Rhamnolipids: diversity of structures, microbial origins and roles

Springer Science and Business Media LLC - Tập 86 - Trang 1323-1336 - 2010
Ahmad Mohammad Abdel-Mawgoud1, François Lépine1, Eric Déziel1
1INRS-Institut Armand-Frappier, Laval, Canada

Tóm tắt

Rhamnolipids are glycolipidic biosurfactants produced by various bacterial species. They were initially found as exoproducts of the opportunistic pathogen Pseudomonas aeruginosa and described as a mixture of four congeners: α-L-rhamnopyranosyl-α-L-rhamnopyranosyl-β-hydroxydecanoyl-β-hydroxydecanoate (Rha-Rha-C10-C10), α-L-rhamnopyranosyl-α-L-rhamnopyranosyl-β-hydroxydecanoate (Rha-Rha-C10), as well as their mono-rhamnolipid congeners Rha-C10-C10 and Rha-C10. The development of more sensitive analytical techniques has lead to the further discovery of a wide diversity of rhamnolipid congeners and homologues (about 60) that are produced at different concentrations by various Pseudomonas species and by bacteria belonging to other families, classes, or even phyla. For example, various Burkholderia species have been shown to produce rhamnolipids that have longer alkyl chains than those produced by P. aeruginosa. In P. aeruginosa, three genes, carried on two distinct operons, code for the enzymes responsible for the final steps of rhamnolipid synthesis: one operon carries the rhlAB genes and the other rhlC. Genes highly similar to rhlA, rhlB, and rhlC have also been found in various Burkholderia species but grouped within one putative operon, and they have been shown to be required for rhamnolipid production as well. The exact physiological function of these secondary metabolites is still unclear. Most identified activities are derived from the surface activity, wetting ability, detergency, and other amphipathic-related properties of these molecules. Indeed, rhamnolipids promote the uptake and biodegradation of poorly soluble substrates, act as immune modulators and virulence factors, have antimicrobial activities, and are involved in surface motility and in bacterial biofilm development.

Tài liệu tham khảo

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 17:1367–1371 Abdel-Mawgoud AM, Aboulwafa MM, Hassouna NAH (2009) Characterization of rhamnolipid produced by Pseudomonas aeruginosa isolate Bs20. Appl Biochem Biotechnol 157:329–345 Abouseoud M, Maachi R, Amrane A, Boudergua S, Nabi A (2008a) Evaluation of different carbon and nitrogen sources in production of biosurfactant by Pseudomonas fluorescens. Conference on Desalination and the Environment. Sani Resort, Halkidiki, Greece, pp 143–151 Abouseoud M, Yataghene A, Amrane A, Maachi R (2008b) Biosurfactant production by free and alginate entrapped cells of Pseudomonas fluorescens. J Ind Microbiol Biotech 35:1303–1308 Alhede M, Bjarnsholt T, Jensen PO, Phipps RK, Moser C, Christophersen L, Christensen LD, van Gennip M, Parsek M, Hoiby N, Rasmussen TB, Givskov M (2009) Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiol Sgm 155:3500–3508 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 66:3262–3268 Andrä J, Rademann J, Howe J, Koch MHJ, Heine H, Zähringer U, Brandenburg K (2006) Endotoxin-like properties of a rhamnolipid exotoxin from Burkholderia (Pseudomonas) plantarii: immune cell stimulation and biophysical characterization. Biol Chem 387:301–310 Arino S, Marchal R, Vandecasteele JP (1996) Identification and production of a rhamnolipidic biosurfactant by a Pseudomonas species. Appl Microbiol Biotechnol 45:162–168 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 84:769–776 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 44:238–243 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 12:7116–7124 Beal R, Betts WB (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol 89:158–168 Bédard M, McClure CD, Schiller NL, Francoeur C, Cantin A, Denis M (1993) Release of interleukin-8, interleukin-6, and colony-stimulating factors by upper airway epithelial cells: implication for cystic fibrosis. Am J Resir Cell Mol Biol 9:455–462 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 85:1–8 Bergmann U, Scheffer J, Koller M, Schonfeld W, Erbs G, Muller FE, Konig W (1989) Induction of inflammatory mediators (histamine and leukotrienes) from rat peritoneal mast cells and human granulocytes by Pseudomonas aeruginosa strains from burn patients. Infect Immun 57:2187–2195 Bergström S, Theorell H, Davide H (1946a) On a metabolic product of Ps. pyocyanea. Pyolipic acid, active against M. tuberculosis. Arkiv Chem Mineral Geol 23A(13):1–12 Bergström S, Theorell H, Davide H (1946b) Pyolipic acid. A metabolic product of Pseudomonas pyocyanea active against Mycobacterium tuberculosis. Arch Biochem Biophys 10:165–166 Boles BR, Thoendel M, Singh PK (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57:1210–1223 Burger MM, Glaser L, Burton RM (1963) The enzymatic synthesis of a rhamnose-containing glycolipid by extracts of Pseudomonas aeruginosa. J Biol Chem 238:2595–2602 Caiazza NC, Shanks RMQ, O'Toole GA (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187:7351–7361 Caiazza NC, Merritt JH, Brothers KM, O'Toole GA (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:3603–3612 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 29:867–870 Christova N, Tuleva B, Lalchev Z, Jordanova A, Jordanov B (2004) Rhamnolipid biosurfactants produced by Renibacterium salmoninarum 27BN during growth on n-hexadecane. Z Nat Forsch C J Biosci 59:70–74 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 184:3027–3033 Cuny P, Acquaviva M, Gilewicz M (2004) Phenanthrene degradation, emulsification and surface tension activities of a Pseudomonas putida strain isolated from a coastal oil contaminated microbial mat. Ophelia 58:283–287 Davey ME, Caiazza NC, O'Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036 de Andrès C, Espuny MJ, Robert M, Mercadé ME, Guinea J (1991) Cellular lipid accumulation by Pseudomonas aeruginosa 44T1. Appl Microbiol Biotechnol 35:813–816 Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64 Déziel E, Lépine F, Dennie D, Boismenu D, Mamer OA, Villemur R (1999) Liquid chromatography/mass spectrometry analysis of mixtures of rhamnolipids produced by Pseudomonas aeruginosa strain 57RP grown on mannitol or naphthalene. Biochim Biophys Acta Mol Cell Biol Lipids 1440:244–252 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 1485:145–152 Déziel E, Comeau Y, Villemur R (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183:1195–1204 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. Microbiol Sgm 149:2005–2013 Dubeau D, Déziel E, Woods D, Lépine F (2009) Burkholderia thailandensis harbors two identical rhl gene clusters responsible for the biosynthesis of rhamnolipids. BMC Microbiology 9:263 Edwards JR, Hayashi JA (1965) Structure of a rhamnolipid from Pseudomonas aeruginosa. Arch Biochem Biophys 111:415–421 Fraser GM, Hughes C (1999) Swarming motility. Curr Opin Microbiol 2:630–635 Fujita K, Akino T, Yoshioka H (1988) Characteristics of the heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun 56:1385–1387 Fung DC, Somerville M, Richardson PS, Sheehan JK (1995) Mucus glycoconjugate complexes released from feline trachea by a bacterial toxin. Am J Respir Cell Mol Biol 12:296–306 Graham A, Steel DM, Wilson R, Cole PJ, Alton E, Geddes DM (1993) Effects of purified Pseudomonas rhamnolipids on bioelectric properties of sheep tracheal epithelium. Exp Lung Res 19:77–89 Gruber T, Chmiel H, Käppeli O, Sticher