Rhamnolipids: Detection, Analysis, Biosynthesis, Genetic Regulation, and Bioengineering of Production

  • Ahmad Mohammad Abdel-Mawgoud
  • Rudolf Hausmann
  • Francois Lépine
  • Markus M. Müller
  • Eric Déziel
Chapter
Part of the Microbiology Monographs book series (MICROMONO, volume 20)

Abstract

As promising biotechnological products, rhamnolipids (RLs) are the most investigated biosurfactants. Over the years, important efforts have been spent and an array of techniques has been developed for the isolation of producing bacterial strains and the characterization of a large variety of RL homologs and congeners. Investigations on RL production by the best known producer, the opportunistic pathogen Pseudomonas aeruginosa, have shown that production of RLs proceeds through de novo biosynthesis of precursors. Over the last 15 years, the genetic details underlying RL production in P. aeruginosa have been mostly unraveled, revealing a complex regulatory mechanism controlled by quorum sensing pathways of intercellular communication. A number of nutritional and cultivation factors affecting RL productivity have also been identified, while the use of many affordable and renewable raw substrates has been described to optimize the production. Multidisciplinary approaches are increasingly adopted to develop methods for the safe, cost-effective, and highly efficient production of RLs at the industrial scale.

Keywords

High Performance Liquid Chromatography Quorum Sensing Solid State Fermentation Corn Steep Liquor Acyl Carrier Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abadi HAH, Rashedi H, Amoabediny G, Asadi MM (2009) Purification of rhamnolipid using colloidal magnetic nanoparticles. Afr J Biotechnol 8:3097–3106Google Scholar
  2. Abalos A, Pinazo A, Infante MR, Casals M, Garcia F, Manresa A (2001) Physicochemical and antimicrobial properties of new rhamnolipids produced by Pseudomonas aeruginosa AT10 from soybean oil refinery wastes. Langmuir 17:1367–1371Google Scholar
  3. Abalos A, Maximo F, Manresa MA, Bastida J (2002) Utilization of response surface methodology to optimize the culture media for the production of rhamnolipids by Pseudomonas aeruginosa AT10. J Chem Technol Biotechnol 77:777–784Google Scholar
  4. Abdel-Mawgoud AM, Aboulwafa MM, Hassouna NAH (2009) Characterization of rhamnolipid produced by Pseudomonas aeruginosa isolate BS20. Appl Biochem Biotechnol 157:329–345PubMedGoogle Scholar
  5. Abdel-Mawgoud AM, Lépine F, Déziel E (2010) Rhamnolipids: diversity of structures, microbial origins, and roles. Appl Microbiol Biotechnol 86:1323–1336PubMedGoogle Scholar
  6. Abouseoud M, Yataghene A, Amrane A, Maachi R (2008) Biosurfactant production by free and alginate entrapped cells of Pseudomonas fluorescens. J Ind Microbiol Biotechnol 35:1303–1308PubMedGoogle Scholar
  7. Al-Tahhan RA, Sandrin TR, Bodour AA, Maier RM (2000) Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Environ Microbiol 66:3262–3268PubMedGoogle Scholar
  8. Andrä J, Rademann J, Howe J, Koch MHJ, Heine H, Zahringer U, Brandenburg K (2006) Endotoxin-like properties of a rhamnolipid exotoxin from Burkholderia (Pseudomonas) plantarii: immune cell stimulation and biophysical characterization. Biol Chem 387:301–310PubMedGoogle Scholar
  9. Arino S, Marchal R, Vandecasteele JP (1996) Identification and production of a rhamnolipidic biosurfactant by a Pseudomonas species. Appl Microbiol Biotechnol 45:162–168Google Scholar
  10. Arino S, Marchal R, Vandecasteele JP (1998a) Involvement of a rhamnolipid-producing strain of Pseudomonas aeruginosa in the degradation of polycyclic aromatic hydrocarbons by a bacterial community. J Appl Microbiol 84:769–776PubMedGoogle Scholar
  11. Arino S, Marchal R, Vandecasteele JP (1998b) Production of new extracellular glycolipids by a strain of Cellulomonas cellulans (Oerskovia xanthineolytica) and their structural characterization. Can J Microbiol 44:238–243Google Scholar
  12. Asci Y, Nurbas M, Acikel YS (2007) Sorption of Cd(II) onto kaolin as a soil component and desorption of Cd(II) from kaolin using rhamnolipid biosurfactant. J Hazard Mater 139:50–56PubMedGoogle Scholar
  13. Asci Y, Nurbas M, Acikel YS (2008) Removal of zinc ions from a soil component Na-feldspar by a rhamnolipid biosurfactant. Desalination 223(1–3):361–365Google Scholar
  14. Avramova T, Sotirova A, Galabova D, Karpenko E (2008) Effect of Triton X-100 and rhamnolipid PS-17 on the mineralization of phenanthrene by Pseudomonas sp cells. Int Biodeterior Biodegradation 62:415–420Google Scholar
  15. Bauer J, Brandenburg K, Zahringer U, Rademann J (2006) Chemical synthesis of a glycolipid library by a solid-phase strategy allows elucidation of the structural specificity of immunostimulation by rhamnolipids. Chem Eur J 12:7116–7124PubMedGoogle Scholar
  16. Beal R, Betts WB (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol 89:158–168PubMedGoogle Scholar
  17. Benincasa M (2007) Rhamnolipid produced from agroindustrial wastes enhances hydrocarbon biodegradation in contaminated soil. Curr Microbiol 54:445–449PubMedGoogle Scholar
  18. Benincasa M, Contiero J, Manresa MA, Moraes IO (2002) Rhamnolipid production by Pseudomonas aeruginosa LBI growing on soapstock as the sole carbon source. J Food Eng 54:283–288Google Scholar
  19. Benincasa M, Abalos A, Oliveira I, Manresa A (2004) Chemical structure, surface properties and biological activities of the biosurfactant produced by Pseudomonas aeruginosa LBI from soapstock. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 85:1–8Google Scholar
  20. Bergström S, Theorell H, Davide H (1946a) On a metabolic product of Ps. pyocyania. Pyolipic acid active against M. tuberculosis. Arkiv Kemi Mineral Geol 23A:1–12Google Scholar
  21. Bergström S, Theorell H, Davide H (1946b) Pyolipic acid. A metabolic product of Pseudomonas pyocyanea active against Mycobacterium tuberculosis. Arch Biochem Biophys 10:165–166Google Scholar
  22. Bjarnsholt T, Givskov M (2007) The role of quorum sensing in the pathogenicity of the cunning aggressor Pseudomonas aeruginosa. Anal Bioanal Chem 387:409–414PubMedGoogle Scholar
