Abstract
Almost all knowledge about bacterial production of biosurfactants (BSFs) is limited to aerobic conditions. However, it is also known that bacteria can produce BSFs under oxygen-limiting conditions. These substances may be involved in important environmental processes (e.g. formation of gas hydrates and biofilms) or be applied in biotechnological processes (e.g. bioremediation and microbial enhancement of oil recovery, MEOR). Up to now, only few bacteria are described with the ability to produce BSFs under microaerobic and anaerobic conditions. Most of them belong to the Bacillus and Pseudomonas genera. However, BSF production under oxygen limitation has been detected in other bacterial groups (e.g. Anaerophaga and Thermoanaerobacter) involving different biosynthetic pathways. In this review, we summarize the current knowledge on growth requirements, cultivation conditions and properties of BSFs produced under oxygen-limiting conditions. In addition, we discuss the potential applications of microaerophilic and anaerobic BSF-producing bacteria in the perspective of bioremediation or MEOR strategies, energy and industry.
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Abdel-Mawgoud A, Lépine F, Déziel E (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86:1323–1336. doi:10.1007/s00253-010-2498-2
Albino JD, Nambi IM (2010) Partial characterization of biosurfactant produced under anaerobic conditions by Pseudomonas sp. ANBIOSURF-1. Adv Mater Res 93–94:623–626. doi:10.4028/www.scientific.net/AMR.93-94.623
Boe K, Kougias PG, Pacheco F et al (2012) Effect of substrates and intermediate compounds on foaming in manure digestion systems. Water Sci Technol 66:2146–2154. doi:10.2166/wst.2012.438
Boles BR, Thoendel M, Singh PK (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57:1210–1223. doi:10.1111/j.1365-2958.2005.04743.x
Bregnard TP-A, Höhener P, Zeyer J (1998) Bioavailability and biodegradation of weathered diesel fuel in aquifer material under denitrifying conditions. Environ Toxicol Chem 17:1222–1229. doi:10.1002/etc.5620170705
Castorena-Cortés G, Zapata-Peñasco I, Roldán-Carrillo T et al (2012) Evaluation of indigenous anaerobic microorganisms from Mexican carbonate reservoirs with potential MEOR application. J Pet Sci Eng 81:86–93. doi:10.1016/j.petrol.2011.12.010
Chang BV, Chiang F, Yuan SY (2005) Anaerobic degradation of nonylphenol in sludge. Chemosphere 59:1415–1420. doi:10.1016/j.chemosphere.2004.12.055
Chang BV, Yuan SY, Ren Y-L (2012) Anaerobic degradation of tetrabromobisphenol-A in river sediment. Ecol Eng 49:73–76. doi:10.1016/j.ecoleng.2012.08.038
Chayabutra C, Ju LK (2000) Degradation of n-hexadecane and its metabolites by Pseudomonas aeruginosa under microaerobic and anaerobic denitrifying conditions. Appl Environ Microbiol 66:493–498. doi:10.1128/AEM.66.2.493-498.2000.Updated
Chayabutra C, Wu J, Ju L-K (2001) Rhamnolipid production by Pseudomonas aeruginosa under denitrification: effects of limiting nutrients and carbon substrates. Biotechnol Bioeng 72:25–33. doi:10.1002/1097-0290(20010105)72:1<25::AID-BIT4>3.0.CO;2-J
Chrzanowski Ł, Owsianiak M, Szulc A et al (2011) Interactions between rhamnolipid biosurfactants and toxic chlorinated phenols enhance biodegradation of a model hydrocarbon-rich effluent. Int Biodeterior Biodegradation 65:605–611. doi:10.1016/j.ibiod.2010.10.015
Chrzanowski Ł, Dziadas M, Ławniczak Ł et al (2012) Biodegradation of rhamnolipids in liquid cultures: effect of biosurfactant dissipation on diesel fuel/B20 blend biodegradation efficiency and bacterial community composition. Bioresour Technol 111:328–335. doi:10.1016/j.biortech.2012.01.181