P, Fiechter A (1993) Integrated process for continuous rhamnolipid biosynthesis. In: Kosaric N (ed) Surfactant science series—biosurfactants: production, properties, application. Marcel Dekker, Inc, New York, pp 157–173 Guerra-Santos L, Kappeli O, Fiechter A (1984) Pseudomonas aeruginosa biosurfactant production in continuous culture with glucose as carbon source. Appl Environ Microbiol 48:301–305 Gunther NW, Nunez A, Fett W, Solaiman DKY (2005) Production of rhamnolipids by Pseudomonas chlororaphis, a nonpathogenic bacterium. Appl Environ Microbiol 71:2288–2293 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 Biotech 33:914–920 Guo YP, Hu YY, Gu RR, Lin H (2009) Characterization and micellization of rhamnolipidic fractions and crude extracts produced by Pseudomonas aeruginosa mutant MIG-N146. J Colloid Interface Sci 331:356–363 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 6:155–161 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 81:316–322 Haferburg D, Hommel R, Kleber HP, Kluge S, Schuster G, Zschiegner HJ (1987) Antiphytovirale Aktivität von Rhamnolipid aus Pseudomonas aeruginosa. Acta Biotechnol 7:353–356 Harshey RM (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273 Hauser G, Karnovsky ML (1954) Studies on the production of glycolipide by Pseudomonas aeruginosa. J Bacteriol 68:645–654 Häussler S, Nimtz M, Domke T, Wray V, Steinmetz I (1998) Purification and characterization of a cytotoxic exolipid of Burkholderia pseudomallei. Infect Immun 66:1588–1593 Häussler S, Rohde M, von Neuhoff N, Nimtz M, Steinmetz I (2003) Structural and functional cellular changes induced by Burkholderia pseudomallei rhamnolipid. Infect Immun 71:2970–2975 Hingley ST, Hastie A, Kueppers F, Higgins ML, Weinbaum G, Shryock T (1986) Effect of ciliostatic factors from Pseudomonas aeruginosa on rabbit respiratory cilia. Infect Immun 51:254–262 Hirayama T, Kato I (1982) Novel methyl rhamnolipids from Pseudomonas aeruginosa. FEBS Lett 139:81–85 Hisatsuka K-I, Nakahara T, Sang N, Yamada K (1971) Formation of rhamnolipid by Pseudomonas aeruginosa and its function in hydrocarbon fermentation. Agric Biol Chem 35:686–692 Hommel R (1994) Formation and function of biosurfactants for degradation of water-insoluble substrates. In: Ratledge C (ed) Biochemistry of microbial degradation. Kluwer Academic Publishers, London, pp 63–87 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 Journal 273:5101–5112 Husain S (2008) Effect of surfactants on pyrene degradation by Pseudomonas fluorescens 29L. World J Microbiol Biotechnol 24:2411–2419 Irie Y, O'Toole GA, Yuk MH (2005) Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. Fems Microbiol Lett 250:237–243 Ishigami Y, Gama Y, Nagahora H, Yamaguchi M, Nakahara H, Kamata T (1987a) The pH-sensitive conversion of molecular aggregates of rhamnolipid biosurfactant. Chem Lett 16:763–766 Ishigami Y, Gama Y, Yamaguchi M, Nakahara H, Kamata T (1987b) Surface active properties of rhamnolipids as microbial biosurfactants. J Jpn Oil ChemSoc 36:791–796 Ishigami Y, Ishii F, Choi YK, Kajiuchi T (1996) Estimation of polarity and fluidity of colloidal interfaces and biosurfaces using rhamnolipid B pyrenacylester as surface-active fluorescent probe. Colloid Surf B 7:215–220 Itoh S, Suzuki T (1972) Effect of rhamnolipids on growth of Pseudomonas aeruginosa mutant deficient in n-paraffin-utilizing ability. Agric Biol Chem 36:2233–2235 Itoh S, Honda H, Tomita F, Suzuki T (1971) Rhamnolipids produced by Pseudomonas aeruginosa grown on n-paraffin (mixture of C12, C13 and C14 fractions). J Antibiot 24:855–859 Janiyani KL, Wate SR, Joshi SR (1992) Surfactant production by Pseudomonas stutzeri. J Microb Biotechnol 7:18–21 Jarvis FG, Johnson MJ (1949) A