[en] Surfactin is a lipoheptapeptide produced by several Bacillus species and identified for the first time in 1969. At first, the biosynthesis of this remarkable biosurfactant was described in this review. The peptide moiety of the surfactin is synthesized using huge multienzymatic proteins called NonRibosomal Peptide Synthetases. This mechanism is responsible for the peptide biodiversity of the members of the surfactin family. In addition, on the fatty acid side, fifteen different isoforms (from C12 to C17) can be incorporated so increasing the number of the surfactin-like biomolecules. The review also highlights the last development in metabolic modeling and engineering and in synthetic biology to direct surfactin biosynthesis but also to generate novel derivatives. This large set of different biomolecules leads to a broad spectrum of physico-chemical properties and biological activities. The last parts of the review summarized the numerous studies related to the production processes optimization as well as the approaches developed to increase the surfactin productivity of Bacillus cells taking into account the different steps of its biosynthesis from gene transcription to surfactin degradation in the culture medium.
This work was founded by the ERACoBioTech program
(BestBioSurf project), the European INTERREG Va
SmartBioControl/Bioscreen project and the national funding agencies, the Walloon Region (Belgium), the Dutch Research
Council (NWO) (the Netherlands), the Agency for Renewable
Resources (FNR) (Germany), the Federal Ministry of Food
and Agriculture (Germany), and the Ministry of Science,
Technology and Innovation (Argentina) and Innovate UK (the
United Kingdom)
Abraham M. J., Murtola T., Schulz R., Pall S., Smith J. C., Hess B., et al. (2015). Gromacs: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2, 19–25. 10.1016/j.softx.2015.06.001
Ahimou F., Jacques P., Deleu M., (2000). Surfactin and iturin A effects on Bacillus subtilis surface hydrophobicity. Enzyme Microb. Technol. 27, 749–754. 10.1016/S0141-0229(00)00295-711118581
Akpa E., Jacques P., Wathelet B., Paquot M., Fuchs R., Budzikiewicz H., et al. (2001). Influence of culture conditions on lipopeptide production by Bacillus subtilis. Appl. Biochem. Biotechnol. 91–93, 551–561. 10.1385/ABAB:91-93:1-9:55111963884
Alanjary M., Cano-Prieto C., Gross H., Medema M. H., (2019). Computer-aided re-engineering of nonribosomal peptide and polyketide biosynthetic assembly lines. Nat. Prod. Rep. 36, 1249–1261. 10.1039/C9NP00021F31259995
Alvarez V. M., Guimarães C. R., Jurelevicius D., de Castilho L. V. A., de Sousa J. S., da Mota F. F., et al. (2020). Microbial enhanced oil recovery potential of surfactin-producing Bacillus subtilis AB2.0. Fuel 272:117730. 10.1016/j.fuel.2020.117730
Ansaldi M., Marolt D., Stebe T., Mandic-Mulec I., Dubnau D., (2002). Specific activation of the Bacillus quorum-sensing systems by isoprenylated pheromone variants. Mol. Microbiol. 44, 1561–1573. 10.1046/j.1365-2958.2002.02977.x12067344
Auchtung J. M., Lee C. A., Grossman A. D., (2006). Modulation of the ComA-dependent quorum response in Bacillus subtilis by multiple rap proteins and Phr peptides. J. Bacteriol. 188, 5273–5285. 10.1128/JB.00300-0616816200
Bernheimer A. W., Avigad L. S., (1970). Nature and properties of a cytolytic agent produced by Bacillus subtilis. J. Gen. Microbiol. 61, 361–369. 10.1099/00221287-61-3-3614992273
Bloudoff K., Schmeing T. M., (2017). Structural and functional aspects of the nonribosomal peptide synthetase condensation domain superfamily: discovery, dissection and diversity. Biochim. Biophys. Acta Proteins Proteom. (1865) 1587–1604. 10.1016/j.bbapap.2017.05.01028526268
Bonmatin J.-M., Laprevote O., Peypoux F., (2003). Diversity among microbial cyclic lipopeptides: iturins and surfactins. Activity-structure relationships to design new bioactive agents. Comb. Chem. High Throughput Screen. 6, 541–556. 10.2174/13862070310629871614529379
Bozhüyük K. A. J., Linck A., Tietze A., Kranz J., Wesche F., Nowak S., et al. (2019). Modification and de novo design of non-ribosomal peptide synthetases using specific assembly points within condensation domains. Nat. Chem. 11, 653–661. 10.1038/s41557-019-0276-z31182822
Brasseur R., Killian J. A., De Kruijff B., Ruysschaert J. M., (1987). Conformational analysis of gramicidin-gramicidin interactions at the air/water interface suggests that gramicidin aggregates into tube-like structures similar as found in the gramicidin-induced hexagonal HII phase. BBA - Biomembr. 903, 11–17. 10.1016/0005-2736(87)90150-72443166
Brück H. L., Coutte F., Dhulster P., Gofflot S., Jacques P., Delvigne F., (2020). Growth dynamics of bacterial populations in a two-compartment biofilm bioreactor designed for continuous surfactin biosynthesis. Microorganisms 8:679. 10.3390/microorganisms805067932392736
Brück H. L., Delvigne F., Dhulster P., Jacques P., Coutte F., (2019). Molecular strategies for adapting Bacillus subtilis 168 biosurfactant production to biofilm cultivation mode. Bioresour. Technol. 293:122090. 10.1016/j.biortech.2019.12209031499329
Chandler S., Van Hese N., Coutte F., Jacques P., Höfte M., De Vleesschauwer D., (2015). Role of cyclic lipopeptides produced by Bacillus subtilis in mounting induced immunity in rice (Oryza sativa L.). Physiol. Mol. Plant Pathol. 91, 20–30. 10.1016/j.pmpp.2015.05.010
Chen H. L., Chen Y. S., Juang R. S., (2007). Separation of surfactin from fermentation broths by acid precipitation and two-stage dead-end ultrafiltration processes. J. Memb. Sci. 299, 114–121. 10.1016/j.memsci.2007.04.031
Choi K. H., Heath R. J., Rock C. O., (2000). β-ketoacyl-acyl carrier protein synthase III (FabH) is a determining factor in branched-chain fatty acid biosynthesis. J. Bacteriol. 182, 365–370. 10.1128/JB.182.2.365-370.200010629181
Christensen Q. H., Martin N., Mansilla M. C., de Mendoza D., Cronan J. E., (2011). A novel amidotransferase required for lipoic acid cofactor assembly in Bacillus subtilis. Mol Microbiol. 80, 350–363. 10.1111/j.1365-2958.2011.07598.x21338421
Chtioui O., Dimitrov K., Gancel F., Dhulster P., Nikov I., (2012). Rotating discs bioreactor, a new tool for lipopeptides production. Process Biochem. 47, 2020–2024. 10.1016/j.procbio.2012.07.013
Cooper D. G., Macdonald C. R., Duff S. J. B. B., Kosaric N., (1981). Enhanced production of surfactin from bacillus subtilis by continuous product removal and metal cation additions. Appl. Environ. Microbiol. 42, 408–412. 10.1128/AEM.42.3.408-412.198116345840