Cooper DG, Zajic JE, Gerson DF, Manninrn KI (1980) Isolation and identification of biosurfactants produced during anaerobic growth of Clostridium pasteurianum. J Ferment Technol 58:83–86
Crabbé A, Schurr MJ, Monsieurs P et al (2011) Transcriptional and proteomic responses of Pseudomonas aeruginosa PAO1 to spaceflight conditions involve Hfq regulation and reveal a role for oxygen. Appl Environ Microbiol 77:1221–1230. doi:10.1128/AEM.01582-10
Czajkowski R, de Boer WJ, van Veen JA, van der Wolf JM (2012) Characterization of bacterial isolates from rotting potato tuber tissue showing antagonism to Dickeya sp. biovar 3 in vitro and in planta. Plant Pathol 61:169–182. doi:10.1111/j.1365-3059.2011.02486.x
da Silva MLB, Soares HM, Furigo A et al (2014) Effects of nitrate injection on microbial enhanced oil recovery and oilfield reservoir souring. Appl Biochem Biotechnol 174:1810–1821. doi:10.1007/s12010-014-1161-2
Damasceno FRC, Freire DMG, Cammarota MC (2014) Assessing a mixture of biosurfactant and enzyme pools in the anaerobic biological treatment of wastewater with a high-fat content. Environ Technol 35:2035–2045. doi:10.1080/09593330.2014.890249
Das P, Mukherjee S, Sen R (2008) Genetic regulations of the biosynthesis of microbial surfactants: an overview. Biotechnol Genet Eng Rev 25:165–186. doi:10.5661/bger-25-165
Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. Microbiology 185:1027–1036. doi:10.1128/JB.185.3.1027-1036.2003
Davis DA, Lynch HC, Varley J (1999) The production of Surfactin in batch culture by Bacillus subtilis ATCC 21332 is strongly influenced by the conditions of nitrogen metabolism. Enzyme Microb Technol 25:322–329. doi:10.1016/S0141-0229(99)00048-4
De Kievit TR (2009) Quorum sensing in Pseudomonas aeruginosa biofilms. Environ Microbiol 11:279–288. doi:10.1111/j.1462-2920.2008.01792.x
De Rienzo D, Mayri A, De Ranson IU, Dorta B (2014) Biosurfactant production in aerobic and anaerobic conditions by different species of the genus Pseudomonas. J Life Sci 8:201–210. doi:10.17265/1934-7391/2014.03.001
Denger K, Schink B (1995) New halo- and thermotolerant fermenting bacteria producing surface-active compounds. Appl Microbiol Biotechnol 44:161–166. doi:10.1007/s002530050535
Denger K, Ludwig W, Warthmann R, Schink B (2002) Anaerophaga thermohalophila gen. nov., sp. nov., a moderately thermohalophilic, strictly anaerobic fermentative bacterium. Int J Syst Evol Microbiol 52:173–178. doi:10.1099/00207713-52-1-173
Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64
Elliot R, Singhal N, Swift S (2010) Surfactants and bacterial bioremediation of polycyclic aromatic hydrocarbon contaminated soil—unlocking the targets. Crit Rev Environ Sci Technol 41:78–124. doi:10.1080/00102200802641798
Espinosa-Urgel M (2003) Resident parking only: rhamnolipids maintain fluid channels in biofilms. J Bacteriol 185:699–700. doi:10.1128/JB.185.3.699-700.2003
Fakhry S, Sorrentini I, Ricca E et al (2008) Characterization of spore forming Bacilli isolated from the human gastrointestinal tract. J Appl Microbiol 105:2178–2186. doi:10.1111/j.1365-2672.2008.03934.x
Fickers P, Leclère V, Guez J-S et al (2008) Temperature dependence of mycosubtilin homologue production in Bacillus subtilis ATCC6633. Res Microbiol 159:449–457. doi:10.1016/j.resmic.2008.05.004
Folmsbee MJ, Mcinerney MJ, Nagle DP, David P (2004) Anaerobic growth of Bacillus mojavensis and Bacillus subtilis requires deoxyribonucleosides or DNA. Appl Environ Microbiol 70:5252–5257. doi:10.1128/AEM.70.9.5252-5257.2004
