The involvement of rhamnolipids in microbial cell adhesion and biofilm development - an approach for control?

Letters in Applied Microbiology

Volumn 58, Issue 5, 2014, Pages 447-453

  Nickzad, A ^a   Deziel E ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

Biofilms; Biosurfactants; Pseudomonas aeruginosa

Indexed keywords

BACTERIA; BIODEGRADABILITY; BIOFILMS; BIOMOLECULES; LIPIDS; METABOLITES; SURFACE ACTIVE AGENTS;

BIO-SURFACTANTS; BIOFILM DEVELOPMENT; CELLS ADHESION; CLINICAL SETTINGS; EFFICIENT STRATEGY; INDUSTRIAL SETTINGS; MICROBIAL CELLS; PSEUDOMONAS AERUGINOSA; RHAMNOLIPIDS; SIDE EFFECT;

CELL ADHESION;

ANTIFOULING AGENT; BIOSURFACTANT; RHAMNOLIPID;

ANTIFOULING; BACTERIOLOGY; BACTERIUM; BIODEGRADATION; BIOFILM; LIPID; MICROBIAL COMMUNITY; PRODUCTION COST; SECONDARY METABOLITE; SURFACTANT;

ARTICLE; BIODEGRADABILITY; BIOFILM; CELL ADHESION; CELL PROLIFERATION; DISPERSION; NONHUMAN; PLANKTON; PRODUCTIVITY; PSEUDOMONAS AERUGINOSA; TOXICITY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

BIOFILMS; BIOSURFACTANTS; PSEUDOMONAS AERUGINOSA;

BACTERIAL ADHESION; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODEGRADATION, ENVIRONMENTAL; BIOFILMS; GLYCOLIPIDS; PSEUDOMONAS AERUGINOSA; SURFACE-ACTIVE AGENTS;

EID: 84898919895     PISSN: 02668254     EISSN: 1472765X     Source Type: Journal    
DOI: 10.1111/lam.12211     Document Type: Article

References (65)