Cosmina P., Rodriguez F., de Ferra F., Grandi G., Perego M., Venema G., et al. (1993). Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis. Mol. Microbiol. 8, 821–831. 10.1111/j.1365-2958.1993.tb01629.x8355609
Coutte F., Leclère V., Béchet M., Guez J. S., Lecouturier D., Chollet-Imbert M., et al. (2010a). Effect of pps disruption and constitutive expression of srfA on surfactin productivity, spreading and antagonistic properties of Bacillus subtilis 168 derivatives. J. Appl. Microbiol. 109, 480–491. 10.1111/j.1365-2672.2010.04683.x20148996
Coutte F., Lecouturier D., Yahia S. A., Leclère V., Béchet M., Jacques P., et al. (2010b). Production of surfactin and fengycin by Bacillus subtilis in a bubbleless membrane bioreactor. Appl. Microbiol. Biotechnol. 87, 499–507. 10.1007/s00253-010-2504-820221757
Coutte F., Niehren J., Dhali D., John M., Versari C., Jacques P., (2015). Modeling leucine's metabolic pathway and knockout prediction improving the production of surfactin, a biosurfactant from Bacillus subtilis. Biotechnol. J. 10, 1216–1234. 10.1002/biot.20140054126220295
Czinkóczky R., Németh Á., (2020). Techno-economic assessment of Bacillus fermentation to produce surfactin and lichenysin. Biochem. Eng. J. 163:107719. 10.1016/j.bej.2020.107719
Davis D. A., Lynch H. C., Varley J., (2001). The application of foaming for the recovery of Surfactin from B. subtilis ATCC 21332 cultures. Enzyme Microb. Technol. 28, 346–354. 10.1016/S0141-0229(00)00327-611240190
de Araujo L. L. G. C., Sodré L. G. P., Brasil L. R., Domingos D. F., de Oliveira V. M., da Cruz G. F., (2019). Microbial enhanced oil recovery using a biosurfactant produced by Bacillus safensis isolated from mangrove microbiota - Part I biosurfactant characterization and oil displacement test. J. Pet. Sci. Eng. 180, 950–957. 10.1016/j.petrol.2019.06.031
De Faria A. F., Teodoro-Martinez D. S., De Oliveira Barbosa G. N., Gontijo Vaz B., Serrano Silva Í., Garcia J. S., et al. (2011). Production and structural characterization of surfactin (C 14/Leu7) produced by Bacillus subtilisisolate LSFM-05 grown on raw glycerol from the biodiesel industry. Process Biochem. 46, 1951–1957. 10.1016/j.procbio.2011.07.001
Deleu M., Bouffioux O., Razafindralambo H., Paquot M., Hbid C., Thonart P., et al. (2003). Interaction of surfactin with membranes: a computational approach. Langmuir 19, 3377–3385. 10.1021/la026543z
Deleu M., Lorent J., Lins L., Brasseur R., Braun N., El Kirat K., et al. (2013). Effects of surfactin on membrane models displaying lipid phase separation. Biochim. Biophys. Acta Biomembr. (1828). 801–815. 10.1016/j.bbamem.2012.11.00723159483
Deleu M., Razafindralambo H., Popineau Y., Jacques P., Thonart P., Paquot M., (1999). Interfacial and emulsifying properties of lipopeptides from Bacillus subtilis. Colloids Surf. Physicochem. Eng. Asp. 152, 3–10. 10.1016/S0927-7757(98)00627-X18479055
Deravel J., Lemière S., Coutte F., Krier F., Van Hese N., Béchet M., et al. (2014). Mycosubtilin and surfactin are efficient, low ecotoxicity molecules for the biocontrol of lettuce downy mildew. Appl. Microbiol. Biotechnol. 98, 6255–6264. 10.1007/s00253-014-5663-124723290
Desmyttere H., Deweer C., Muchembled J., Sahmer K., Jacquin J., Coutte F., et al. (2019). Antifungal activities of bacillus subtilis lipopeptides to two venturia inaequalis strains possessing different tebuconazole sensitivity. Front. Microbiol. 10:2327. 10.3389/fmicb.2019.0232731695685
Dhali D., (2016). Correlation Between Lipopeptide Biosynthesis and their Precursor Metabolism in Bacillus subtilis.
Dhali D., Coutte F., Argüelles A., Auger S., Bidnenko V., Chataign,é G. et al. (2017). Genetic engineering of the branched fatty acid metabolic pathway of Bacillus subtilis for the overproduction of surfactin C14isoform. Biotechnol. J. 12, 1–23. 10.1002/biot.20160057428371347
Dieckmann R., Lee Y. O., van Liempt H., von Döhren H., Kleinkauf H., (1995). Expression of an active adenylate-forming domain of peptide synthetases corresponding to acyl-CoA-synthetases. FEBS Lett. 357, 212–216. 10.1016/0014-5793(94)01342-X7805893
D'Souza C., Nakano M. M., Zuber P., (1994). Identification of comS, a gene of the srfA operon that regulates the establishment of genetic competence in Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 91, 9397–9401. 10.1073/pnas.91.20.93977937777
Dufour S., Deleu M., Nott K., Wathelet B., Thonart P., Paquot M., (2005). Hemolytic activity of new linear surfactin analogs in relation to their physico-chemical properties. Biochim. Biophys. Acta - Gen. Subj. (1726). 87–95. 10.1016/j.bbagen.2005.06.01516026933
Eeman M., Berquand A., Dufrêne Y. F., Paquot M., Dufour S., Deleu M., (2006). Penetration of surfactin into phospholipid monolayers: nanoscale interfacial organization. Langmuir 22, 11337–11345. 10.1021/la061969p17154623
Eivazihollagh A., Svanedal I., Edlund H., Norgren M., (2019). On chelating surfactants: Molecular perspectives and application prospects. J. Mol. Liq. 278, 688–705. 10.1016/j.molliq.2019.01.076
Eppelmann K., Stachelhaus T., Marahiel M. A., (2002). Exploitation of the selectivity-conferring code of nonribosomal peptide synthetases for the rational design of novel peptide antibiotics. Biochemistry 41, 9718–9726. 10.1021/bi025940612135394
Fei D., Zhou G., Yu Z., Gang H., Liu J., Yang S., et al. (2020). Low-toxic and nonirritant biosurfactant surfactin and its performances in detergent formulations. J. Surfactants Deterg. 23, 109–118. 10.1002/jsde.12356
Fenibo E. O., Douglas S. I., Stanley H. O., (2019). A review on microbial surfactants: production, classifications, properties and characterization. J. Adv. Microbiol. 18, 1–22. 10.9734/jamb/2019/v18i330170
Francius G., Dufour S., Deleu M., Paquot M., Mingeot-Leclercq M. P., Dufrêne Y. F., (2008). Nanoscale membrane activity of surfactins: Influence of geometry, charge and hydrophobicity. Biochim. Biophys. Acta - Biomembr. 2058–2068. 10.1016/j.bbamem.2008.03.02318455997
Fujita Y., Matsuoka H., Hirooka K., (2007). Regulation of fatty acid metabolism in bacteria. Mol. Microbiol. 66, 829–839. 10.1111/j.1365-2958.2007.05947.x17919287
Fuma S., Fujishima Y., Corbell,' N Souzal C. D.', Nakano, M. M., Zuberl P., Yamane K., (1993). Nucleotide sequence of 5' portion of srfA that contains the region required for competence establishment in Bacillus subtilus. Nucleic Acids Res. 21, 93–97. 10.1093/nar/21.1.938441623