Folmsbee M, Duncan K, Han SO et al (2006) Re-identification of the halotolerant, biosurfactant-producing Bacillus licheniformis strain JF-2 as Bacillus mojavensis strain JF-2. Syst Appl Microbiol 29:645–649. doi:10.1016/j.syapm.2006.01.010
Ganidi N, Tyrrel S, Cartmell E (2009) Anaerobic digestion foaming causes—a review. Bioresour Technol 100:5546–5554. doi:10.1016/j.biortech.2009.06.024
Geys R, Soetaert W, Van Bogaert I (2014) Biotechnological opportunities in biosurfactant production. Curr Opin Biotechnol 30C:66–72. doi:10.1016/j.copbio.2014.06.002
Gogotov IN, Miroshnikov AI (2009) The influence of growth medium composition and physicochemical factors on biosurfactant production by the bacterium Bacillus licheniformis VKM B-511. Appl Biochem Microbiol 45:588–592. doi:10.1134/S0003683809060027
Grishchenkov VG, Townsend RT, McDonald TJ et al (2000) Degradation of petroleum hydrocarbons by facultative anaerobic bacteria under aerobic and anaerobic conditions. Process Biochem 35:889–896. doi:10.1016/S0032-9592(99)00145-4
Gudiña EJ, Pereira JFB, Rodrigues LR et al (2012) Isolation and study of microorganisms from oil samples for application in microbial enhanced oil recovery. Int Biodeterior Biodegrad 68:56–64. doi:10.1016/j.ibiod.2012.01.001
Gudiña EJ, Rangarajan V, Sen R, Rodrigues LR (2013) Potential therapeutic applications of biosurfactants. Trends Pharmacol Sci 34:667–675. doi:10.1016/j.tips.2013.10.002
Guez JS, Müller CH, Danze PM et al (2008) Respiration activity monitoring system (RAMOS), an efficient tool to study the influence of the oxygen transfer rate on the synthesis of lipopeptide by Bacillus subtilis ATCC6633. J Biotechnol 134:121–126. doi:10.1016/j.jbiotec.2008.01.003
Hamdache A, Azarken R, Lamarti A et al (2013) Comparative genome analysis of Bacillus spp. and its relationship with bioactive nonribosomal peptide production. Phytochem Rev 12:685–716. doi:10.1007/s11101-013-9278-4
Hasegawa R, Toyama K, Miyanaga K, Tanji Y (2014) Identification of crude-oil components and microorganisms that cause souring under anaerobic conditions. Appl Microbiol Biotechnol 98:1853–1861. doi:10.1007/s00253-013-5107-3
Hassett DJ, Cuppoletti J, Trapnell B et al (2002) Anaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: rethinking antibiotic treatment strategies and drug targets. Adv Drug Deliv Rev 54:1425–1443. doi:10.1016/S0169-409X(02)00152-7
Huang HW, Chang BV, Lee CC (2014) Reductive debromination of decabromodiphenyl ether by anaerobic microbes from river sediment. Int Biodeterior Biodegrad 87:60–65. doi:10.1016/j.ibiod.2013.10.011
Huang X, Shen C, Liu J, Lu L (2015) Improved volatile fatty acid production during waste activated sludge anaerobic fermentation by different bio-surfactants. Chem Eng J 264:280–290. doi:10.1016/j.cej.2014.11.078
Javaheri M, Jenneman GE, McInerney MJ, Knapp RM (1985) Anaerobic production of a biosurfactant by Bacillus licheniformis JF-2. Appl Environ Microbiol 50:698–700
Jennings EM (2005) Microbial biosurfactant production: the effect of the Bacillus strain JF-2 biosurfactant on anaerobic hydrocarbon degradation, and the presence of indigenous biosurfactant-producing bacteria in soils. Dissertation. University of Oklahoma, Norman
Jennings E, Tanner R (2004) The effects of a Bacillus biosurfactant on methanogenic hexadecane degradation. Bioremediat J 8:79–86. doi:10.1080/10889860490453195
Khire JM (2010) Bacterial biosurfactants, and their role in microbial enhanced oil recovery (MEOR). In: Sen R (ed) Biosurfactants, 1st edn. Landes Bioscience/Springer Science+Business Media, LLC, Berlin, pp 146–157