  23. Bollinger N, Hassett DJ, Iglewski BH, Costerton JW, McDermott TR (2001) Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J Bacteriol 183:1990–1996PubMedGoogle Scholar
  24. Bredenbruch F, Nimtz M, Wray V, Morr M, Muller R, Häussler S (2005) Biosynthetic pathway of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines. J Bacteriol 187:3630–3635PubMedGoogle Scholar
  25. Bredenbruch F, Geffers R, Nimtz M, Buer J, Häussler S (2006) The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol 8:1318–1329PubMedGoogle Scholar
  26. Brencic A, Lory S (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72:612–632PubMedGoogle Scholar
  27. Burger MM, Glaser L, Burton RM (1963) The enzymatic synthesis of a rhamnose-containing glycolipid by extracts of Pseudomonas aeruginosa J. Biol Chem 238:2595–2602Google Scholar
  28. Burger MM, Glaser L, Burton RM, Elizabeth FN, Victor G (1966) Formation of rhamnolipids of Pseudomonas aeruginosa. Methods Enzymol, Marcel Dekker, Inc., New York 8:441–445Google Scholar
  29. 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 73:622–638PubMedGoogle Scholar
  30. Cabrera-Valladares N, Richardson AP, Olvera C, Trevino LG, Déziel E, Lépine F, Soberón-Chávez G (2006) Monorhamnolipids and 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs) production using Escherichia coli as a heterologous host. Appl Microbiol Biotechnol 73:187–194PubMedGoogle Scholar
  31. Caiazza NC, Shanks RMQ, O’Toole GA (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187:7351–7361PubMedGoogle Scholar
  32. Calfee MW, Coleman JP, Pesci EC (2001) Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 98:11633–11637PubMedGoogle Scholar
  33. Cameotra SS, Singh P (2009) Synthesis of rhamnolipid biosurfactant and mode of hexadecane uptake by Pseudomonas species. Microb Cell Fact 8:16PubMedGoogle Scholar
  34. Camilios Neto D, Meira JA, de Araujo JM, Mitchell DA, Krieger N (2008) Optimization of the production of rhamnolipids by Pseudomonas aeruginosa UFPEDA 614 in solid-state culture. Appl Microbiol Biotechnol 81:441–448PubMedGoogle Scholar
  35. Campos-Garcia J, Caro AD, Najera R, Miller-Maier RM, Al-Tahhan RA, Soberón-Chávez G (1998) The Pseudomonas aeruginosa rhlG gene encodes an NADPH-dependent beta-ketoacyl reductase which is specifically involved in rhamnolipid synthesis. J Bacteriol 180:4442–4451PubMedGoogle Scholar
  36. Carrillo PG, Mardaraz C, Pitta-Alvarez SI, Giulietti AM (1996) Isolation and selection of biosurfactant-producing bacteria. World J Microbiol Biotechnol 12:82–84Google Scholar
  37. Carty NL, Layland N, Colmer-Hamood JA, Calfee MW, Pesci EC, Hamood AN (2006) PtxR modulates the expression of QS-controlled virulence factors in the Pseudomonas aeruginosa strain PAO1. Mol Microbiol 61:782–794PubMedGoogle Scholar
  38. Celik GY, Aslim B, Beyatli Y (2008) Enhanced crude oil biodegradation and rhamnolipid production by Pseudomonas stutzeri strain G11 in the presence of Tween-80 and Triton X-100. J Environ Biol 29:867–870PubMedGoogle Scholar
  39. Cha M, Lee N, Kim M, Lee S (2008) Heterologous production of Pseudomonas aeruginosa EMS1 biosurfactant in Pseudomonas putida. Bioresour Technol 99:2192–2199PubMedGoogle Scholar
  40. Chandrasekaran EV, BeMiller JN (1980) In: Whistler RL (ed) Methods in carbohydrate chemistry. Academic press, New York, p 89Google Scholar
  41. Chang JS, Chou CL, Lin GH, Sheu SY, Chen WM (2005) Pseudoxanthomonas kaohsiungensis, sp nov., a novel bacterium isolated from oil-polluted site produces extracellular surface activity. Syst Appl Microbiol 28:137–144PubMedGoogle Scholar
  42. Chayabutra C, Wu J, Ju LK (2001) Rhamnolipid production by Pseudomonas aeruginosa under denitrification: effects of limiting nutrients and carbon substrates. Biotechnol Bioeng 72:25–33PubMedGoogle Scholar
  43. Chen G (2004) Rhamnolipid biosurfactant behavior in solutions. J Biomater Sci Polym Ed 15:229–235PubMedGoogle Scholar
  44. Chen SY, Lu WB, Wei YH, Chen WM, Chang JS (2007a) Improved production of biosurfactant with newly isolated Pseudomonas aeruginosa S2. Biotechnol Prog 23:661–666PubMedGoogle Scholar
  45. Chen SY, Wei YH, Chang JS (2007b) Repeated pH-stat fed-batch fermentation for rhamnolipid production with indigenous Pseudomonas aeruginosa S2. Appl Microbiol Biotechnol 76:67–74PubMedGoogle Scholar
  46. Cho YC, Ostrofsky EB, Rhee GY (2004) Effects of a rhamnolipid biosurfactant on the reductive dechlorination of polychlorinated biphenyls by St. Lawrence River (North America) microorganisms. Environ Toxicol Chem 23:1425–1430PubMedGoogle Scholar
  47. Christova N, Tuleva B, Lalchev Z, Jordanova A, Jordanov B (2004) Rhamnolipid biosurfactants produced by Renibacterium salmoninarum 27BN during growth on n-hexadecane. Z Naturforsch C 59:70–74PubMedGoogle Scholar
  48. Churchill SA, Griffin RA, Jones LP, Churchill PF (1995) Biodegradation rate enhancement of hydrocarbons by an oleophilic fertilizer and a rhamnolipid biosurfactant. J Environ Qual 24:19–28Google Scholar
  49. Cohen R, Exerowa D (2007) Surface forces and properties of foam films from rhamnolipid biosurfactants. Adv Colloid Interface Sci 134–135:24–34PubMedGoogle Scholar
  50. Cohen R, Exerowa D, Pigov I, Heckmann R, Lang S (2004) DLVO and non-DLVO forces in thin liquid films from rhamnolipids. J Adhes 80:875–894Google Scholar
  51. Cosson P, Zulianello L, Join-Lambert O, Faurisson F, Gebbie L, Benghezal M, van Delden C, Curty LK, Köhler T (2002) Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J Bacteriol 184:3027–3033PubMedGoogle Scholar
  52. De Jonghe K, De Dobbelaere I, Sarrazyn R, Hofte M (2005) Control of Phytophthora cryptogea in the hydroponic forcing of witloof chicory with the rhamnolipid-based biosurfactant formulation PRO1. Plant Pathol 54:219–226Google Scholar
  53. Dekimpe V, Déziel E (2009) Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155:712–723PubMedGoogle Scholar
  54. deKoster CG, Vos B, Versluis C, Heerma W, Haverkamp J (1994) High-performance thin-layer chromatography/fast atom bombardment (tandem) mass spectrometry of Pseudomonas rhamnolipids. Biol Mass Spectrom 23:179–185Google Scholar