Gang H., He H., Yu Z., Wang Z., Liu J., He X., et al. (2020). A coarse-grained model for microbial lipopeptide surfactin and its application in self-assembly. J. Phys. Chem. (2020). 1839–1846. 10.1021/acs.jpcb.9b1138132083878
Gao L., Han J., Liu H., Qu X., Lu Z., Bie X., (2017). Plipastatin and surfactin coproduction by Bacillus subtilis pB2-L and their effects on microorganisms. Antonie van Leeuwenhoek. Int. J. Gen. Mol. Microbiol. 110, 1007–1018. 10.1007/s10482-017-0874-y
Geissler M., Kühle I., Heravi K. M., Altenbuchner J., Henkel M., Hausmann R., (2019). Evaluation of surfactin synthesis in a genome reduced Bacillus subtilis strain. AMB Expr. 9:84. 10.1186/s13568-019-0806-531190306
Geissler M., Oellig C., Moss K., Schwack W., Henkel M., Hausmann R., (2017). High-performance thin-layer chromatography (HPTLC) for the simultaneous quantification of the cyclic lipopeptides Surfactin, Iturin A and Fengycin in culture samples of Bacillus species. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 1044–1045, 214–224. 10.1016/j.jchromb.2016.11.013
Ghribi D., Ellouze-Chaabouni S., (2011). Enhancement of bacillus subtilis lipopeptide biosurfactants production through optimization of medium composition and adequate control of aeration. Biotechnol. Res. Int. (2011) 2011:653654. 10.4061/2011/65365421966596
Grangemard I., Peypoux F., Wallach J., Das B. C., Labb,é H Caille A., et al. (1997). Lipopeptides with improved properties: structure by NMR, purification by HPLC and structure-activity relationships of new isoleucyl-rich surfactins. J. Pept. Sci. 3, 145–154. 10.1002/(SICI)1099-1387(199703)3:2<145::AID-PSC96>3.0.CO;2-Y9230480
Grangemard I., Wallach J., Maget-Dana R., Peypoux F., (2001). Lichenysin: A more efficient cation chelator than surfactin. Appl. Biochem. Biotechnol. 90, 199–210. 10.1385/ABAB:90:3:19911318033
Grangemard I., Wallach J., Peypoux F., (1999). Evidence of surfactin hydrolysis by a bacterial endoprotease. Biotechnol. Lett. 21, 241–244. 10.1023/A:1005444717166
Graumann P. L., Marahiel M. A., (1999). Cold Shock Response in Bacillus subtilis JMMB Symposium. J. Mol. Microbiol. Biotechnol 1, 203–209.10943551
Gudiña E. J., Fernandes E. C., Rodrigues A. I., Teixeira J. A., Rodrigues L. R., (2015). Biosurfactant production by Bacillus subtilis using corn steep liquor as culture medium. Front. Microbiol. 6:59. 10.3389/fmicb.2015.0005925705209
Guez J. S., Müller C. H., Danze P. M., Büchs J., Jacques P., (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. 10.1016/j.jbiotec.2008.01.00318282625
Habe H., Taira T., Imura T., (2018). Surface activity and Ca 2+-dependent aggregation property of lichenysin produced by Bacillus licheniformis NBRC 104464. J. Oleo Sci. 67, 1307–1313. 10.5650/jos.ess1810730305561
Hamoen L. W., Eshuis H., Jongbloed J., Venema G., van Sinderen D., (1995). A small gene, designated comS, located within the coding region of the fourth amino acid-activation domain of srfA, is required for competence development in Bacillus subtilis. Mol. Microbiol. 15, 55–63. 10.1111/j.1365-2958.1995.tb02220.x7752896
Hayashi K., Kensuke T., Kobayashi K., Ogasawara N., Ogura M., (2006). Bacillus subtilis RghR (YvaN) represses rapG and rapH, which encode inhibitors of expression of the srfA operon. Mol. Microbiol. 59, 1714–1729. 10.1111/j.1365-2958.2006.05059.x16553878
Hayashi K., Ohsawa T., Kobayashi K., Ogasawara N., Ogura M., (2005). The H2O2 stress-responsive regulator perr positively regulates srfA expression in Bacillus subtilis. J. Bacteriol. 187, 6659–6667. 10.1128/JB.187.19.6659-6667.200516166527
Hbid C., Jacques P., Razafindralambo H., Mpoyo M. K., Meurice E., Paquot M., et al. (1996). Influence of the production of two lipopeptides, Iturin A and Surfactin S1, on oxygen transfer during Bacillus subtilis fermentation. Appl. Biochem. Biotechnol. 57–58, 571–579. 10.1007/BF02941737
Heath R. J., Su N., Murphy C. K., Rock C. O., (2000). The enoyl-[acyl-carrier-protein] reductases FabI and FabL from Bacillus subtilis. J. Biol. Chem. 275, 40128–40133. 10.1074/jbc.M005611200
Henry G., Deleu M., Jourdan E., Thonart P., Ongena M., (2011). The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cell. Microbiol. 13, 1824–1837. 10.1111/j.1462-5822.2011.01664.x21838773
Heuson E., Etchegaray A., Filipe S. L., Beretta D., Chevalier M., Phalip V., et al. (2018). Screening of lipopeptide producing strains of Bacillus sp. using a new automated and sensitive fluorescence detection method. Biotechnol. J. 14:1800314. 10.1002/biot.20180031430430761
Hlavica P., Lehnerer M., (2010). Oxidative biotransformation of fatty acids by cytochromes P450: predicted key structural elements orchestrating substrate specificity, regioselectivity and catalytic efficiency. Curr. Drug Metab. 11, 85–104. 10.2174/13892001079111088120302567
Hoefler B. C., Gorzelnik K. V., Yang J. Y., Hendricks N., Dorrestein P. C., Straight P. D., (2012). Enzymatic resistance to the lipopeptide surfactin as identified through imaging mass spectrometry of bacterial competition. Proc. Natl. Acad. Sci. U.S.A. 109, 13082–13087. 10.1073/pnas.120558610922826229
Horowitz S., Gilbert J. N., Griffin W. M., (1990). Isolation and characterization of a surfactant produced by Bacillus licheniformis 86. J. Ind. Microbiol. 6, 243–248. 10.1007/BF01575868
Hu F., Liu Y., Li S., (2019). Rational strain improvement for surfactin production: enhancing the yield and generating novel structures. Microb. Cell Fact. 18:42. 10.1186/s12934-019-1089-x30819187
Huang X., Liu J., Wang Y., Liu J., Lu L., (2015). The positive effects of Mn 2+ on nitrogen use and surfactin production by Bacillus subtilis ATCC 21332. Biotechnol. Biotechnol. Equip. 29, 381–389. 10.1080/13102818.2015.100690526019656
Hwang Y. H., Park B. K., Lim J. H., Kim M. S., Park S. C., Hwang M. H., et al. (2007). Lipopolysaccharide-binding and neutralizing activities of surfactin C in experimental models of septic shock. Eur. J. Pharmacol. 556, 166–171. 10.1016/j.ejphar.2006.10.03117126323
Jacques P., Hbid C., Destain J., Razafindralambo H., Paquot M., De Pauw E., et al. (1999). Optimization of biosurfactant lipopeptide production from Bacillus subtilis S499 by plackett-burman design. Appl. Biochem. Biotechnol. 77, 223–234. 10.1385/ABAB:77:1-3:223
Jahan R., Bodratti A. M., Tsianou M., Alexandridis P., (2020). Biosurfactants, natural alternatives to synthetic surfactants: physicochemical properties and applications. Adv. Colloid Interface Sci. 275:102061. 10.1016/j.cis.2019.10206131767119