Kim HS, Yoon BD, Lee CH et al (1997) Production and properties of a lipopeptide biosurfactant from Bacillus subtilis C9. J Ferment Bioeng 84:41–46. doi:10.1016/S0922-338X(97)82784-5
Kim W, Tengra FK, Young Z et al (2013) Spaceflight promotes biofilm formation by Pseudomonas aeruginosa. PLoS ONE 8:e62437. doi:10.1371/journal.pone.0062437
Konz D, Doekel S, Marahiel MA (1999) Molecular and biochemical characterization of the protein template controlling biosynthesis of the lipopeptide lichenysin. J Bacteriol 181:133–40
Kougias PG, Boe K, O-Thong S et al (2014a) Anaerobic digestion foaming in full-scale biogas plants: a survey on causes and solutions. Water Sci Technol 69:889–895. doi:10.2166/wst.2013.792
Kougias PG, De Francisci D, Treu L et al (2014b) Microbial analysis in biogas reactors suffering by foaming incidents. Bioresour Technol 167:24–32. doi:10.1016/j.biortech.2014.05.080
La Rivière JWM (1955) The production of surface active compounds by micro-organisms and its possible significance in oil recovery. I. Some general observations on the change of surface tension in microbial cultures. Antonie Van Leeuwenhoek 21:1–8
Lanoil BD, Sassen R, La Duc MT et al (2001) Bacteria and Archaea physically associated with Gulf of Mexico gas hydrates. Appl Environ Microbiol 67:5143–5153. doi:10.1128/AEM.67.11.5143
Lequette Y, Greenberg EP (2005) Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37–44. doi:10.1128/JB.187.1.37
Li S, Pi Y, Bao M et al (2015) Effect of rhamnolipid biosurfactant on solubilization of polycyclic aromatic hydrocarbons. Mar Pollut Bull 101:219–225. doi:10.1016/j.marpolbul.2015.09.059
Lin SC, Sharma MM, Georgiou G (1993) Production and deactivation of biosurfactant by Bacillus licheniformis JF-2. Biotechnol Prog 9:138–145. doi:10.1021/bp00020a004
Lin SC, Carswell KS, Sharma MM, Georgiou G (1994a) Continuous production of the lipopeptide biosurfactant of Bacillus licheniformis JF-2. Appl Microbiol Biotechnol 41:281–285. doi:10.1007/BF00221219
Lin SC, Minton MA, Sharma MM, Georgiou G (1994b) Structural and immunological characterization of a biosurfactant produced by Bacillus licheniformis JF-2. Appl Environ Microbiol 60:31–38
Madigan MT, Martinko JM, Bender KS et al (2014) Brock biology of microorganisms, 14th edn. Pearson, London
Mandal SM, Sharma S, Pinnaka AK et al (2013) Isolation and characterization of diverse antimicrobial lipopeptides produced by Citrobacter and Enterobacter. BMC Microbiol 13:152. doi:10.1186/1471-2180-13-152
Marsh TL, Zhang X, Knapp RM et al (1995) Mechanisms of microbial oil recovery by Clostridium acetobutylicum and Bacillus strain JF-2. In: Bryant R (ed) The fifth international conference on microbial enhanced oil recovery and related biotechnology for solving environmental problems. National Technical Information Service, Springfield, pp 593–610
McInerney MJ, Jenneman GE, Knapp RM, Menzie DE (1985) Biosurfactant and enhanced oil recovery. Patent US4522261 A
McInerney MJ, Javaheri M, Nagle DP (1990) Properties of the biosurfactant produced by Bacillus licheniformis strain JF-2. J Ind Microbiol 5:95–101. doi:10.1007/BF01573858
Megharaj M, Ramakrishnan B, Venkateswarlu K et al (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int 37:1362–1375. doi:10.1016/j.envint.2011.06.003
Mnif S, Chamkha M, Labat M, Sayadi S (2011) Simultaneous hydrocarbon biodegradation and biosurfactant production by oilfield-selected bacteria. J Appl Microbiol 111:525–536. doi:10.1111/j.1365-2672.2011.05071.x
Mohan PK, Nakhla G, Yanful EK (2006) Biokinetics of biodegradation of surfactants under aerobic, anoxic and anaerobic conditions. Water Res 40:533–540. doi:10.1016/j.watres.2005.11.030