  55. Déziel E, Paquette G, Villemur R, Lépine F, Bisaillon JG (1996) Biosurfactant production by a soil Pseudomonas strain growing on polycyclic aromatic hydrocarbons. Appl Environ Microbiol 62:1908–1912PubMedGoogle Scholar
  56. Déziel E, Comeau Y, Villemur R (1999a) Two-liquid-phase bioreactors for enhanced degradation of hydrophobic/toxic compounds. Biodegradation 10:219–233PubMedGoogle Scholar
  57. Déziel E, Lépine F, Dennie D, Boismenu D, Mamer OA, Villemur R (1999b) Liquid chromatography/mass spectrometry analysis of mixtures of rhamnolipids produced by Pseudomonas aeruginosa strain 57RP grown on mannitol or naphthalene. Biochim Biophys Acta/Mol Cell Biol Lipids 1440:244–252Google Scholar
  58. Déziel E, Lépine F, Milot S, Villemur R (2000) Mass spectrometry monitoring of rhamnolipids from a growing culture of Pseudomonas aeruginosa strain 57RP. Biochim Biophys Acta/Mol Cell Biol Lipids 1485:145–152Google Scholar
  59. 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 149:2005–2013PubMedGoogle Scholar
  60. Déziel E, Lépine F, Milot S, He J, Mindrinos MN, Tompkins RG, Rahme LG (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci USA 101:1339–1344PubMedGoogle Scholar
  61. Déziel E, Gopalan S, Tampakaki AP, Lépine F, Padfield KE, Saucier M, Xiao GP, Rahme LG (2005) The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol 55:998–1014PubMedGoogle Scholar
  62. Diggle SP, Winzer K, Lazdunski A, Williams P, Camara M (2002) Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J Bacteriol 184:2576–2586PubMedGoogle Scholar
  63. Diggle SP, Winzer K, Chhabra SR, Worrall KE, Camara M, 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 50:29–43PubMedGoogle Scholar
  64. Dong YH, Zhang XF, Xu JL, Tan AT, Zhang LH (2005) VqsM, a novel AraC-type global regulator of quorum-sensing signalling and virulence in Pseudomonas aeruginosa. Mol Microbiol 58:552–564PubMedGoogle Scholar
  65. Duan K, Surette MG (2007) Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems. J Bacteriol 189:4827–4836PubMedGoogle Scholar
  66. Dubeau D, Déziel E, Woods D, Lépine F (2009) Burkholderia thailandensis harbors two identical rhl gene clusters responsible for the biosynthesis of rhamnolipids. BMC Microbiol 9:263PubMedGoogle Scholar
  67. Dubern JF, Diggle SP (2008) Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol Biosyst 4:882–888PubMedGoogle Scholar
  68. Dubey KV, Juwarkar AA, Singh SK (2005) Adsorption-desorption process using wood-based activated carbon for recovery of biosurfactant from fermented distillery wastewater. Biotechnol Prog 21:860–867PubMedGoogle Scholar
  69. Duynstee HI, van Vliet MJ, van der Marel GA, van Boom JH (1998) An efficient synthesis of (R)-3-{(R)-3-[2-O-(a-L-rhamnopyranosyl)-a-L-rhamnopyranosyl] oxydecanoyl}oxydecanoic acid, a rhamnolipid from Pseudomonas aeruginosa. Eur J Org Chem 1998:303–307Google Scholar
  70. Edwards JR, Hayashi JA (1965) Structure of a rhamnolipid from Pseudomonas aeruginosa. Arch Biochem Biophys 111:415–421PubMedGoogle Scholar
  71. Farrow JM, Sund ZM, Ellison ML, Wade DS, Coleman JP, Pesci EC (2008) PqsE functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol 190:7043–7051PubMedGoogle Scholar
  72. Fujita K, Akino T, Yoshioka H (1988) Characteristics of the heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun 56:1385–1387PubMedGoogle Scholar
  73. Fuqua C, Greenberg EP (2002) Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695PubMedGoogle Scholar
  74. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275PubMedGoogle Scholar
  75. Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184:6472–6480PubMedGoogle Scholar
  76. Gartshore J, Lim YC, Cooper DG (2000) Quantitative analysis of biosurfactants using Fourier Transform Infrared (FT-IR) spectroscopy. Biotechnol Lett 22:169–172Google Scholar
  77. Giani C, Wullbrandt D, Rothert R, Meiwes J (1997) Pseudomonas aeruginosa and its use in a process for the biotechnological preparation of L-Rhamnose Hoechst Aktiengesellschaft. Frankfurt am Main, Germany, p 10Google Scholar
  78. Glaser L, Kornfeld S (1961) The enzymatic synthesis of thymidine-linked sugars. II- Thymidine diphosphate L-rhamnose. J Biol Chem 236:1795–1799PubMedGoogle Scholar
  79. Glick R, Gilmour C, Tremblay J, Satanower S, Avidan O, Déziel E, Greenberg EP, Poole K, Banin E (2010) Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 192:2973–2980PubMedGoogle Scholar
  80. Gross H, Loper JE (2009) Genomics of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26:1408–1446PubMedGoogle Scholar
  81. Gruber T (1991) Verfahrenstechnische aspekte der kontinuierlichen produktion von biotensiden am beispiel der rhamnolipide Lehrstuhl für Bioprozesstechnik der Universität Stuttgart. Universität Stuttgart, Stuttgart, p 121Google Scholar
  82. Guerra-Santos L (1985) Physiology of Pseudomonas aeruginosa biosurfactant production in continuous culture Institute of Biotechnology. Swiss Federal Institute of Technology, ZürichGoogle Scholar
  83. Guerra-Santos L, Käppeli O, Fiechter A (1984) Pseudomonas aeruginosa biosurfactant production in continuous culture with glucose as carbon source. Appl Environ Microbiol 48:301–305PubMedGoogle Scholar
  84. Guerra-Santos LH, Käppeli O, Fiechter A (1986) Dependence of Pseudomonas aeruginosa continous culture biosurfactant production on nutritional and environmental factors. Appl Microbiol Biotechnol 24:443–448Google Scholar
  85. Gunther NW, Nunez A, Fett W, Solaiman DKY (2005) Production of rhamnolipids by Pseudomonas chlororaphis, a nonpathogenic bacterium. Appl Environ Microbiol 71:2288–2293PubMedGoogle Scholar
  86. Gunther NW, Nunez A, Fortis L, Solaiman DKY (2006) Proteomic based investigation of rhamnolipid production by Pseudomonas chlororaphis strain NRRL B-30761. J Ind Microbiol Biotechnol 33:914–920PubMedGoogle Scholar
  87. Gupta R, Gobble TR, Schuster M (2009) GidA posttranscriptionally regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 191:5785–5792PubMedGoogle Scholar
  88. Haba E, Espuny MJ, Busquets M, Manresa A (2000) Screening and production of rhamnolipids by Pseudomonas aeruginosa 47T2 NCIB 40044 from waste frying oils. J Appl Microbiol 88:379–387PubMedGoogle Scholar
