-Gal, I., and Kolter, R., Synthesis and activity of biomimetic biofilm disruptors, J. Am. Chem. Soc., 2013, vol. 135, pp. 2927–2930.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Burrell, M., Hanfrey, C.C., Murray, E.J., Stanley-Wall, N.R., and Michael, A.J., Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation, J. Biol. Chem., 2010, vol. 285, pp. 39224–39238.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Mathema, V.B., Koh, Y.S., and Thakuri, B.C., Parthenolide, a sesquiterpene lactone, expresses multiple anti-cancer and anti-inflammatory activities, Inflammation, 2012, vol. 35, pp. 560–565.

    Article  CAS  PubMed  Google Scholar 

  79. Romero, D., Sanabria-Valentín, E., and Vlamakis, H., Biofilm inhibitors that target amyloid proteins, Chem. Biol., 2013, vol. 20, pp. 102–110.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Schwartz, K., Syed, A.K., Stephenson, R.E., Rickard, A.H., and Boles, B.R., Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms, PLoS Pathog., 2012, vol. 8(6): e1002744

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  81. Rosenbluh, A. and Rosenberg, E., 1990. Role of autocide AMI in development of Myxococcus xanthus, J. Bacteriol., vol. 172, pp. 4307–4314.

  82. Karatan, E., Duncan, T.R., and Watnick, P.I., NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine, J. Bacteriol., 2005, vol. 187, pp. 7434–7443.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Schreiber, F., Beutler, M., and Enning, D., The role of nitric-oxide-synthase-derived nitric oxide in multicellular traits of Bacillus subtilis 3610: biofilm formation, swarming, and dispersal, BMC Microbiol., 2011, vol. 11:111. doi: 10.1186/1471-2180-11-111

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. Li, Y., Heine, S., and Entian, M., NO-induced biofilm dispersion in Pseudomonas aeruginosa is mediated by a MHYT-domain coupled phosphodiesterase, J. Bacteriol., 2013, vol. 195, pp. 3531–3542.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Plakunov, V.K., Strelkova, E.A., and Zhurina, M.V., Persistence and adaptive mutagenesis in biofilms, Microbiology (Moscow), 2010, vol. 79, no. 4, pp. 424–434.

    Article  CAS  Google Scholar 

  86. Ryall, B., Eydallin, G., and Ferenci, T., Culture history and population heterogeneity as determinants of bacterial adaptation: the adaptomics of a single environmental transition, Microbiol. Mol. Biol. Rev., 2012, vol. 76, pp. 597–625.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. K. Plakunov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhurina, M.V., Gannesen, A.V., Zdorovenko, E.L. et al. Composition and functions of the extracellular polymer matrix of bacterial biofilms. Microbiology 83, 713–722 (2014). https://doi.org/10.1134/S002626171406023X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S002626171406023X

Keywords

Navigation