Mukherjee AK (2007) Potential application of cyclic lipopeptide biosurfactants produced by Bacillus subtilis strains in laundry detergent formulations. Lett Appl Microbiol 45:330–335. doi:10.1111/j.1472-765X.2007.02197.x
Nakhla G, Al-Sabawi M, Bassi A, Liu V (2003) Anaerobic treatability of high oil and grease rendering wastewater. J Hazard Mater 102:243–255. doi:10.1016/S0304-3894(03)00210-3
Nazina T, Griror’yan A, Feng Q (2007) Microbiological and production characteristics of the high-temperature Kongdian petroleum reservoir revealed during field trial of biotechnology for the enhancement. Microbiology 76:297–309. doi:10.1134/S002626170703006X
Nazina T, Griror’yan AA, Shestakova NM et al (2008) MEOR study enhances production in a high-temperature reservoir. World Oil 229:97–101
Nelson DL, Cox MM (2005) Lehninger principles of biochemistry, 4th edn. W. H. Freeman and Company, New York
Nerurkar AS (2010) Structural and molecular characteristics of lichenysin and its relationship with surface activity. In: Sen R (ed) Biosurfactants, 1st edn. Landes Bioscience/Springer Science+Business Media, LLC, Berlin, pp 304–315
Nguyen TT, Youssef NH, McInerney MJ, Sabatini DA (2008) Rhamnolipid biosurfactant mixtures for environmental remediation. Water Res 42:1735–1743. doi:10.1016/j.watres.2007.10.038
Nickzad A, Déziel E (2014) The involvement of rhamnolipids in microbial cell adhesion and biofilm development—an approach for control? Lett Appl Microbiol 58:447–453. doi:10.1111/lam.12211
Nihorimbere V, Cawoy H, Seyer A et al (2012) Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol 79:176–191. doi:10.1111/j.1574-6941.2011.01208.x
Nitschke M, Costa SGVAO (2007) Biosurfactants in food industry. Trends Food Sci Technol 18:252–259. doi:10.1016/j.tifs.2007.01.002
Nitschke M, Costa SGVAO, Contiero J (2005) Rhamnolipid surfactants: an update on the general aspects of these remarkable biomolecules. Biotechnol Prog 21:1593–1600. doi:10.1021/bp050239p
Nozawa T, Tanikawa T, Hasegawa H et al (2007) Rhamnolipid-dependent spreading growth of Pseudomonas aeruginosa on a high-agar medium: marked enhancement under CO2-rich anaerobic conditions. Microbiol Immunol 51:703–712. doi:10.1111/j.1348-0421.2007.tb03959.x
Okkotsu Y, Tieku P, Fitzsimmons LF et al (2013) Pseudomonas aeruginosa AlgR phosphorylation modulates rhamnolipid production and motility. J Bacteriol 195:5499–5515. doi:10.1128/JB.00726-13
Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14:10197–10228. doi:10.3390/ijms140510197
Pacwa-Plociniczak M, Plaza GA, Piotrowska-Seget Z, Cameotra SS (2011) Environmental applications of biosurfactants: recent advances. Int J Mol Sci 12:633–654. doi:10.3390/ijms12010633
Pamp SJ, Tolker-Nielsen T (2007) Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 189:2531–2539. doi:10.1128/JB.01515-06
Pelczar MJ Jr, Chan ECS, Krieg NR et al (1993) Microbiology: concepts and applications, 1st edn. McGraw-Hill Inc, New York
Pereira JFB, Gudiña EJ, Costa R et al (2013) Optimization and characterization of biosurfactant production by Bacillus subtilis isolates towards microbial enhanced oil recovery applications. Fuel 111:259–268. doi:10.1016/j.fuel.2013.04.040
Perfumo A, Rancich I, Banat IM (2010) Possibilities and challenges for biosurfactants use in petroleum industry. In: Sen R (ed) Biosurfactants, 1st edn. Landes Bioscience/Springer Science+Business Media, LLC, Berlin, pp 135–145
Petruy R (1997) Digestion of a milk-fat emulsion. Bioresour Technol 61:141–149. doi:10.1016/S0960-8524(97)00042-4