  89. Haba E, Abalos A, Jauregui O, Espuny MJ, Manresa A (2003a) Use of liquid chromatography-mass spectroscopy for studying the composition and properties of rhamnolipids produced by different strains of Pseudomonas aeruginosa. J Surfactants Deterg 6:155–161Google Scholar
  90. Haba E, Pinazo A, Jauregui O, Espuny MJ, Infante MR, Manresa A (2003b) Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotechnol Bioeng 81:316–322PubMedGoogle Scholar
  91. Haferburg D, Hommel R, Kleber H-P, Kluge S, Schuster G, Zschiegner H-J (1987) Antiphytovirale aktivität von rhamnolipid aus Pseudomonas aeruginosa. Acta Biotechnol 7:353–356Google Scholar
  92. Hansen J, Accorsini FR, Benincasa M (2008) Physicochemical properties of a biosurfactant produced from agroindustrial wastes. Int Biodeterior Biodegradation 62:15–16Google Scholar
  93. Hauser G, Karnovsky ML (1954) Studies on the production of glycolipide by Pseudomonas aeruginosa. J Bacteriol 68:645–654PubMedGoogle Scholar
  94. Hauser G, Karnovsky ML (1957) Rhamnose and rhamnolipid biosynthesis by Pseudomonas aeruginosa. J Biol Chem 224:91–105PubMedGoogle Scholar
  95. Hauser G, Karnovsky ML (1958) Studies on the biosynthesis of L-rhamnose. J Biol Chem 233:287–291PubMedGoogle Scholar
  96. Häussler S, Nimtz M, Domke T, Wray V, Steinmetz I (1998) Purification and characterization of a cytotoxic exolipid of Burkholderia pseudomallei. Infect Immun 66:1588–1593PubMedGoogle Scholar
  97. Häussler S, Rohde M, von Neuhoff N, Nimtz M, Steinmetz I (2003) Structural and functional cellular changes induced by Burkholderia pseudomallei rhamnolipid. Infect Immun 71:2970–2975PubMedGoogle Scholar
  98. Helbert JR, Brown KD (1957) Color reaction of anthrone with monosaccharide mixtures and oligo- and polysaccharides containing hexuronic acids. Anal Chem 29:1464–1466Google Scholar
  99. Hembach T (1994) Untersuchungen zur mikrobiellen Umsetzung von Maiskeimöl zu Rhamnolipid Fakultät I Allgemeine und angewandte Naturwissenschaften der Universität Hohenheim. Universität Hohenheim, Stuttgart, p 105Google Scholar
  100. Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, Singer D, Camara M, Williams P, Haas D (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186:2936–2945PubMedGoogle Scholar
  101. Heyd M, Kohnert A, Tan TH, Nusser M, Kirschhofer F, Brenner-Weiss G, Franzreb M, Berensmeier S (2008) Development and trends of biosurfactant analysis and purification using rhamnolipids as an example. Anal Bioanal Chem 391:1579–1590PubMedGoogle Scholar
  102. Hirayama T, Kato I (1982) Novel methyl rhamnolipids from Pseudomonas aeruginosa. FEBS Lett 139:81–85Google Scholar
  103. Hoang TT, Schweizer HP (1997) Fatty acid biosynthesis in Pseudomonas aeruginosa: cloning and characterization of the fabAB operon encoding beta-hydroxyacyl-acyl carrier protein dehydratase (FabA) and beta-ketoacyl-acyl carrier protein synthase I (FabB). J Bacteriol 179:5326–5332PubMedGoogle Scholar
  104. Hoang TT, Schweizer HP (1999) Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis. J Bacteriol 181:5489–5497PubMedGoogle Scholar
  105. Hodge JE, Hofreiter BT (1962) In: Whistler RL, Wolfrom ML (eds) Methods in carbohydrate chemistry. Academic press, New York, p 380Google Scholar
  106. Hommel RK, Ratledge C (1993) Biosynthetic mechanisms of low molecular weight surfactants and their precursors molecules. In: Kosaric N (ed) Surfactant science series – Biosurfactants: production, properties, application. Marcel Dekker, New YorkGoogle Scholar
  107. Howe J, Bauer J, Andra J, Schromm AB, Ernst M, Rossle M, Zahringer U, Rademann J, Brandenburg K (2006) Biophysical characterization of synthetic rhamnolipids. FEBS J 273:5101–5112PubMedGoogle Scholar
  108. Jain DK, Collins-Thompson DL, Lee H, Trevors JT (1991) A drop-collapsing test for screening surfactant-producing microorganisms. J Microbiol Meth 13:271–279Google Scholar
  109. Jarvis FG, Johnson MJ (1949) A glyco-lipide produced by Pseudomonas aeruginosa. J Am Chem Soc 71:4124–4126Google Scholar
  110. Jensen V, Lons D, Zaoui C, Bredenbruch F, Meissner A, Dieterich G, Munch R, Häussler S (2006) RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J Bacteriol 188:8601–8606PubMedGoogle Scholar
  111. Jensen PO, Bjarnsholt T, Phipps R, Rasmussen TB, Calum H, Christoffersen L, Moser C, Williams P, Pressler T, Givskov M, Hoiby N (2007) Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153:1329–1338PubMedGoogle Scholar
  112. Johnson MK, Boese-Marrazzo D (1980) Production and properties of heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun 29:1028–1033PubMedGoogle Scholar
  113. Jude F, Kohler T, Branny P, Perron K, Mayer MP, Comte R, van Delden C (2003) Posttranscriptional control of quorum-sensing-dependent virulence genes by DksA in Pseudomonas aeruginosa. J Bacteriol 185:3558–3566PubMedGoogle Scholar
  114. Juhas M, Wiehlmann L, Huber B, Jordan D, Lauber J, Salunkhe P, Limpert AS, von Gotz F, Steinmetz I, Eberl L, Tummler B (2004) Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150:831–841PubMedGoogle Scholar
  115. Kim BS, Lee JY, Hwang BK (2000) In vivo control and in vitro antifungal activity of rhamnolipid B, a glycolipid antibiotic, against Phytophthora capsici and Colletotrichum orbiculare. Pest Manage Sci 56:1029–1035Google Scholar
  116. Kim EJ, Wang W, Deckwer WD, Zeng AP (2005) Expression of the quorum-sensing regulatory protein LasR is strongly affected by iron and oxygen concentrations in cultures of Pseudomonas aeruginosa irrespective of cell density. Microbiology 151:1127–1138PubMedGoogle Scholar
  117. Koch AK, Käppeli O, Fiechter A, Reiser J (1991) Hydrocarbon assimilation and biosurfactant production in Pseudomonas aeruginosa mutants. J Bacteriol 173:4212–4219PubMedGoogle Scholar
  118. 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 182:5990–5996PubMedGoogle Scholar
  119. Kurioka S, Liu PV (1967) Effect of the hemolysin of Pseudomonas aeruginosa on phosphatides and on phospholipase C activity. J Bacteriol 93:670–674PubMedGoogle Scholar
  120. Lang S, Katsiwela E, Wagner F (1989) Antimicrobial effects of biosurfactants. Fat Sci Technol 91:363–366Google Scholar