Glyco-lipide produced by Pseudomonas aeruginosa. J Am Chem Soc 71:4124–4126 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. Microbiol Sgm 153:1329–1338 Johnson MK, Boese-Marrazzo D (1980) Production and properties of heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun 29:1028–1033 Kanthakumar K, Taylor GW, Cundell DR, Dowling RB, Johnson M, Cole PJ, Wilson R (1996) The effect of bacterial toxins on levels of intracellular adenosine nucleotides and human ciliary beat frequency. Pulm Pharmacol Ther 9:223–230 Kharazmi A, Bibi Z, Nielsen H, Hoiby N, Döring G (1989) Effect of Pseudomonas aeruginosa rhamnolipid on human neutrophil and monocyte function. Apmis 97:1068–1072 Koch AK, Käppeli O, Fiechter A, Reiser J (1991) Hydrocarbon assimilation and biosurfactant production in Pseudomonas aeruginosa mutants. J Bacteriol 173:4212–4219 Köhler T, Curty LK, Barja F, van Delden C, Pechère JC (2000) Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182:5990–5996 König B, Bergmann U, König W (1992) Induction of inflammatory mediator release (serotonin and 12- hydroxyeicosatetraenoic acid) from human platelets by Pseudomonas aeruginosa glycolipid. Infect Immun 60:3150–3155 Kownatzki R, Tümmler B, Döring G (1987) Rhamnolipid of Pseudomonas aeruginosa in sputum of cystic fibrosis patients. Lancet 1:1026–1027 Kurioka S, Liu PV (1967) Effect of the hemolysin of Pseudomonas aeruginosa on phosphatides and on phospholipase C activity. J Bacteriol 93:670–674 Lang S, Wagner F (1987) Structures and properties of biosurfactants. In: Kosaric N, Cairns WL, Gray NCC (eds) Biosurfactants and biotechnology. Marcel Dekker Inc, New York, pp 21–45 Lang S, Wullbrandt D (1999) Rhamnose lipids—biosynthesis, microbial production and application potential. Appl Microbiol Biotechnol 51:22–32 Lang S, Katsiwela E, Wagner F (1989) Antimicrobial effects of biosurfactants. Fat Sci Technol 91:363–366 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 55:1409–1413 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 37:41–46 Lequette Y, Greenberg EP (2005) Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37–44 Maier RM, Soberón-Chávez G (2000) Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl Microbiol Biotechnol 54:625–633 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 27:137–142 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 864:211–220 Matsuyama T, Nakagawa Y (1996) Surface-active exolipids: analysis of absolute chemical structures and biological functions. J Microbiol Methods 25:165–175 McClure CD, Schiller NL (1992) Effects of Pseudomonas aeruginosa rhamnolipids on monocyte-derived macrophages. J Leukoc Biol 51:97–102 McClure CD, Schiller NL (1996) Inhibition of macrophage phagocytosis by Pseudomonas aeruginosa rhamnolipids in vitro and in vivo. Curr Microbiol 33:109–117 Mireles JR 2nd, Toguchi A, Harshey RM (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183:5848–5854 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 189:7752–7764 Murray TS, Kazmierczak BI (2008) Pseudomonas aeruginosa exhibits sliding motility in the absence of type IV pili and flagella. J Bacteriol 190:2700–2708 Nayak AS, Vijaykumar MH, Karegoudar TB (2009) Characterization of biosurfactant produced by Pseudoxanthomonas sp PNK-04 and its application in bioremediation. Int Biodeterior Biodegrad 63:73–79 Neu TR (1996) Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60:151–166 Nitschke M, Costa S, Contiero J (2005) Rhamnolipid surfactants: an update on the general aspects of these remarkable biomolecules. Biotechnol Prog 21:1593–1600 Nitschke M, Costa S, Contiero J (2009) Structure and applications of a rhamnolipid surfactant produced in soybean oil waste. Appl Biochem Biotechnol. doi:10.1007/s12010-009-8707-8 