Peypoux F, Pommier MT, Marion D et al (1986) Revised structure of mycosubtilin, a peptidolipid antibiotic from Bacillus subtilis. J Antibiot (Tokyo) 39:636–641. doi:10.7164/antibiotics.39.636
Peypoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553–563. doi:10.1007/s002530051432
Pinzon NM, Cook AG, Ju L-K (2013) Continuous rhamnolipid production using denitrifying Pseudomonas aeruginosa cells in hollow-fiber bioreactor. Biotechnol Prog 29:352–358. doi:10.1002/btpr.1701
Plugge CM (2005) Anoxic media design, preparation and considerations. In: Jared RL (ed) Methods in enzymology, volume 397: environmental microbiology. Academic Press, Cambridge, pp 3–16
Reis RS, Pereira AG, Neves BC, Freire DMG (2011) Gene regulation of rhamnolipid production in Pseudomonas aeruginosa—a review. Bioresour Technol 102:6377–6384. doi:10.1016/j.biortech.2011.03.074
Rogers RE, Kothapalli C, Lee MS, Woolsey JR (2003) Catalysis of gas hydrates by biosurfactants in seawater-saturated sand/clay. Can J Chem Eng 81:973–980. doi:10.1002/cjce.5450810508
Ron EZ, Rosenberg E (2001) Natural roles of biosurfactants. Environ Microbiol 3:229–236. doi:10.1046/j.1462-2920.2001.00190.x
Sabatini DA, Knox RC, Harwell JH (1998) Surfactant selection criteria for enhanced subsurface remediation: laboratory and field observations. In: Rehage H, Peschel G (eds) Structure, dynamics and properties of disperse colloidal systems. Steinkopff, Darmstadt, pp 168–173
Sandrin TR, Chech AM, Maier RM (2000) A rhamnolipid biosurfactant reduces cadmium toxicity during naphthalene biodegradation. Appl Environ Microbiol 66:4585–4588. doi:10.1128/AEM.66.10.4585-4588.2000
Satpute SK, Banat IM, Dhakephalkar PK et al (2010) Biosurfactants, bioemulsifiers and exopolysaccharides from marine microorganisms. Biotechnol Adv 28:436–450. doi:10.1016/j.biotechadv.2010.02.006
Schooling SR, Charaf UK, Allison DG, Gilbert P (2004) A role for rhamnolipid in biofilm dispersion. Biofilms 1:91–99. doi:10.1017/S147905050400119X
Sen R (2008) Biotechnology in petroleum recovery: the microbial EOR. Prog Energy Combust Sci 34:714–724. doi:10.1016/j.pecs.2008.05.001
Sen R (2010a) Surfactin: biosynthesis, genetics and potential applications. In: Sen R (ed) Biosurfactants, 1st edn. Landes Bioscience/Springer Science+Business Media, LLC, Berlin, pp 316–323
Sen R (ed) (2010b) Biosurfactants, 1st edn. Landes Bioscience/Springer Science+Business Media, LLC, Berlin
Simpson DR, Natraj N, McInerney M, Duncan K (2011) Biosurfactant-producing Bacillus are present in produced brines from Oklahoma oil reservoirs with a wide range of salinities. Appl Microbiol Biotechnol 91:1083–1093. doi:10.1007/s00253-011-3326-z
Singh A, Van Hamme JD, Ward OP (2007) Surfactants in microbiology and biotechnology: part 2. Application aspects. Biotechnol Adv 25:99–121. doi:10.1016/j.biotechadv.2006.10.004
Soberón-Chávez G, Lépine F, Déziel E (2005) Production of rhamnolipids by Pseudomonas aeruginosa. Appl Microbiol Biotechnol 68:718–725. doi:10.1007/s00253-005-0150-3
Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857. doi:10.1111/j.1365-2958.2005.04587.x
Sullivan ER (1998) Molecular genetics of biosurfactant production. Curr Opin Biotechnol 9:263–269. doi:10.1016/s0958-1669(98)80057-8
Swannell RP, Lee K, McDonagh M (1996) Field evaluations of marine oil spill bioremediation. Microbiol Rev 60:342–365
Trebbau de Acevedo G, McInerney MJ (1996) Emulsifying activity in thermophilic and extremely thermophilic microorganisms. J Ind Microbiol 16:1–7. doi:10.1007/BF01569914
Trejo-Hernández A, Andrade-Domínguez A, Hernández M, Encarnación S (2014) Interspecies competition triggers virulence and mutability in Candida albicans–Pseudomonas aeruginosa mixed biofilms. ISME J. doi:10.1038/ismej.2014.53