  121. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A (1996) A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21:1137–1146PubMedGoogle Scholar
  122. Lazdunski AM, Ventre I, Sturgis JN (2004) Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 2:581–592PubMedGoogle Scholar
  123. Lee KM, Hwang SH, Ha SD, Jang JH, Lim DJ, Kong JY (2004) Rhamnolipid production in batch and fed-batch fermentation using Pseudomonas aeruginosa BYK-2 KCTC 18012P. Biotechnol Bioprocess Eng 9:267–273Google Scholar
  124. Lee M, Kim MK, Vancanneyt M, Swings J, Kim SH, Kang MS, Lee ST (2005) Tetragenococcus koreensis sp. nov., a novel rhamnolipid-producing bacterium. Int J Syst Evol Microbiol 55:1409–1413PubMedGoogle Scholar
  125. Lépine F, Déziel E, Milot S, Villemur R (2002) Liquid chromatographic/mass spectrometric detection of the 3-(3-hydroxyalkanoyloxy)alkanoic acid precursors of rhamnolipids in Pseudomonas aeruginosa cultures. J Mass Spectrom 37:41–46PubMedGoogle Scholar
  126. Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188:3365–3370PubMedGoogle Scholar
  127. Lindhout T, Lau PC, Brewer D, Lam JS (2009) Truncation in the core oligosaccharide of lipopolysaccharide affects flagella-mediated motility in Pseudomonas aeruginosa PAO1 via modulation of cell surface attachment. Microbiology 155:3449–3460PubMedGoogle Scholar
  128. Linhardt RJ, Bakhit R, Daniels L, Mayerl F, Pickenhagen W (1989) Microbially produced rhamnolipid as a source of rhamnose. Biotechnol Bioeng 33:365–368PubMedGoogle Scholar
  129. Madison LL, Huisman GW (1999) Metabolic engineering of poly(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63:21–53PubMedGoogle Scholar
  130. Manresa MA, Bastida J, Mercade ME, Robert M, Deandres C, Espuny MJ, Guinea J (1991) Kinetic-studies on surfactant production by Pseudomonas aeruginosa-44T1. J Ind Microbiol 8:133–136Google Scholar
  131. Martinez-Toledo A, Rios-Leal E, Vazquez-Duhalt R, Gonzalez-Chavez Mdel C, Esparza-Garcia JF, Rodriguez-Vazquez R (2006) Role of phenanthrene in rhamnolipid production by P. putida in different media. Environ Technol 27:137–142PubMedGoogle Scholar
  132. Mata-Sandoval JC, Karns J, Torrents A (1999) High-performance liquid chromatography method for the characterization of rhamnolipid mixtures produced by Pseudomonas aeruginosa UG2 on corn oil. J Chromatogr A 864:211–220PubMedGoogle Scholar
  133. Matsufuji M, Nakata K, Yoshimoto A (1997) High production of rhamnolipids by Pseudomonas aeruginosa growing on ethanol. Biotechnol Lett 19:1213–1215Google Scholar
  134. Mechaly A, Belakhov V, Shoham Y, Baasov T (1997) An efficient chemical-enzymatic synthesis of 4-nitrophenyl [beta]-xylobioside: a chromogenic substrate for xylanases. Carbohydr Res 304:111–115Google Scholar
  135. Medina G, Juarez K, Diaz R, Soberón-Chávez G (2003a) Transcriptional regulation of Pseudomonas aeruginosa rhlR, encoding a quorum-sensing regulatory protein. Microbiology 149:3073–3081PubMedGoogle Scholar
  136. Medina G, Juarez K, Soberón-Chávez G (2003b) 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 185:377–380PubMedGoogle Scholar
  137. Medina G, Juarez K, Valderrama B, Soberón-Chávez G (2003c) Mechanism of Pseudomonas aeruginosa RhlR transcriptional regulation of the rhlAB promoter. J Bacteriol 185:5976–5983PubMedGoogle Scholar
  138. Mercade ME, Manresa MA, Robert M, Espuny MJ, Deandres C, Guinea J (1993) Olive oil mill effluent (OOME) – new substrate for biosurfactant production. Bioresour Technol 43:1–6Google Scholar
  139. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199PubMedGoogle Scholar
  140. Miller DJ, Zhang YM, Rock CO, White SW (2006) Structure of RhlG, an essential beta-ketoacyl reductase in the rhamnolipid biosynthetic pathway of Pseudomonas aeruginosa. J Biol Chem 281:18025–18032PubMedGoogle Scholar
  141. Monteiro SA, Sassaki GL, de Souza LM, Meira JA, de Araujo JM, Mitchell DA, Ramos LP, Krieger N (2007) Molecular and structural characterization of the biosurfactant produced by Pseudomonas aeruginosa DAUPE 614. Chem Phys Lipids 147:1–13PubMedGoogle Scholar
  142. Morici LA, Carterson AJ, Wagner VE, Frisk A, Schurr JR, Bentrup KHZ, Hassett DJ, Iglewski BH, Sauer K, Schurr MJ (2007) Pseudomonas aeruginosa AlgR represses the Rhl quorum-sensing system in a biofilm-specific manner. J Bacteriol 189:7752–7764PubMedGoogle Scholar
  143. Morikawa M, Hirata Y, Imanaka T (2000) A study on the structure-function relationship of lipopeptide biosurfactants. Biochim Biophys Acta/Mol Cell Biol Lipids 1488:211–218Google Scholar
  144. Müller MM, Hörmann B, Syldatk C, Hausmann R (2010) Pseudomonas aeruginosa PAO1 as a model for rhamnolipid production in bioreactor systems. Appl Microbiol Biotechnol 87(1):167–174PubMedGoogle Scholar
  145. Mulligan CN, Gibbs BF (1989) Correlation of nitrogen metabolism with biosurfactant production by Pseudomonas aeruginosa. Appl Environ Microbiol 55:3016–3019PubMedGoogle Scholar
  146. Mulligan CN, Gibbs BF (1990) Recovery of biosurfactants by ultrafiltration. J Chem Technol Biotechnol 47:23–29PubMedGoogle Scholar
  147. Mulligan C, Gibbs B (1993) Factors influencing the economics of biosurfactants. In: Kosaric N (ed) Biosurfactants: production, properties, applications. Marcel Dekker, NY, pp 329–371Google Scholar
  148. Nayak AS, Vijaykumar MH, Karegoudar TB (2009) Characterization of biosurfactant produced by Pseudoxanthomonas sp PNK-04 and its application in bioremediation. Int Biodeterior Biodegradation 63:73–79Google Scholar
  149. Nguyen TT, Sabatini DA (2009) Formulating alcohol-free microemulsions using rhamnolipid biosurfactant and rhamnolipid mixtures. J Surfactants Deterg 12:109–115Google Scholar
  150. Nielsen C, Stanghellini M, Ferrin D (2005) Efficacy of rhamnolipid and saponin biosurfactants in the management of Phytophthora root rot of pepper in a recirculating cultural system. Phytopathology 95:S75Google Scholar
  151. Nielsen CJ, Ferrin DM, Stanghellini ME (2006) Efficacy of biosurfactants in the management of Phytophthora capsici on pepper in recirculating hydroponic systems. Can J Plant Pathol 28:450–460Google Scholar
  152. Nitschke M, Costa S, Contiero J (2005) Rhamnolipid surfactants: an update on the general aspects of these remarkable biomolecules. Biotechnol Prog 21:1593–1600PubMedGoogle Scholar