Jauregi P., Coutte F., Catiau L., Lecouturier D., Jacques P., (2013). Micelle size characterization of lipopeptides produced by B. subtilis and their recovery by the two-step ultrafiltration process. Sep. Purif. Technol. 104, 175–182. 10.1016/j.seppur.2012.11.017
Jiang J., Gao L., Bie X., Lu Z., Liu H., Zhang C., et al. (2016). Identification of novel surfactin derivatives from NRPS modification of Bacillus subtilis and its antifungal activity against Fusarium moniliforme. BMC Microbiol. 16:31. 10.1186/s12866-016-0645-326957318
Jiao S., Li X., Yu H., Yang H., Li X., Shen Z., (2017). In situ enhancement of surfactin biosynthesis in Bacillus subtilis using novel artificial inducible promoters. Biotechnol. Bioeng. 114, 832–842. 10.1002/bit.2619727723092
Johnson B. A., Hage A., Kalveram B., Mears M., Plante J. A., Rodriguez S. E., et al. (2019). Peptidoglycan-associated cyclic lipopeptide disrupts viral infectivity. J. Virol. 93:e01282–e01219. 10.1128/JVI.01282-1931462558
Joshi S. J., Al-Wahaibi Y. M., Al-Bahry S. N., Elshafie A. E., Al-Bemani A. S., Al-Bahri A., et al. (2016). Production, characterization, and application of bacillus licheniformis W16 biosurfactant in enhancing oil recovery. Front. Microbiol. 7:1853. 10.3389/fmicb.2016.0185327933041
Jung J., Yu K. O., Ramzi A. B., Choe S. H., Kim S. W., Han S. O., (2012). Improvement of surfactin production in Bacillus subtilis using synthetic wastewater by overexpression of specific extracellular signaling peptides, comX and phrC. Biotechnol. Bioeng. 109, 2349–2356. 10.1002/bit.2452422511326
Kakinuma A., Hori M., Isono M., Tamura G., Arima K., (1969a). Determination of amino acid sequence in surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis. Agric. Biol. Chem. 33, 971–972. 10.1080/00021369.1969.10859408
Kakinuma A., Sugino H., Isono M., Tamura G., Arima K., (1969b). Determination of fatty acid in surfactin and elucidation of the total structure of surfactin. Agric. Biol. Chem. 33, 973–976. 10.1080/00021369.1969.10859409
Kämpfer P., (1994). Limits and possibilities of total fatty acid analysis for classification and identification of Bacillusspecies. Syst. Appl. Microbiol. 17, 86–98. 10.1016/S0723-2020(11)80035-4
Kaneda T., (1969). Fatty acids in Bacillus larvae, Bacillus lentimorbus, and Bacillus popilliae. J. Bacteriol. 98, 143–146. 10.1128/JB.98.1.143-146.19695781571
Kaneda T., (1991). Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microb. Rev. 55, 288–302. 10.1128/MR.55.2.288-302.19911886522
Kim H.-S., Yoon B.-D. Y., Suh H.-H., Oh H.-M., Katsuragi T., Tani Y., (1997). Production and properties of a lipopeptide biosurfactant from Bacillus subtilis C9. J. Ferment. Bioeng. 84, 41–46. 10.1016/S0922-338X(97)82784-5
Kowall M., Vater J., Kluge B., Stein T., Franke P., Ziessow D., (1998). Separation and characterization of surfactin isoforms produced by Bacillus subtilis OKB 105. J. Colloid Interface Sci. 204, 1–8. 10.1006/jcis.1998.55589665760
Kraas F. I., Helmetag V., Wittmann M., Strieker M., Marahiel M. A., (2010). Functional dissection of surfactin synthetase initiation module reveals insights into the mechanism of lipoinitiation. Chem. Biol. 17, 872–880. 10.1016/j.chembiol.2010.06.01520797616
Kracht M. R. O. K. O. S. H., Ozel M., Kowall M., Pauli G., Vatera J., Özel M., et al. (1999). Antiviral and hemolytic activities of surfactin isoforms and their methyl ester derivatives. J. Antibiot. 52, 613–619. 10.7164/antibiotics.52.61310513840
Lebecque S., Crowet J. M., Nasir M. N., Deleu M., Lins L., (2017). Molecular dynamics study of micelles properties according to their size. J. Mol. Graph. Model. 72, 6–15. 10.1016/j.jmgm.2016.12.00727992815
Li X., Yang H., Zhang D., Li X., Yu H., Shen Z., (2015). Overexpression of specific proton motive force-dependent transporters facilitate the export of surfactin in Bacillus subtilis. J. Ind. Microbiol. Biotechnol. 42, 93–103. 10.1007/s10295-014-1527-z25366377
Li Y., Yang S., Mu B., (2010). The surfactin and lichenysin isoforms produced by Bacillus licheniformis HSN 221. Anal. Lett. 43, 929–940. 10.1080/00032710903491047
Lien Grosdidier A., Zoete V., Michielin O., (2011). SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res. 39, 270–277. 10.1093/nar/gkr36621624888
Lins L., Brasseur R., (1995). The hydrophobic effect in protein folding. FASEB J. 9, 535–540. 10.1096/fasebj.9.7.7737462
Liu J., Zuber P., (1998). A molecular switch controlling competence and motility: competence regulatory factors ComS, MecA, and ComK control σ(D)-dependent gene expression in Bacillus subtilis. J. Bacteriol. 180, 4243–4251. 10.1128/JB.180.16.4243-4251.1998
Liu J. F., Yang J., Yang S. Z., Ye R. Q., Mu B. Z., (2012). Effects of different amino acids in culture media on surfactin variants produced by Bacillus subtilis TD7. Appl. Biochem. Biotechnol. 166, 2091–2100. 10.1007/s12010-012-9636-522415784
Liu K., Sun Y., Cao M., Wang J., Lu J. R., Xu H., (2020). Rational design, properties, and applications of biosurfactants: a short review of recent advances. Curr. Opin. Colloid Interface Sci. 45, 57–67. 10.1016/j.cocis.2019.12.005
Liu Q., Lin J., Wang W., Huang H., Li S., (2015). Production of surfactin isoforms by Bacillus subtilis BS-37 and its applicability to enhanced oil recovery under laboratory conditions. Biochem. Eng. J. 93, 31–37. 10.1016/j.bej.2014.08.023
Liu T., Montastruc L., Gancel F., Zhao L., Nikov I., (2007). Integrated process for production of surfactin. Part 1: adsorption rate of pure surfactin onto activated carbon. Biochem. Eng. J. 35, 333–340. 10.1016/j.bej.2007.01.025
Liu X. Y., Yang S. Z., Mu B. Z., (2009). Production and characterization of a C15-surfactin-O-methyl ester by a lipopeptide producing strain Bacillus subtilis HSO121. Process Biochem. 44, 1144–1151. 10.1016/j.procbio.2009.06.014
Loiseau C., Schlusselhuber M., Bigot R., Bertaux J., Berjeaud J. M., Verdon J., (2015). Surfactin from Bacillus subtilis displays an unexpected anti-Legionella activity. Appl. Microbiol. Biotechnol. 99, 5083–5093. 10.1007/s00253-014-6317-z25573468
Long X., He N., He Y., Jiang J., Wu T., (2017). Biosurfactant surfactin with pH-regulated emulsification activity for efficient oil separation when used as emulsifier. Bioresour. Technol. 241, 200–206. 10.1016/j.biortech.2017.05.12028570884
López D., Vlamakis H., Losick R., Kolter R., (2009). Paracrine signaling in a bacterium. Genes Dev. 23, 1631–1638. 10.1101/gad.1813709
Lu Y. J., Zhang Y. M., Rock C. O., (2004). Product diversity and regulation of type II fatty acid synthases. Biochem. Cell Biol. 82, 145–155. 10.1139/o03-07615052334