1. Abdel-Mawgoud, A.M., Lépine, F. and Déziel, E. (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86, 1323-1336.
2. Abdel-Mawgoud, A., Hausmann, R., Lépine, F., Müller, M. and Déziel, E. (2011) Rhamnolipids: detection, analysis, biosynthesis, genetic regulation, and bioengineering of production. In Biosurfactants ed. Soberón-Chávez, G. pp. 13-55. Berlin Heidelberg: Springer.
3. Al-Tahhan, R.A., Sandrin, T.R., Bodour, A.A. and Maier, R.M. (2000) Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Microbiol Biotechnol 66, 3262-3268.
4. Banat, I.M., Makkar, R.S. and Cameotra, S.S. (2000) Potential commercial applications of microbial surfactants. Appl Microbiol Biotechnol 53, 495-508.
5. Barken, K.B., Pamp, S.J., Yang, L., Gjermansen, M., Bertrand, J.J., Klausen, M., Givskov, M., Whitchurch, C.B. et al. (2008) Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10, 2331-2343.
6. Bergström, S., Theorell, H. and Davide, H. (1946) On a metabolic product of Ps. pyocyania. Pyolipic acid active against M. tuberculosis. Arkiv Kemi Mineral Geol 8, 23A-1.
7. Boles, B.R., Thoendel, M. and Singh, P.K. (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57, 1210-1223.
8. Boyle, K.E., Heilmann, S., van Ditmarsch, D. and Xavier, J.B. (2013) Exploiting social evolution in biofilms. Curr Opin Microbiol 16, 207-212.
9. Caiazza, N.C., Shanks, R.M. and O'Toole, G.A. (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187, 7351-7361.
10. Chrzanowski, Ł., Ławniczak, Ł. and Czaczyk, K. (2012) Why do microorganisms produce rhamnolipids? World J Microbiol Biotechnol 28, 401-419.
11. Davey, M.E. and O'Toole, G.A. (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64, 847-867.
12. 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.
13. 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.
14. Desai, J.D. and Banat, I.M. (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61, 47-64.
15. Déziel, E., Lépine, F., Dennie, D., Boismenu, D., Mamer, O.A. and 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.
16. Déziel, E., Lépine, F., Milot, S. and Villemur, R. (2000) Mass spectrometry monitoring of rhamnolipids from a growing culture of Pseudomonas aeruginosa strain 57RP. Biochim Biophys Acta 1485, 145-152.
17. Déziel, E., Lépine, F., Milot, S. and 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. Microbiol 149, 2005-2013.
18. Donlan, R.M. (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17, 66-72.
19. Dunne, W.M. Jr (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15, 155-166.
20. Dusane, D.H., Nancharaiah, Y.V., Zinjarde, S.S. and Venugopalan, V.P. (2010) Rhamnolipid mediated disruption of marine Bacillus pumilus biofilms. Colloids Surf B Biointerfaces 81, 242-248.
21. Dusane, D.H., Dam, S., Nancharaiah, Y.V., Kumar, A.R., Venugopalan, V.P. and Zinjarde, S.S. (2012) Disruption of Yarrowia lipolytica biofilms by rhamnolipid biosurfactant. Aquat Biosyst 8, 17.
22. Flemming, H.C. and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8, 623-633.
23. Glick, R., Gilmour, C., Tremblay, J., Satanower, S., Avidan, O., Deziel, E., Greenberg, E.P., Poole, K. et al. (2010) Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 192, 2973-2980.
24. Hall-Stoodley, L., Costerton, J.W. and Stoodley, P. (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95-108.
25. Herman, D.C., Zhang, Y. and Miller, R.M. (1997) Rhamnolipid (biosurfactant) effects on cell aggregation and biodegradation of residual hexadecane under saturated flow conditions. Appl Environ Microbiol 63, 3622-3627.
26. Hisatsuka, K.-I., Nakahara, T., Sano, N. and Yamada, K. (1971) Formation of rhamnolipid by Pseudomonas aeruginosa and its function in hydrocarbon fermentation. Agr Biol Chem 35, 686-692.
27. Irie, Y., O'Toole, G.A. and Yuk, M.H. (2005) Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol Lett 250, 237-243.
28. Itoh, S., Honda, H., Tomita, F. and Suzuki, T. (1971) Rhamnolipids produced by Pseudomonas aeruginosa grown on n-paraffin (mixture of C 12, C 13 and C 14 fractions). J Antibiot (Tokyo) 24, 855-859.
29. Jarvis, F.G. and Johnson, M.J. (1949) A glycolipide produced by Pseudomonas aeruginosa. J Am Chem Soc 71, 4124-4126.
30. Kanmani, P., Satish kumar, R., Yuvaraj, N., Paari, K.A., Pattukumar, V. and Arul, V. (2011) Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. Bioresour Technol 102, 4827-4833.
31. Kaplan, J.B. (2010) Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res 89, 205-218.
32. Kearns, D.B. (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8, 634-644.
33. 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.
34. 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.