  153. Noordman WH, Brusseau ML, Janssen DB (2000) Adsorption of a multicomponent rhamnolipid surfactant to soil. Environ Sci Technol 34:832–838Google Scholar
  154. Ochoa-Loza FJ, Artiola JF, Maier RM (2001) Stability constants for the complexation of various metals with a rhamnolipid biosurfactant. J Environ Qual 30:479–485PubMedGoogle Scholar
  155. Ochsner UA, Reiser J (1995) Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92:6424–6428PubMedGoogle Scholar
  156. Ochsner UA, Fiechter A, 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 269:19787–19795PubMedGoogle Scholar
  157. Ochsner UA, Koch A, Fiechter A, Reiser J (1994b) Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol 176:2044–2054PubMedGoogle Scholar
  158. Ochsner UA, Reiser J, Fiechter A, Witholt B (1995) Production of Pseudomonas aeruginosa rhamnolipid biosurfactants in heterologous hosts. Appl Environ Microbiol 61:3503–3506PubMedGoogle Scholar
  159. Ochsner UA, Hembach T, Fiechter A (1996) Production of rhamnolipid biosurfactants. Adv Biochem Eng Biotechnol 53:89–118PubMedGoogle Scholar
  160. Oliveira FJS, Vazquez L, de Campos NP, de Franca FP (2009) Production of rhamnolipids by a Pseudomonas alcaligenes strain. Process Biochem 44:383–389Google Scholar
  161. Olvera C, Goldberg JB, Sanchez R, Soberón-Chávez G (1999) The Pseudomonas aeruginosa algC gene product participates in rhamnolipid biosynthesis. FEMS Microbiol Lett 179:85–90PubMedGoogle Scholar
  162. Onbasli D, Aslim B (2008) Determination of antimicrobial activity and production of some metabolites by Pseudomonas aeruginosa B1 and B2 in sugar beet molasses. Afr J Biotechnol 7:4614–4619Google Scholar
  163. Onbasli D, Aslim B (2009) Biosurfactant production in sugar beet molasses by some Pseudomonas spp. J Environ Biol 30:161–163PubMedGoogle Scholar
  164. Ozdemir G, Malayoglu U (2004) Wetting characteristics of aqueous rhamnolipids solutions. Colloids Surf B Biointerfaces 39:1–7PubMedGoogle Scholar
  165. Ozdemir G, Peker S, Helvaci SS (2004) Effect of pH on the surface and interfacial behavior of rhamnolipids R1 and R2. Colloids Surf A Physicochem Eng Asp 234:135–143Google Scholar
  166. Pajarron AM, Dekoster CG, Heerma W, Schmidt M, Haverkamp J (1993) Structure identification of natural rhamnolipid mixtures by fast-atom-bombardment tandem mass-spectrometry. Glycoconj J 10:219–226Google Scholar
  167. Palanisamy P, Raichur AM (2009) Synthesis of spherical NiO nanoparticles through a novel biosurfactant mediated emulsion technique. Mater Sci Eng C Biomim Supramol Syst 29:199–204Google Scholar
  168. Pearson JP, Pesci EC, Iglewski BH (1997) Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767PubMedGoogle Scholar
  169. Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132PubMedGoogle Scholar
  170. Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:11229–11234PubMedGoogle Scholar
  171. Pham TH, Webb JS, Rehm BHA (2004) The role of polyhydroxyalkanoate biosynthesis by Pseudomonas aeruginosa in rhamnolipid and alginate production as well as stress tolerance and biofilm formation. Microbiology 150:3405–3413PubMedGoogle Scholar
  172. Piljac A, Stipcevic T, Piljac-Zegarac J, Piljac G (2008) Successful treatment of chronic decubitus ulcer with 0.1% dirhamnolipid ointment. J Cutan Med Surg 12:142–146PubMedGoogle Scholar
  173. Pinzon N, Ju L-K (2009a) Improved detection of rhamnolipid production using agar plates containing methylene blue and cetyl trimethylammonium bromide. Biotechnol Lett 31:1583–1588PubMedGoogle Scholar
  174. Pinzon NM, Ju LK (2009b) Analysis of rhamnolipid biosurfactants by methylene blue complexation. Appl Microbiol Biotechnol 82:975–981PubMedGoogle Scholar
  175. Pornsunthorntawee O, Chavadej S, Rujiravanit R (2009) Solution properties and vesicle formation of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa SP4. Colloids Surf B Biointerfaces 72:6–15PubMedGoogle Scholar
  176. Potvin E, Sanschagrin F, Levesque RC (2008) Sigma factors in Pseudomonas aeruginosa. FEMS Microbiol Rev 32:38–55PubMedGoogle Scholar
  177. Price NPJ, Ray KJ, Vermillion K, Kuo TM (2009) MALDI-TOF mass spectrometry of naturally occurring mixtures of monorhamnolipids and dirhamnolipids. Carbohydr Res 344:204–209PubMedGoogle Scholar
  178. Rahim R, Burrows LL, Monteiro MA, Perry MB, Lam JS (2000) Involvement of the rml locus in core oligosaccharide and O polysaccharide assembly in Pseudomonas aeruginosa. Microbiology 146:2803–2814PubMedGoogle Scholar
  179. 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 40:708–718PubMedGoogle Scholar
  180. Rahman KSM, Rahman TJ, McClean S, Marchant R, Banat IM (2002) Rhamnolipid biosurfactant production by strains of Pseudomonas aeruginosa using low-cost raw materials. Biotechnol Prog 18:1277–1281PubMedGoogle Scholar
  181. Raichur AM (2007) Dispersion of colloidal alumina using a rhamnolipid biosurfactant. J Dispersion Sci Technol 28:1272–1277Google Scholar
  182. Ramana KV, Charyulu NCLN, Karanth NG (1991) A mathematical model for the production of biosurfactants by Pseudomonas aeuginosa CFTR-6: production of biomass. J Chem Technol Biotechnol 51:525–538Google Scholar
  183. Rampioni G, Schuster M, Greenberg EP, Zennaro E, Leoni L (2009) Contribution of the RsaL global regulator to Pseudomonas aeruginosa virulence and biofilm formation. FEMS Microbiol Lett 301:210–217PubMedGoogle Scholar
  184. Rehm BHA, Kruger N, Steinbuchel A (1998) A new metabolic link between fatty acid de novo synthesis and polyhydroxyalkanoic acid synthesis – the phaG gene from Pseudomonas putida KT2440 encodes a 3-hydroxyacyl-acyl carrier protein coenzyme A transferase. J Biol Chem 273:24044–24051PubMedGoogle Scholar
  185. Rehm BHA, Mitsky TA, Steinbuchel A (2001) Role of fatty acid de novo biosynthesis in polyhydroxyalkanoic acid (PHA) and rhamnolipid synthesis by pseudomonads: establishment of the transacylase (PhaG)-mediated pathway for PHA biosynthesis in Escherichia coli. Appl Environ Microbiol 67:3102–3109PubMedGoogle Scholar