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 75:3780–3790. doi:10.1128/IAI.00201-07
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 24:604–620. doi:10.1016/j.biotechadv.2006.08.001
Vander Wauven C, Piérard A, Kley-Raymann M, Haas D (1984) Pseudomonas aeruginosa mutants affected in anaerobic growth on arginine: evidence for a four-gene cluster encoding the arginine deiminase pathway. J Bacteriol 160:928–934
Vasileva-Tonkova E, Gesheva V (2007) Biosurfactant production by antarctic facultative anaerobe Pantoea sp. during growth on hydrocarbons. Curr Microbiol 54:136–141. doi:10.1007/s00284-006-0345-6
Walters MC, Roe F, Bugnicourt A et al (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47:317–323. doi:10.1128/AAC.47.1.317-323.2003
Wang S, Yu S, Zhang Z et al (2014) Coordination of swarming motility, biosurfactant synthesis, and biofilm matrix exopolysaccharide production in Pseudomonas aeruginosa. Appl Environ Microbiol 80:6724–6732. doi:10.1128/AEM.01237-14
Wenjie X, Li Y, Ping W et al (2012) Characterization of a thermophilic and halotolerant Geobacillus pallidus H9 and its application in microbial enhanced oil recovery (MEOR). Ann Microbiol 62:1779–1789. doi:10.1007/s13213-012-0436-5
Widdel F (2010) Cultivation of anaerobic microorganisms with hydrocarbons as growth substrates. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 3787–3798
Wolicka D, Borkowski A (2007) The geomicrobiological role of sulphate-reducing bacteria in environments contaminated by petroleum products. Geomicrobiol J 24:599–607. doi:10.1080/01490450701672117
Worlitzsch D, Tarran R, Ulrich M et al (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109:317–325. doi:10.1172/JCI200213870
Xia W-J, Luo Z, Dong H-P et al (2012) Synthesis, characterization, and oil recovery application of biosurfactant produced by indigenous Pseudomonas aeruginosa WJ-1 using waste vegetable oils. Appl Biochem Biotechnol 166:1148–1166. doi:10.1007/s12010-011-9501-y
Yakimov MM, Timmis KN, Wray V, Fredrickson HL (1995) Characterization of a new lipopeptide surfactant produced by thermotolerant and halotolerant subsurface Bacillus licheniformis BAS50. Appl Environ Microbiol 61:1706–1713
Yakimov MM, Amro MM, Bock M et al (1997) The potential of Bacillus licheniformis strains for in situ enhanced oil recovery. J Pet Sci Eng 18:147–160. doi:10.1016/S0920-4105(97)00015-6
Yeh DH, Pennell KD, Pavlostathis SG (1998) Toxicity and biodegradability screening of nonionic surfactants using sediment-derived methanogenic consortia. Water Sci Technol 38:55–62. doi:10.1016/S0273-1223(98)00607-6
Yeh M-S, Wei Y-H, Chang J-S (2006) Bioreactor design for enhanced carrier-assisted surfactin production with Bacillus subtilis. Process Biochem 41:1799–1805. doi:10.1016/j.procbio.2006.03.027
Yen TF, Park JK, Il Lee K, Li Y (1991) Fate of surfactant vesicles surviving from thermophilic, halotolerant, spore forming, Clostridium thermohydrosulfuricum. In: Donaldson EC (ed) Microbial enhancement of oil recovery—recent advances. Elsevier, Amesterdam, pp 297–309
Yoon SS, Hennigan RF, Hilliard GM et al (2002) Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 3:593–603. doi:10.1016/S1534-5807(02)00295-2
Youssef NH, Duncan KE, McInerney MJ (2005) Importance of 3-hydroxy fatty acid composition of lipopeptides for biosurfactant activity. Appl Environ Microbiol 71:7690–7695. doi:10.1128/AEM.71.12.7690-7695.2005
Youssef N, Simpson DR, Duncan KE et al (2007) In situ biosurfactant production by Bacillus strains injected into a limestone petroleum reservoir. Appl Environ Microbiol 73:1239–1247. doi:10.1128/AEM.02264-06