Maass D., Moya Ramírez I., García Román M., Jurado Alameda E., Ulson de Souza A. A., Borges Valle J. A., et al. (2016). Two-phase olive mill waste (alpeorujo) as carbon source for biosurfactant production. J. Chem. Technol. Biotechnol. 91, 1990–1997. 10.1002/jctb.4790
Maget-Dana R., Thimon L., Peypoux F., Ptak M., (1992). Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74, 1047–1051. 10.1016/0300-9084(92)90002-V1292612
Marahiel M. A., Stachelhaus T., Mootz H. D., (1997). Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97, 2651–2673. 10.1021/cr960029e11851476
Marcelino L., Puppin-Rontani J., Coutte F., Machini M. T., Etchegaray A., Puppin-Rontani R. M., (2019). Surfactin application for a short period (10/20 s) increases the surface wettability of sound dentin. Amino Acids 51, 1233–1240. 10.1007/s00726-019-02750-131197572
Marini P., Li S. J., Gardiol D., Cronan J. E., De Mendoza D., (1995). The genes encoding the biotin carboxyl carrier protein and biotin carboxylase subunits of Bacillus subtilis acetyl coenzyme a carboxylase, the first enzyme of fatty acid synthesis. J. Bacteriol. 177, 7003–7006. 10.1128/JB.177.23.7003-7006.19957592499
Marrink S. J., Risselada H. J., Yefimov S., Tieleman D. P., De Vries A. H., (2007). The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812–7824. 10.1021/jp071097f17569554
Martin N., Christensen Q. H., Mansilla M. C., Cronan J. E., de Mendoza D., (2011). A novel two-gene requirement for the octanoyltransfer reaction of Bacillus subtilis lipoic acid biosynthesis. Mol Microbiol. 80, 335–349. 10.1111/j.1365-2958.2011.07597.x21338420
Martinez L., Andrade R., Birgin E. G., Martínez J. M., (2009). PACKMOL: A package for building initial configurations for molecular dynamics simulations. J. Comput. Chem. 30, 2157–2164. 10.1002/jcc.2122419229944
Matsunaga I., Ueda A., Fujiwara N., Sumimoto T., Ichihara K., (1999). Characterization of the ybdT gene product of Bacillus subtilis: novel fatty acid β-hydroxylating cytochrome P450. Lipids 34, 841–846. 10.1007/s11745-999-0431-310529095
Meena K. R., Parmar A., Sharma A., Kanwar S. S., (2018). A novel approach for body weight management using a bacterial surfactin lipopeptide. Obes. Med. 10, 24–28. 10.1016/j.obmed.2018.05.003
Menkhaus M., Ullrich C., Kluge B., Vater J., Vollenbroich D., Kamp R. M., (1993). Structural and functional organization of the surfactin synthetase multienzyme system. J. Biol. Chem. 268, 7678–7684. 10.1016/S0021-9258(18)53010-68096516
Miyazaki N., Sugai Y., Sasaki K., Okamoto Y., Yanagisawa S., (2020). Screening of the effective additive to inhibit surfactin from forming precipitation with divalent cations for surfactin enhanced oil recovery. Energies 13:2430. 10.3390/en13102430
Mnif I., Besbes S., Ellouze-Ghorbel R., Ellouze-Chaabouni S., Ghribi D., (2013). Improvement of bread dough quality by Bacillus subtilis SPB1 biosurfactant addition: optimized extraction using response surface methodology. J. Sci. Food Agric. 93, 3055–3064. 10.1002/jsfa.613923512731
Mohammadipour M., Mousivand M., Jouzani G. S., Abbasalizadeh S., (2009). Molecular and biochemical characterization of Iranian surfactin-producing Bacillus subtilis isolates and evaluation of their biocontrol potential against Aspergillus flavus and Colletotrichum gloeosporioides. Can. J. Microbiol. 55, 395–404. 10.1139/W08-14119396239
Mootz H. D., Finking R., Marahiel M. A., (2001). 4′-Phosphopantetheine transfer in primary and secondary metabolism of Bacillus subtilis. J. Biol. Chem. 276, 37289–37298. 10.1074/jbc.M10355620011489886
Mootz H. D., Kessler N., Linne U., Eppelmann K., Schwarzer D., Marahiel M. A., (2002). Decreasing the ring size of a cyclic nonribosomal peptide antibiotic by in-frame module deletion in the biosynthetic genes. J. Am. Chem. Soc. 124, 10980–10981. 10.1021/ja027276m12224936
Morbidoni H. R., De Mendoza D., Cronan J. E., (1996). Bacillus subtilis acyl carrier protein is encoded in a cluster of lipid biosynthesis genes. J. Bacteriol. 178, 4794–4800. 10.1128/JB.178.16.4794-4800.19968759840
Morikawa M., Hirata Y., Imanaka T., (2000). A study on the structure-function relationship of lipopeptide biosurfactants. Biochim. Biophys. Acta - Gen. Subj. (1488). 211–218. 10.1016/S1388-1981(00)00124-411082531
Morris G. M., Ruth H., Lindstrom W., Sanner M. F., Belew R. K., Goodsell D. S., et al. (2009). Software news and updates AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785–2791. 10.1002/jcc.21256
Moya Ramírez I., Tsaousi K., Rudden M., Marchant R., Jurado Alameda E., García Román M., et al. (2015). Rhamnolipid and surfactin production from olive oil mill waste as sole carbon source. Bioresour. Technol. 198, 231–236. 10.1016/j.biortech.2015.09.01226398666
Mulligan C. N., Yong R. N., Gibbs B. F., James S., Bennett H. P. J., (1999). Metal removal from contaminated soil and sediments by the biosurfactant surfactin. Environ. Sci. Technol. 33, 3812–3820. 10.1021/es9813055
Nagai S., Okimura K., Kaizawa N., Ohki K., Kanatomo S., (1996). Study on surfactin, a cyclic depsipeptide. II. Synthesis of surfactin B2 produced by Bacillus natto KMD (2311). Chem. Pharm. Bull. 44, 5–10. 10.1248/cpb.44.58582044
Nakano M. M., Corbell N., Besson J., Zuber P., (1992). Isolation and characterization of sfp: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis. MGG Mol. Gen. Genet. 232, 313–321. 10.1007/BF002800111557038
Nakano M. M., Marahiel M. A., Zuber P., (1988). Identification of a genetic locus required for biosynthesis of the lipopeptide antibiotic surfactin in Bacillus subtilis. J. Bacteriol. 170, 5662–5668. 10.1128/JB.170.12.5662-5668.19882848009
Naruse N., Tenmyo O., Kobaru S., Kamei H., Miyaki T., Konishi M., et al. (1990). Pumilacidin, a complex of new antiviral antibiotics production, isolation, chemical properties, structure and biological activity. J. Antibiot. 43, 267–280. 10.7164/antibiotics.43.2672157695
Niehren J., Versari C., John M., Coutte F., Jacques P., Predicting P. J., (2016). Predicting changes of reaction networks with partial kinetic information. BioSystems 149, 113–124. 10.1016/j.biosystems.2016.09.00327769750
Nitschke M., Pastore G. M., (2004). Biosurfactant production by Bacillus subtilis using cassava-processing effluent. Appl. Biochem. Biotechnol. 112, 163–172. 10.1385/ABAB:112:3:16315007184
Ohadi M., Shahravan A., Dehghannoudeh N., Eslaminejad T., Banat I. M., Dehghannoudeh G., (2020). Potential use of microbial surfactant in microemulsion drug delivery system: a systematic review. Drug Des. Devel. Ther. 14, 541–550. 10.2147/DDDT.S23232532103896