  186. Reiling HE, Thanei-Wyss U, Guerra-Santos LH, Hirt R, Kappeli O, Fiechter A (1986) Pilot plant production of rhamnolipid biosurfactant by Pseudomonas aeruginosa. Appl Environ Microbiol 51:985–989PubMedGoogle Scholar
  187. Remichkova M, Galabova D, Roeva I, Karpenko E, Shulga A, Galabov AS (2008) Anti-herpesvirus activities of Pseudomonas sp S-17 rhamnolipid and its complex with alginate. Z Naturforsch C 63:75–81PubMedGoogle Scholar
  188. Rendell NB, Taylor GW, Somerville M, Todd H, Wilson R, Cole PJ (1990) Characterization of Pseudomonas rhamnolipids. Biochim Biophys Acta 1045:189–193PubMedGoogle Scholar
  189. Ritter C, Luckner M (1971) Biosynthesis of 2-n-alkyl-4-hydroxyquinoline derivatives (pseudane) in Pseudomonas aeruginosa. Eur J Biochem 18:391–400PubMedGoogle Scholar
  190. Robertson BD, Frosch M, van Putten JP (1994) The identification of cryptic rhamnose biosynthesis genes in Neisseria gonorrhoeae and their relationship to lipopolysaccharide biosynthesis. J Bacteriol 176:6915–6920PubMedGoogle Scholar
  191. Rooney AP, Price NP, Ray KJ, Kuo TM (2009) Isolation and characterization of rhamnolipid-producing bacterial strains from a biodiesel facility. FEMS Microbiol Lett 295:82–87PubMedGoogle Scholar
  192. Santa Anna LM, Sebastian GV, Menezes EP, Alves TLM, Santos AS, Pereira N, Freire DMG (2002) Production of biosurfactants from Pseudomonas aeruginosa PA1 isolated in oil environments. Braz J Chem Eng 19:159–166Google Scholar
  193. Sarachat T, Pornsunthorntawee O, Chavadej S, Rujiravanit R (2010) Purification and concentration of a rhamnolipid biosurfactant produced by Pseudomonas aeruginosa SP4 using foam fractionation. Bioresour Technol 101:324–330PubMedGoogle Scholar
  194. Schaefer AL, Val DL, Hanzelka BL, Cronan JE Jr, Greenberg EP (1996) Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc Natl Acad Sci USA 93:9505–9509PubMedGoogle Scholar
  195. Schenk T, Schuphan I, Schmidt B (1995) High-performance liquid-chromatographic determination of the rhamnolipids produced by Pseudomonas aeruginosa. J Chromatogr A 693:7–13PubMedGoogle Scholar
  196. Schenk T, Breitschwerdt A, Kessels G, Schuphan I, Schmidt B (1997) A biosynthetic route to [C-14]-labelled rhamnolipids. J Labelled Comp Radiopharm 39:705–710Google Scholar
  197. Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079PubMedGoogle Scholar
  198. Shen W, Zhao JF, Ai FX, Tuoheti S, Yang SL (2009) Components, structure and antimicrobial activity of metabolite of Pseudonomas sp. BS-03. Nanjing Li Gong Daxue Xuebao/J Nanjing Univ Sci Technol 33:814–819Google Scholar
  199. Siegmund I, Wagner F (1991) New method for detecting rhamnolipids excreted by Pseudomonas species during growth on mineral agar. Biotechnol Tech 5:265–268Google Scholar
  200. Siemann M, Wagner F (1993) Prospects and limits for the production of biosurfactants using immobilized biocatalysts. In: Kosaric N (ed) Surfactant science series – Biosurfactants. Marcel Dekker, New York, 48:99–133Google Scholar
  201. Sierra G (1960) Hemolytic effect of a glycolipid produced by Pseudomonas aeruginosa. Antonie Leeuwenhoek 26:189–192PubMedGoogle Scholar
  202. Sim L, Ward OP, Li ZY (1997) Production and characterisation of a biosurfactant isolated from Pseudomonas aeruginosa UW-1. J Ind Microbiol Biotechnol 19:232–238PubMedGoogle Scholar
  203. Singh A, Van Hamme JD, Ward OP (2007) Surfactants in microbiology and biotechnology: Part 2. Application aspects. Biotechnol Adv 25:99–121PubMedGoogle Scholar
  204. Soberón-Chávez G (2004) Biosynthesis of rhamnolipids. In: Ramos J-L (ed) Pseudomonas. Kluwer/Plenum, New York, pp 173–189Google Scholar
  205. Soberón-Chávez G, Lépine F, Déziel E (2005) Production of rhamnolipids by Pseudomonas aeruginosa. Appl Microbiol Biotechnol 68:718–725PubMedGoogle Scholar
  206. Sotirova AV, Spasova DI, Galabova DN, Karpenko E, Shulga A (2008) Rhamnolipid-biosurfactant permeabilizing effects on gram-positive and gram-negative bacterial strains. Curr Microbiol 56:639–644PubMedGoogle Scholar
  207. Sotirova A, Spasova D, Vasileva-Tonkova E, Galabova D (2009) Effects of rhamnolipid-biosurfactant on cell surface of Pseudomonas aeruginosa. Microbiol Res 164:297–303PubMedGoogle Scholar
  208. Southard WH, Hayashi JA, Barkulis SS (1959) Studies of streptococcal cell walls. IV. The conversion of D-glucose to cell wall L-rhamnose. J Bacteriol 78:79–81PubMedGoogle Scholar
  209. Stipcevic T, Pijac A, Pijac G (2006) Enhanced healing of full-thickness burn wounds using di-rhamnolipid. Burns 32:24–34PubMedGoogle Scholar
  210. Syldatk C, Wagner F (1987) Production of biosurfactants. In: Kosaric N, Cairns WL, Gray NCC (eds) Biosurfactants and biotechnology. Marcel Dekker, New York, pp 89–120Google Scholar
  211. Syldatk C, Matulovic U, Wagner F (1984) Biotenside – Neue Verfahren zur mikrobiellen Herstellung grenzflächenaktiver, anionischer Glykolipide. Biotech-Forum 1:58–66Google Scholar
  212. Syldatk C, Lang S, Matulovic U, Wagner F (1985) Production of four interfacial active rhamnolipids from n-alkanes or glycerol by resting cells of Pseudomonas species DSM 2874. Z Naturforsch C 40:61–67PubMedGoogle Scholar
  213. Timm A, Steinbuchel A (1990) Formation of polyesters consisting of medium-chain-length 3-hydroxyalkanoic acids from gluconate by Pseudomonas aeruginosa and other fluorescent pseudomonads. Appl Environ Microbiol 56:3360–3367PubMedGoogle Scholar
  214. Totten PA, Lara JC, Lory S (1990) The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J Bacteriol 172:389–396PubMedGoogle Scholar
  215. Tremblay J, Richardson AP, Lépine F, Déziel E (2007) Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour. Environ Microbiol 9:2622–2630PubMedGoogle Scholar
  216. Tripathy SS, Raichur AM (2008) Dispersibility of barium titanate suspension in the presence of polyelectrolytes: a review. J Dispersion Sci Technol 29:230–239Google Scholar
  217. Trummler K, Effenberger F, Syldatk C (2003) An integrated microbial/enzymatic process for production of rhamnolipids and L-(+)-rhamnose from rapeseed oil with Pseudomonas sp DSM 2874. Eur J Lipid Sci Technol 105:563–571Google Scholar
  218. Tuleva BK, Ivanov GR, Christova NE (2002) Biosurfactant production by a new Pseudomonas putida strain. Z Naturforsch C 57:356–360PubMedGoogle Scholar