Youssef N, Simpson DR, McInerney MJ, Duncan KE (2013) In-situ lipopeptide biosurfactant production by Bacillus strains correlates with improved oil recovery in two oil wells approaching their economic limit of production. Int Biodeterior Biodegrad 81:127–132. doi:10.1016/j.ibiod.2012.05.010
Yuan SYY, Chen SJJ, Chang BVV (2011) Anaerobic degradation of tetrachlorobisphenol-A in river sediment. Int Biodeterior Biodegrad 65:185–190. doi:10.1016/j.ibiod.2010.11.001
Zhang G, Rogers RE, French WT, Lao W (2007) Investigation of microbial influences on seafloor gas-hydrate formations. Mar Chem 103:359–369. doi:10.1016/j.marchem.2006.10.005
Zhao F, Mandlaa M, Hao J et al (2014) Optimization of culture medium for anaerobic production of rhamnolipid by recombinant Pseudomonas stutzeri Rhl for microbial enhanced oil recovery. Lett Appl Microbiol 59:231–237. doi:10.1111/lam.12269
Zhao F, Cui Q, Han S et al (2015a) Enhanced rhamnolipid production of Pseudomonas aeruginosa SG by increasing copy number of rhlAB genes with modified promoter. RSC Adv 5:70546–70552. doi:10.1039/C5RA13415C
Zhao F, Ma F, Shi R et al (2015b) Production of rhamnolipids by Pseudomonas aeruginosa is inhibited by H2S but resumes in a co-culture with P. stutzeri: applications for microbial enhanced oil recovery. Biotechnol Lett 37:1803–1808. doi:10.1007/s10529-015-1859-4
Zhao F, Shi R, Zhao J et al (2015c) Heterologous production of Pseudomonas aeruginosa rhamnolipid under anaerobic conditions for microbial enhanced oil recovery. J Appl Microbiol 118:379–389. doi:10.1111/jam.12698
Zhao F, Zhang J, Shi R et al (2015d) Production of biosurfactant by a Pseudomonas aeruginosa isolate and its applicability to in situ microbial enhanced oil recovery under anoxic conditions. RSC Adv 5:36044–36050. doi:10.1039/C5RA03559G
Zhao X, Gong Y, O’Reilly SE, Zhao D (2015e) Effects of oil dispersant on solubilization, sorption and desorption of polycyclic aromatic hydrocarbons in sediment-seawater systems. Mar Pollut Bull 92:160–169. doi:10.1016/j.marpolbul.2014.12.042
Zhao F, Zhou J-D, Ma F et al (2016a) Simultaneous inhibition of sulfate-reducing bacteria, removal of H2S and production of rhamnolipid by recombinant Pseudomonas stutzeri Rhl: applications for microbial enhanced oil recovery. Bioresour Technol 207:24–30. doi:10.1016/j.biortech.2016.01.126
Zhao F, Zhou J, Han S et al (2016b) Medium factors on anaerobic production of rhamnolipids by Pseudomonas aeruginosa SG and a simplifying medium for in situ microbial enhanced oil recovery applications. World J Microbiol Biotechnol 32:54. doi:10.1007/s11274-016-2020-9
Zheng C, Yu L, Huang L et al (2012) Investigation of a hydrocarbon-degrading strain, Rhodococcus ruber Z25, for the potential of microbial enhanced oil recovery. J Pet Sci Eng 81:49–56. doi:10.1016/j.petrol.2011.12.019
Acknowledgements
Financial support for this work was provided by CESAM—Centre for Environmental and Marine Studies (FCT UID/AMB/50017/2013), CICECO—Aveiro Institute of Materials, POCI-01-0145-FEDER-007679 (FCT UID/CTM/50011/2013) and the Portuguese Foundation for Science and Technology (FCT) in the form of a PhD Grant to P. M. Domingues (SFRH/BD/88162/2012).
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M. Domingues, P., Almeida, A., Serafim Leal, L. et al. Bacterial production of biosurfactants under microaerobic and anaerobic conditions. Rev Environ Sci Biotechnol 16, 239–272 (2017). https://doi.org/10.1007/s11157-017-9429-y
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DOI: https://doi.org/10.1007/s11157-017-9429-y