Ohno A., Ano T., Shoda M., (1995a). Effect of temperature on production of lipopeptide antibiotics, iturin A and surfactin by a dual producer, Bacillus subtilis RB14, in solid-state fermentation. J. Ferment. Bioeng. 80, 517–519. 10.1016/0922-338X(96)80930-5
Ohno A., Ano T., Shoda M., (1995b). Production of a lipopeptide antibiotic, surfactin, by recombinant Bacillus subtilis in solid state fermentation. Biotechnol. Bioeng. 47, 209–214. 10.1002/bit.26047021218623394
Ohsawa T., Tsukahara K., Sato T., Ogura M., (2006). Superoxide stress decreases expression of srfA through inhibition of transcription of the comQXP quorum-sensing locus in Bacillus subtilis. J. Biochem. 139, 203–211. 10.1093/jb/mvj02316452308
Ong S. A., Wu J. C., (2018). A simple method for rapid screening of biosurfactant-producing strains using bromothymol blue alone. Biocatal. Agric. Biotechnol. 16, 121–125. 10.1016/j.bcab.2018.07.027
Ongena M., Jacques P., (2008). Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16, 115–125. 10.1016/j.tim.2007.12.00918289856
Ongena M., Jourdan E., Adam A., Paquot M., Brans A., Joris B., et al. (2007). Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol. 9, 1084–1090. 10.1111/j.1462-2920.2006.01202.x17359279
Pagadoy M., Peypoux F., Wallach J., (2005). Solid-phase synthesis of surfactin, a powerful biosurfactant produced by Bacillus subtilis, and of four analogues. Int. J. Pept. Res. Ther. 11, 195–202. 10.1007/s10989-005-6790-4
Paraszkiewicz K., Bernat P., Kuśmierska A., Chojniak J., Płaza G., (2018). Structural identification of lipopeptide biosurfactants produced by Bacillus subtilis strains grown on the media obtained from renewable natural resources. J. Environ. Manage. 209, 65–70. 10.1016/j.jenvman.2017.12.03329275286
Park S. Y., Kim Y. H., (2009). Surfactin inhibits immunostimulatory function of macrophages through blocking NK-κB, MAPK and Akt pathway. Int. Immunopharmacol. 9, 886–893. 10.1016/j.intimp.2009.03.01319336264
Peypoux F., Bonmatin J., Labbe H., Grangemard I., Das B. C., Ptak M., et al. (1994). [Ala4]Surfactin, a novel isoform from. Eur. J. Biochem. 224, 89–96. 10.1111/j.1432-1033.1994.tb19998.x8076655
Peypoux F., Bonmatin J.-M., Labbé H., Das B. C., Ptak M., Michel G., (1991). Isolation and characterization of a new variant of surfactin, the [Val7]surfactin. Eur. J. Biochem. 202, 101–106. 10.1111/j.1432-1033.1991.tb16349.x1935967
Quadri L. E. N., Weinreb P. H., Lei M., Nakano M. M., Zuber P., Walsh C. T., (1998). Characterization of Sfp, a Bacillus subtilis phosphopantetheinyl transferase for peptidyl carder protein domains in peptide synthetases. Biochemistry 37, 1585–1595. 10.1021/bi9719861
Rausch C., Hoof I., Weber T., Wohlleben W., Huson D. H., (2007). Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution. BMC Evol. Biol. 7:78. 10.1186/1471-2148-7-7817506888
Rausch C., Weber T., Kohlbacher O., Wohlleben W., Huson D. H., (2005). Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res. 33, 5799–5808. 10.1093/nar/gki88516221976
Razafindralambo H., Popineau Y., Deleu M., Hbid C., Jacques P., Thonart P., et al. (1998). Foaming properties of lipopeptides produced by Bacillus subtilis: effect of lipid and peptide structural attributes. J. Agric. Food Chem. 46, 911–916. 10.1021/jf970592d
Roongsawang N., Washio K., Morikawa M., (2011). Diversity of nonribosomal peptide synthetases involved in the biosynthesis of lipopeptide biosurfactants. Int. J. Mol. Sci. 12, 141–172. 10.3390/ijms1201014121339982
Runguphan W., Keasling J. D., (2014). Metabolic engineering of Saccharomyces cerevisiae for production of fatty acid-derived biofuels and chemicals. Metab. Eng. 21, 103–113. 10.1016/j.ymben.2013.07.00323899824
Schneider A., Stachelhaus T., Marahiel M. A., (1998). Targeted alteration of the substrate specificity of peptide synthetases by rational module swapping. Mol. Gen. Genet. 257, 308–318. 10.1007/s0043800506529520265
Schneider K. B., Palmer T. M., Grossman A. D., (2002). Characterization of comQ and comX, two genes required for production of comX pheromone in Bacillus subtilis. J. Bacteriol. 184, 410–419. 10.1128/JB.184.2.410-419.200211751817
Schujman G. E., Choi K., Altabe S., Rock C. O., de Mendoza D., (2001). Response of Bacillus subtilisto cerulenin and acquisition of resistance. J. Bacteriol. 183, 3032–3040. 10.1128/JB.183.10.3032-3040.200111325930
Schwarzer D., Mootz H. D., Linne U., Marahiel M. A., (2002). Regeneration of misprimed nonribosomal peptide synthetases by type II thioesterases. Proc. Natl. Acad. Sci. U.S.A. 99, 14083–14088. 10.1073/pnas.21238219912384573
Serre L., Swenson L., Green R., Wei Y., Verwoert I.ra, I., G. S. et al. (1994). Crystallization of the malonyl coenzyme A-acyl carrier protein transacylase from Escherichia coli. J Mol Biol. 242, 99–102. 10.1006/jmbi.1994.15598078074
Serre L., Verbree E. C., Dauter Z., Stuitje A. R., Derewenda Z. S., (1995). The Escherichia coli malonyl-CoA:acyl carrier protein transacylase at 1.5-A resolution. Crystal structure of a fatty acid synthase component. J. Biol. Chem. 270, 12961–12964. 10.1074/jbc.270.22.129617768883
Shakerifard P., Gancel F., Jacques P., Faille C., (2009). Effect of different Bacillus subtilis lipopeptides on surface hydrophobicity and adhesion of Bacillus cereus 98/4 spores to stainless steel and Teflon. Biofouling 25, 533–541. 10.1080/0892701090297794319431000
Shao C., Liu L., Gang H., Yang S., Mu B., (2015). Structural diversity of the microbial surfactin derivatives from selective esterification approach. Int. J. Mol. Sci. 16, 1855–1872. 10.3390/ijms1601185525599527
Sieber S. A., Marahiel M. A., (2005). Molecular mechanisms underlying nonribosomal peptide synthesis: approaches to new antibiotics. Chem. Rev. 105, 715–738. 10.1021/cr030119115700962
Sinderen D., Galli G., Cosmina P., Ferra F., Withoff S., Venema G., et al. (1993). Characterization of the srfA locus of Bacillus subtilis: only the valine-activating domain of srfA is involved in the establishment of genetic competence. Mol. Microbiol. 8, 833–841. 10.1111/j.1365-2958.1993.tb01630.x8355610
Smyth T. J., Perfumo A., Mcclean S., Banat I. M., (2010). “Isolation and analysis of lipopeptides and high molecular weight biosurfactants,” in Handbook of Hydrocarbon and Lipid Microbiology, eds K. N. Timmis, T. J. McGenity, J. R. vanderMeer, and V. deLorenzo (Berlin; Heidelberg: Springer), 3689–3704. 10.1007/978-3-540-77587-4_290