Noordman WH, Janssen DB (2002) Rhamnolipid stimulates uptake of hydrophobic compounds by Pseudomonas aeruginosa. Appl Environ Microbiol 68:4502–4508 Ochsner UA, Fiechter A, Reiser J (1994) Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J Biol Chem 269:19787–19795 Ochsner UA, Hembach T, Fiechter A (1996) Production of rhamnolipid biosurfactants. Adv Biochem Eng Biotechnol 53:89–118 Ohlendorf B, Lorenzen W, Kehraus S, Krick A, Bode HB, König GM (2008) Myxotyrosides A and B, unusual rhamnosides from Myxococcus sp. J Nat Products 72:82–86 Oliveira FJS, Vazquez L, de Campos NP, de Franca FP (2009) Production of rhamnolipids by a Pseudomonas alcaligenes strain. Process Biochem 44:383–389 Onbasli D, Aslim B (2009) Biosurfactant production in sugar beet molasses by some Pseudomonas spp. J Environ Biol 30:161–163 Overhage J, Lewenza S, Marr AK, Hancock REW (2007) Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol 189:2164–2169 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 10:219–226 Pamp SJ, Tolker-Nielsen T (2007) Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 189:2531–2539 Parkins MD, Ceri H, Storey DG (2001) Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 40:1215–1226 Perneel M, D'Hondt L, De Maeyer K, Adiobo A, Rabaey K, Hofte M (2008) Phenazines and biosurfactants interact in the biological control of soil-borne diseases caused by Pythium spp. Environ Microbiol 10:778–788 Pornsunthorntawee O, Wongpanit P, Chavadej S, Abe M, Rujiravanit R (2008) Structural and physicochemical characterization of crude biosurfactant produced by Pseudomonas aeruginosa SP4 isolated from petroleum-contaminated soil. Bioresour Technol 99:1589–1595 Rahim R, Ochsner UA, Olvera C, Graninger M, Messner P, Lam JS, Soberón-Chávez G (2001) Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol Microbiol 40:708–718 Rahman P, Lungut A, Idowu J, Olea M (2009) Biosurfactant production using novel bacteria from Northeast England. Building business on bioscience sustainable innovation conference. Heriot-Watt University, Edinburgh Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97:4885–4890 Read RC, Roberts P, Munro N, Rutman A, Hastie A, Shryock T, Hall R, McDonald-Gibson W, Lund V, Taylor G (1992) Effect of Pseudomonas aeruginosa rhamnolipids on mucociliary transport and ciliary beating. J Appl Physiol 72:2271–2277 Rendell NB, Taylor GW, Somerville M, Todd H, Wilson R, Cole PJ (1990) Characterization Of Pseudomonas Rhamnolipids. Biochim Biophys Acta 1045:189–193 Rooney AP, Price NP, Ray KJ, Kuo TM (2009) Isolation and characterization of rhamnolipid-producing bacterial strains from a biodiesel facility. FEMS Microbiol Lett 295:82–87 Schenk T, Breitschwerdt A, Kessels G, Schuphan I, Schmidt B (1997) A biosynthetic route to [C-14]-labelled rhamnolipids. J Label Comp Radiopharm 39:705–710 Schooling SR, Charaf UK, Allison DG, Gilbert P (2004) A role for rhamnolipid in biofilm dispersion. Biofilms 1:91–99 Sharma A, Jansen R, Nimtz M, Johri BN, Wray V (2007) Rhamnolipids from the rhizosphere bacterium Pseudomonas sp. GRP(3) that reduces damping-off disease in Chilli and tomato nurseries. J Nat Prod 70:941–947 Shaw N (1970) Bacterial glycolipids. Microbiol Mol Biol Rev 34:365–377 Shreve GS, Inguva S, Gunnam S (1995) Rhamnolipid biosurfactant enhancement of hexadecane biodegradation by Pseudomonas aeruginosa. Mol Mar Biol Biotechnol 4:331–337 Shrout JD, Chopp DL, Just CL, Hentzer M, Givskov M, Parsek MR (2006) The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 62:1264–1277 Shryock TR, Silver SA, Banschbach MW, Kramer JC (1984) Effect of Pseudomonas aeruginosa rhamnolipid on human neutrophil migration. Curr Microbiol 10:323–328 Sierra G (1960) Hemolytic