  219. Van Alst NE, Picardo KF, Iglewski BH, Haidaris CG (2007) Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infect Immun 75:3780–3790PubMedGoogle Scholar
  220. Van Dyke MI, Couture P, Brauer M, Lee H, Trevors JT (1993) Pseudomonas aeruginosa UG2 rhamnolipid biosurfactants: structural characterization and their use in removing hydrophobic compounds from soil. Can J Microbiol 39:1071–1078PubMedGoogle Scholar
  221. Van Gennip M, Christensen LD, Alhede M, Phipps R, Jensen PO, Christophersen L, Pamp SJ, Moser C, Mikkelsen PJ, Koh AY, Tolker-Nielsen T, Pier GB, Hoiby N, Givskov M, Bjarnsholt T (2009) Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes. APMIS 117:537–546PubMedGoogle Scholar
  222. Van Hamme JD, Singh A, Ward OP (2006) Physiological aspects – Part 1 in a series of papers devoted to surfactants in microbiology and biotechnology. Biotechnol Adv 24:604–620PubMedGoogle Scholar
  223. Vasileva-Tonkova E, Gesheva V (2005) Glycolipids produced by Antarctic Nocardioides sp during growth on n-paraffin. Process Biochem 40:2387–2391Google Scholar
  224. Vasileva-Tonkova E, Gesheva V (2007) Biosurfactant production by antarctic facultative anaerobe Pantoea sp during growth on hydrocarbons. Curr Microbiol 54:136–141PubMedGoogle Scholar
  225. Venkata Ramana K, Karanth NG (1989) Factors affecting biosurfactant production using Pseudomonas aeruginosa CFTR-6 under submerged conditions. J Chem Technol Biotechnol 45:249–257Google Scholar
  226. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH (2003) Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185:2080–2095PubMedGoogle Scholar
  227. Walas SM (1997) Chemical reactors. In: Perry RH, Green DW (eds) Perry’s chemical engineers’ handbook. McGraw-Hill, New York, pp 23/21–23/61Google Scholar
  228. Walter V, Syldatk C, Hausmann R (2010) Microbial production of rhamnolipid biosurfactants. In: Flickinger MC (ed) Encyclopedia of industrial biotechnology. Wiley-VCH, Weinheim, GermanyGoogle Scholar
  229. Wang XL, Gong LY, Liang SK, Han XR, Zhu CJ, Li YB (2005) Algicidal activity of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa. Harmful Algae 4:433–443Google Scholar
  230. Wang QH, Fang XD, Bai BJ, Liang XL, Shuler PJ, Goddard WA, Tang YC (2007) Engineering bacteria for production of rhamnolipid as an agent for enhanced oil recovery. Biotechnol Bioeng 98:842–853PubMedGoogle Scholar
  231. White SW, Zheng J, Zhang Y-M, Rock CO (2005) The structural biology of type II fatty acid biosynthesis. Annu Rev Biochem 74:791–831PubMedGoogle Scholar
  232. Williams P, Cámara M (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12:182–191PubMedGoogle Scholar
  233. Wu JY, Yeh KL, Lu WB, Lin CL, Chang JS (2008) Rhamnolipid production with indigenous Pseudomonas aeruginosa EM1 isolated from oil-contaminated site. Bioresour Technol 99:1157–1164PubMedGoogle Scholar
  234. Xiao G, Déziel E, He J, Lépine F, Lesic B, Castonguay MH, Milot S, Tampakaki AP, Stachel SE, Rahme LG (2006) MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62:1689–1699PubMedGoogle Scholar
  235. Xie YW, Ye RQ, Liu HL (2006) Synthesis of silver nanoparticles in reverse micelles stabilized by natural biosurfactant. Colloids Surf A Physicochem Eng Asp 279:175–178Google Scholar
  236. Xie YW, Ye RQ, Liu HL (2007) Microstructure studies on biosurfactant-rhamnolipid/n-butanol/water/n-heptane microemulsion system. Colloids Surf A Physicochem Eng Asp 292:189–195Google Scholar
  237. Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H, Hashimoto Y, Ezaki T, Arakawa M (1992) Proposal of Burkholderia Gen-Nov and transfer of 7 species of the genus Pseudomonas homology group-II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) Comb-Nov. Microbiol Immunol 36:1251–1275PubMedGoogle Scholar
  238. Yamaguchi M, Sato M, Yamada K (1976) Microbial production of sugar lipids. Chem Ind 17:741–742Google Scholar
  239. Yilmaz ES, Sidal U (2005) Investigation of antimicrobial effects of a Pseudomonas-originated biosurfactant. Biologia 60:723–725Google Scholar
  240. Yoo DS, Lee BS, Kim EK (2005) Characteristics of microbial biosurfactant as an antifungal agent against plant pathogenic fungus. J Microbiol Biotechnol 15:1164–1169Google Scholar
  241. York JD, Firoozabadi A (2008) Comparing effectiveness of rhamnolipid biosurfactant with a quaternary ammonium salt surfactant for hydrate anti-agglomeration. J Phys Chem B 112:845–851PubMedGoogle Scholar
  242. Yuan XZ, Ren FY, Zeng GM, Zhong H, Fu HY, Liu J, Xu XM (2007) Adsorption of surfactants on a Pseudomonas aeruginosa strain and the effect on cell surface lypohydrophilic property. Appl Microbiol Biotechnol 76:1189–1198PubMedGoogle Scholar
  243. Zhang YM, Miller RM (1992) Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant). Appl Environ Microbiol 58:3276–3282PubMedGoogle Scholar
  244. Zhong H, Zeng GM, Yuan XZ, Fu HY, Huang GH, Ren FY (2007) Adsorption of dirhamnolipid on four microorganisms and the effect on cell surface hydrophobicity. Appl Microbiol Biotechnol 77:447–455PubMedGoogle Scholar
  245. Zhong H, Zeng GM, Liu JX, Xu XM, Yuan XZ, Fu HY, Huang GH, Liu ZF, Ding Y (2008) Adsorption of monorhamnolipid and dirhamnolipid on two Pseudomonas aeruginosa strains and the effect on cell surface hydrophobicity. Appl Microbiol Biotechnol 79:671–677PubMedGoogle Scholar
  246. 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 190:3147–3154PubMedGoogle Scholar
  247. Zhu L, Lin J, Ma J, Cronan JE, Wang H (2009) The triclosan resistance of Pseudomonas aeruginosa PA01 is due to FabV, a triclosan-resistant enoyl-acyl carrier protein reductase. Antimicrob Agents Chemother doi: AAC.01152-01109Google Scholar
  248. Zwietering MH, Jongenburger I, Rombouts FM, Van’t Riet K (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Ahmad Mohammad Abdel-Mawgoud
    • 1
  • Rudolf Hausmann
    • 2
  • Francois Lépine
    • 1
  • Markus M. Müller
    • 2
  • Eric Déziel
    • 1
  1. 1.INRS-Institut Armand FrappierLavalCanada
  2. 2.Institute of Engineering in Life Sciences, Section of Technical BiologyResearch University KarlsruheKarlsruheGermany

Personalised recommendations