Stachelhaus T., Schneider A., Marahiel M. A., (1995). Rational design of peptide antibiotics by targeted replacement of bacterial and fungal domains. Science 269, 69–72. 10.1126/science.76042807604280
Stachelhaus T., Schneider A., Marahiel M. A., (1996). Engineered biosynthesis of peptide antibiotics. Biochem. Pharmacol. 52, 177–186. 10.1016/0006-2952(96)00111-6
Steen E. J., Kang Y., Bokinsky G., Hu Z., Schirmer A., McClure A., et al. (2010). Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 463, 559–562. 10.1038/nature0872120111002
Steller S., Sokoll A., Wilde C., Bernhard F., Franke P., Vater J., (2004). Initiation of surfactin biosynthesis and the role of the SrfD-thioesterase protein. Biochemistry 43, 11331–11343. 10.1021/bi049341615366943
Stiegelmeyer S. M., Giddings M. C., (2013). Agent-based modeling of competence phenotype switching in Bacillus subtilis. Theor. Biol. Med. Model. 10:23. 10.1186/1742-4682-10-2323551850
Süssmuth R. D., Mainz A., (2017). Nonribosomal peptide synthesis—principles and prospects. Angew. Chemie - Int. Ed. 56, 3770–3821. 10.1002/anie.201609079
Taira T., Yanagisawa S., Nagano T., Tsuji T., Endo A., Imura T., (2017). pH-induced conformational change of natural cyclic lipopeptide surfactin and the effect on protease activity. Colloids Surfaces B Biointerf. 156, 382–387. 10.1016/j.colsurfb.2017.05.01728551572
Takahashi T., Ohno O., Ikeda Y., Sawa R., Homma Y., Igarashi M., et al. (2006). Inhibition of lipopolysaccharide activity by a bacterial cyclic lipopeptide surfactin. J. Antibiot. 59, 35–43. 10.1038/ja.2006.616568717
Tanaka K., Amaki Y., Ishihara A., Nakajima H., (2015). Synergistic effects of [Ile7]Surfactin homologues with bacillomycin d in suppression of gray mold disease by Bacillus amyloliquefaciens biocontrol strain SD-32. J. Agric. Food Chem. 63, 5344–5353. 10.1021/acs.jafc.5b01198
Tanaka K., Henry C. S., Zinner J. F., Jolivet E., Cohoon M. P., Xia F., et al. (2013). Building the repertoire of dispensable chromosome regions in Bacillus subtilis entails major refinement of cognate large-scale metabolic model. Nucleic Acids Res. 41, 687–699. 10.1093/nar/gks96323109554
Tang J.-S., Gao H., Hong K., Yu W., Jiang M.-M., Lin H.-P., et al. (2007). Complete assignement of 1H and 13C NMR spectral data of nine surfactin isomers. Magn. Reson. Chem. 45, 488–495. 10.1002/mrc.2048
Tong L., (2013). Structure and function of biotin-dependent carboxylases. Cell. Mol. Life Sci. 70, 863–891. 10.1007/s00018-012-1096-0
Trauger J. W., Kohli R. M., Mootz H. D., Marahiel M. A., Walsh C. T., (2000). Peptide cyclization catalysed by the thioesterase domain of tyrocidine synthetase. Nature 407, 215–218. 10.1038/3502511611001063
Tsuge K., Ano T., Hirai M., Nakamura Y., Shoda M., (1999). The genes degQ, pps, and lpa-8 (sfp) are responsible for conversion of Bacillus subtilis 168 to plipastatin production. Antimicrob. Agents Chemother. 43, 2183–2192. 10.1128/AAC.43.9.218310471562
Tsuge K., Ohata Y., Shoda M., (2001). Gene yerP, involved in surfactin self-resistance in Bacillus subtilis. Antimicrob. Agents Chemother. 45, 3566–3573. 10.1128/AAC.45.12.3566-3573.200111709341
Varvaresou A., Iakovou K., (2015). Biosurfactants in cosmetics and biopharmaceuticals. Lett. Appl. Microbiol. 61, 214–223. 10.1111/lam.1244025970073
Verma A., Kumar A., Debnath M., (2016). Molecular docking and simulation studies to give insight of surfactin amyloid interaction for destabilizing Alzheimer's Ab42 protofibrils. Med. Chem. Res. 25, 1616–1622. 10.1007/s00044-016-1594-y
Vollenbroich D., Pauli G., Ozel M., Vater J., (1997). Antimycoplasma properties and application in cell culture of surfactin, a lipopeptide antibiotic from Bacillus subtilis. Appl. Environ. Microbiol. 63, 44–49. 10.1128/AEM.63.1.44-49.19978979337
Wakil S. J., Stoops J. K., Joshi V. C., (1983). Fatty acid synthesis and its regulation. Annu. Rev. Biochem. 52, 537–579. 10.1146/annurev.bi.52.070183.002541
Wang C., Cao Y., Wang Y., Sun L., Song H., (2019). Enhancing surfactin production by using systematic CRISPRi repression to screen amino acid biosynthesis genes in Bacillus subtilis. Microb. Cell Fact. 18:90. 10.1186/s12934-019-1139-431122258
Wang X., Cai T., Wen W., Ai J., Ai J., Zhang Z., et al. (2020). Surfactin for enhanced removal of aromatic hydrocarbons during biodegradation of crude oil. Fuel 267:117272. 10.1016/j.fuel.2020.117272
Wei Y. H., Lai C. C., Chang J. S., (2007). Using Taguchi experimental design methods to optimize trace element composition for enhanced surfactin production by Bacillus subtilis ATCC 21332. Process Biochem. 42, 40–45. 10.1016/j.procbio.2006.07.025
Willecke K., Pardee A. B., (1971). Fatty acid-requiring mutant of Bacillus subtilis defective in branched chain alpha-keto acid dehydrogenase. J. Biol. Chem. 246, 5264–5272. 10.1016/S0021-9258(18)61902-74999353
Willenbacher J., Mohr T., Henkel M., Gebhard S., Mascher T., Syldatk C., et al. (2016). Substitution of the native srfA promoter by constitutive Pvegin two B. Subtilis strains and evaluation of the effect on Surfactin production. J. Biotechnol. 224, 14–17. 10.1016/j.jbiotec.2016.03.00226953743
Willenbacher J., Yeremchuk W., Mohr T., Syldatk C., Hausmann R., (2015). Enhancement of Surfactin yield by improving the medium composition and fermentation process. AMB Express 5:57. 10.1186/s13568-015-0145-026297438
Willenbacher J., Zwick M., Mohr T., Schmid F., Syldatk C., Hausmann R., (2014). Evaluation of different Bacillus strains in respect of their ability to produce Surfactin in a model fermentation process with integrated foam fractionation. Appl. Microbiol. Biotechnol. 98, 9623–9632. 10.1007/s00253-014-6010-225158834
Wu Q., Zhi Y., Xu Y., (2019). Systematically engineering the biosynthesis of a green biosurfactant surfactin by Bacillus subtilis 168. Metab. Eng. 52, 87–97. 10.1016/j.ymben.2018.11.00430453038
Wu Y. S., Ngai S. C., Goh B. H., Chan K. G., Lee L. H., Chuah L. H., (2017). Anticancer activities of surfactin potential application of nanotechnology assisted surfactin delivery. Front. Pharmacol. 8:761. 10.3389/fphar.2017.0076129123482
Yakimov M. M., Abraham W. R., Meyer H., Laura G., Golyshin P. N., (1999). Structural characterization of lichenysin A components by fast atom bombardment tandem mass spectrometry. Biochim. Biophys. Acta 273–280. 10.1016/S1388-1981(99)00058-X10320810
Yakimov M. M., Fredrickson H. L., Timmis K. N., (1996). Effect of heterogeneity of hydrophobic moieties on surface activity of lichenysin A, a lipopeptide biosurfactant from Bacillus licheniformis BASSO. Biotechnol. Appl. Biochem. 23, 13–18.