effect of a glycolipid produced by Pseudomonas aeruginosa. Antonie Van Leeuwenhoek 26:189–192 Soberón-Chávez G (2004) Biosynthesis of rhamnolipids. In: Ramos JL (ed) Pseudomonas. Kluwer Academic/Plenum Publishers, New York, pp 173–189 Soberón-Chávez G, Lépine F, Déziel E (2005) Production of rhamnolipids by Pseudomonas aeruginosa. Appl Microbiol Biotechnol 68:718–725 Somerville M, Taylor G, Watson D, Rendell NB, Rutman A, Todd H, Davies JR, Wilson R, Cole P, Richardson PS (1992) Release of mucus glycoconjugates by Pseudomonas aeruginosa rhamnolipid into feline trachea in vivo and human bronchus in vitro. Am J Respir Cell Mol Biol 6:116–122 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 56:639–644 Stanghellini ME, Miller RM (1997) Biosurfactants: their identity and potential efficacy in the biological control of zoosporic plant pathogens. Plant Dis 81:4–12 Stutts MJ, Schwab JH, Chen MG, Knowles MR, Boucher RC (1986) Effects of Pseudomonas aeruginosa on bronchial epithelial ion transport. Am Rev Respir Dis 134:17–21 Syldatk C, Lang S, Wagner F, Wray V, Witte L (1985) Chemical and physical characterization of four interfacial-active rhamnolipids from Pseudomonas spec. DSM 2874 grown on n-alkanes. Z Naturforsch C 40:51–60 Tremblay J, Richardson AP, Lépine F, Déziel E (2007) Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour. Environ Microbiol 9:2622–2630 Tuleva BK, Ivanov GR, Christova NE (2002) Biosurfactant production by a new Pseudomonas putida strain. Z Nat Forsch C J Biosci 57:356–360 Urakami T, Ito-Yoshida C, Araki H, Kijima T, Suzuki KI, Komagata K (1994) Transfer of Pseudomonas plantarii and Pseudomonas glumae to Burkholderia as Burkholderia spp. and description of Burkholderia vandii sp. nov. Int J Syst Bacteriol 44:235–245 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 117:537–546 Vasileva-Tonkova E, Gesheva V (2005) Glycolipids produced by Antarctic Nocardioides sp during growth on n-paraffin. Process Biochem 40:2387–2391 Vasileva-Tonkova E, Gesheva V (2007) Biosurfactant production by antarctic facultative anaerobe Pantoea sp during growth on hydrocarbons. Curr Microbiol 54:136–141 Vasileva-Tonkova E, Galabova D, Stoimenova E, Lalchev Z (2006) Production and properties of biosurfactants from a newly isolated Pseudomonas fluorescens HW-6 growing on hexadecane. Z Nat Forsch C J Biosci 61:553–559 Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, Michiels J (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16:496–506 Wang XL, Gong LY, Liang SK, Han XR, Zhu CJ, Li YB (2005) Algicidal activity of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa. Harmful Algae 4:433–443 Wilson NG, Bradley G (1996) The effect of immobilization on rhamnolipid production by Pseudomonas fluorescens. J Appl Bacteriol 81:525–530 Yamaguchi M, Sato M, Yamada K (1976) Microbial production of sugar lipids. Chem Ind 17:741–742 Yamaguchi M, Sato A, Dazai M, Takahara Y (1978) Report of Ferment. Res Inst 51:51 Yeung AT, Torfs EC, Jamshidi F, Bains M, Wiegand I, Hancock RE, Overhage J (2009) Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including MetR. J Bacteriol 191:5592–5602 Zhang YM, Miller RM (1994) Effect of a Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane. Appl Environ Microbiol 60:2101–2106 Zhu K, Rock CO (2008) RhlA converts beta-hydroxyacyl-acyl carrier protein intermediates in fatty acid synthesis to the beta-hydroxydecanoyl-beta-hydroxydecanoate component of rhamnolipids in Pseudomonas aeruginosa. J Bacteriol 190:3147–3154 Zulianello L, Canard C, Köhler T, Caille D, Lacroix JS, Meda P (2006) Rhamnolipids are virulence factors that promote early infiltration of primary human airway epithelia by Pseudomonas aeruginosa. Infect Immun 74:3134–3147