35. Kuiper, I., Lagendijk, E.L., Pickford, R., Derrick, J.P., Lamers, G.E.M., Thomas-Oates, J.E., Lugtenberg, B.J.J. and Bloemberg, G.V. (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51, 97-113.
36. Lequette, Y. and Greenberg, E.P. (2005) Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187, 37-44.
37. 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.
38. Medina, G., Juarez, K. and Soberon-Chavez, G. (2003) The Pseudomonas aeruginosa rhlAB operon is not expressed during the logarithmic phase of growth even in the presence of its activator RhlR and the autoinducer N-butyryl-homoserine lactone. J Bacteriol 185, 377-380.
39. Mireles, J.R. 2nd, Toguchi, A. and Harshey, R.M. (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183, 5848-5854.
40. Ochsner, U.A. and Reiser, J. (1995) Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92, 6424-6428.
41. Ochsner, U.A., Fiechter, A. and Reiser, J. (1994a) 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.
42. Ochsner, U.A., Koch, A.K., Fiechter, A. and Reiser, J. (1994b) Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol 176, 2044-2054.
43. O'Toole, G.A. and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30, 295-304.
44. O'Toole, G., Kaplan, H.B. and Kolter, R. (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54, 49-79.
45. Palmer, J., Flint, S. and Brooks, J. (2007) Bacterial cell attachment, the beginning of a biofilm. J Ind Microbiol Biotechnol 34, 577-588.
46. Pamp, S.J. and Tolker-Nielsen, T. (2007) Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 189, 2531-2539.
47. Partridge, J.D. and Harshey, R.M. (2013) Swarming: flexible roaming plans. J Bacteriol 195, 909-918.
48. Patriquin, G.M., Banin, E., Gilmour, C., Tuchman, R., Greenberg, E.P. and Poole, K. (2008) Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 190, 662-671.
49. Raya, A., Sodagari, M., Pinzon, N.M., He, X., Zhang Newby, B.M. and Ju, L.K. (2010) Effects of rhamnolipids and shear on initial attachment of Pseudomonas aeruginosa PAO1 in glass flow chambers. Environ Sci Pollut Res Int 17, 1529-1538.
50. Rendueles, O. and Ghigo, J.M. (2012) Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 36, 972-989.
51. Rivardo, F., Turner, R.J., Allegrone, G., Ceri, H. and Martinotti, M.G. (2009) Anti-adhesion activity of two biosurfactants produced by Bacillus spp. prevents biofilm formation of human bacterial pathogens. Appl Microbiol Biotechnol 83, 541-553.
52. Rodrigues, L., van der Mei, H., Banat, I.M., Teixeira, J. and Oliveira, R. (2006a) Inhibition of microbial adhesion to silicone rubber treated with biosurfactant from Streptococcus thermophilus A. FEMS Immunol Med Microbiol 46, 107-112.
53. Rodrigues, L.R., Banat, I.M., van der Mei, H.C., Teixeira, J.A. and Oliveira, R. (2006b) Interference in adhesion of bacteria and yeasts isolated from explanted voice prostheses to silicone rubber by rhamnolipid biosurfactants. J Appl Microbiol 100, 470-480.
54. Romero, D. and Kolter, R. (2011) Will biofilm disassembly agents make it to market? Trends Microbiol 19, 304-306.
55. Ron, E.Z. and Rosenberg, E. (2001) Natural roles of biosurfactants. Environ Microbiol 3, 229-236.
56. Schooling, S.R., Charaf, U.K., Allison, D.G. and Gilbert, P. (2004) A role for rhamnolipid in biofilm dispersion. Biofilms 1, 91-99.
57. Shapiro, J.A. (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52, 81-104.
58. Sierra, G. (1960) Hemolytic effect of a glycolipid produced by Pseudomonas aeruginosa. Antonie Van Leeuwenhoek 26, 189-192.
59. Singh, N., Pemmaraju, S.C., Pruthi, P.A., Cameotra, S.S. and Pruthi, V. (2013) Candida biofilm disrupting ability of di-rhamnolipid (RL-2) produced from Pseudomonas aeruginosa DSVP20. Appl Biochem Biotechnol 169, 2374-2391.
60. Sodagari, M., Wang, H., Newby, B.M. and Ju, L.K. (2013) Effect of rhamnolipids on initial attachment of bacteria on glass and octadecyltrichlorosilane-modified glass. Colloids Surf B Biointerfaces 103, 121-128.
61. Tremblay, J., Richardson, A.P., Lepine, F. and Deziel, E. (2007) Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour. Environ Microbiol 9, 2622-2630.
62. Van Gennip, M., Christensen, L.D., Alhede, M., Phipps, R., Jensen, P.O., Christophersen, L., Pamp, S.J., Moser, C. et al. (2009) Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes. APMIS 117, 537-546.
63. Walencka, E., Rozalska, S., Sadowska, B. and Rozalska, B. (2008) The influence of Lactobacillus acidophilus-derived surfactants on staphylococcal adhesion and biofilm formation. Folia Microbiol (Praha) 53, 61-66.
64. 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.
65. Zhang, Y. and Miller, R.M. (1994) Effect of a Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane. Appl Environ Microbiol 60, 2101-2106.