Yakimov M. M., Timmis K. N., Wray V., Fredrickson H. L., (1995). Characterization of a new lipopeptide surfactant produced by thermotolerant and halotolerant subsurface Bacillus licheniformis BAS50. Appl. Environ. Microbiol. 61, 1706–1713. 10.1128/AEM.61.5.1706-1713.19957646007
Yan X., Yu H. J., Hong Q., Li S. P., (2008). Cre/lox system and PCR-based genome engineering in Bacillus subtilis. Appl. Environ. Microbiol. 74, 5556–5562. 10.1128/AEM.01156-0818641148
Yang H., Li X., Li X., Yu H., Shen Z., (2015a). Identification of lipopeptide isoforms by MALDI-TOF-MS/MS based on the simultaneous purification of iturin, fengycin, and surfactin by RP-HPLC. Anal. Bioanal. Chem. 407, 2529–2542. 10.1007/s00216-015-8486-825662934
Yang H., Yu H., Shen Z., (2015b). A novel high-throughput and quantitative method based on visible color shifts for screening Bacillus subtilis THY-15 for surfactin production. J. Ind. Microbiol. Biotechnol. 42, 1139–1147. 10.1007/s10295-015-1635-426065390
Yang Z., Zu Y., Zhu J., Jin M., Cui T., Long X., (2020). Application of biosurfactant surfactin as a pH-switchable biodemulsifier for efficient oil recovery from waste crude oil. Chemosphere 240:124946. 10.1016/j.chemosphere.2019.12494631726598
Yeh E., Kohli R. M., Bruner S. D., Walsh C. T., (2004). Type II thioesterase restores activity of a nrps module stalled with an aminoacyl-S-enzyme that cannot be elongated. ChemBioChem 5, 1290–1293. 10.1002/cbic.20040007715368584
Yeh M. S., Wei Y. H., Chang J. S., (2005). Enhanced production of surfactin from Bacillus subtilis by addition of solid carriers. Biotechnol. Prog. 21, 1329–1334. 10.1021/bp050040c
Youssef N. H., Duncan K. E., Nagle D. P., Savage K. N., Knapp R. M., McInerney M. J., (2004). Comparison of methods to detect biosurfactant production by diverse microorganisms. J. Microbiol. Methods 56, 339–347. 10.1016/j.mimet.2003.11.00114967225
Youssef N. H., Wofford N., McInerney M. J., (2011). Importance of the long-chain fatty acid beta-hydroxylating cytochrome P450 Enzyme YbdT for lipopeptide biosynthesis in Bacillus subtilis strain OKB105. Int. J. Mol. Sci. 12, 1767–1786. 10.3390/ijms1203176721673922
Yuan L., Zhang S., Wang Y., Li Y., Wang X., Yang Q., (2018). Surfactin inhibits membrane fusion during invasion of epithelial cells by enveloped viruses. J. Virol. 92, 1–19. 10.1128/JVI.00809-1830068648
Zanotto A. W., Valério A., de Andrade C. J., Pastore G. M., (2019). New sustainable alternatives to reduce the production costs for surfactin 50 years after the discovery. Appl. Microbiol. Biotechnol. 103, 8647–8656. 10.1007/s00253-019-10123-731515599
Zezzi do Valle Gomes M., Nitschke M., (2012). Evaluation of rhamnolipid and surfactin to reduce the adhesion and remove biofilms of individual and mixed cultures of food pathogenic bacteria. Food Control 25, 441–447. 10.1016/j.foodcont.2011.11.025
Zhang Y., Nakano S., Choi S. Y., Zuber P., (2006). Mutational analysis of the Bacillus subtilis RNA polymerase α C-terminal domain supports the interference model of Spx-dependent repression. J. Bacteriol. 188, 4300–4311. 10.1128/JB.00220-0616740936
Zhao H., Shao D., Jiang C., Shi J., Li Q., Huang Q., et al. (2017). Biological activity of lipopeptides from Bacillus. Appl. Microbiol. Biotechnol. 101, 5951–5960. 10.1007/s00253-017-8396-0
Zhuravleva O. I., Afiyatullov S. S., Ermakova S. P., Nedashkovskaya O. I., Dmitrenok P. S., Denisenko V. A., et al. (2010). New C14-surfactin methyl ester from the marine bacterium Bacillus pumilus KMM 456. Russ. Chem. Bull. 59, 2137–2142. 10.1007/s11172-010-0369-8
Zou A., Liu J., Garamus V. M., Yang Y., Willumeit R., Mu B., (2010). Micellization activity of the natural lipopeptide [Glu1, Asp5] surfactin-C15 in aqueous solution. J. Phys. Chem. B 114, 2712–2718. 10.1021/jp908675s
Zouari R., Besbes S., Ellouze-Chaabouni S., Ghribi-Aydi D., (2016). Cookies from composite wheat-sesame peels flours: dough quality and effect of Bacillus subtilis SPB1 biosurfactant addition. Food Chem. 194, 758–769. 10.1016/j.foodchem.2015.08.06426471616
Zouboulis A. I., Matis K. A., Lazaridis N. K., Golyshin P. N., (2003). The use of biosurfactants in flotation: application for the removal of metal ions. Miner. Eng. 16, 1231–1236. 10.1016/j.mineng.2003.06.013
Zune Q., Telek S., Calvo S., Salmon T., Alchihab M., Toye D., et al. (2016). Influence of liquid phase hydrodynamics on biofilm formation on structured packing: optimization of surfactin production from Bacillus amyloliquefaciens. Chem. Eng. Sci. 170, 628–638. 10.1016/j.ces.2016.08.023