Abstract
Surfactin has many biological activities, such as inhibiting plant diseases, resisting bacteria, fungi, viruses, tumors, mycoplasma, anti-adhesion, etc. It has great application potential in agricultural biological control, clinical medical treatment, environmental treatment and other fields. However, the low yield has been the bottleneck of its popularization and application. It is very important to understand the synthesis route and control strategy of surfactin to improve its yield and purity. In this paper, based on the biosynthetic pathway and regulatory factors of surfactin, its biosynthesis regulation strategy was comprehensively summarized, involving enhancement of endogenous and exogenous precursor supply, modification of the synthesis pathway of lipid chain and peptide chain, improvement of secretion and efflux, and manipulation some global regulatory factors, such as Spo0A, AbrB, ComQXP, phrCSF, etc. to directly or indirectly stimulate surfactin synthesis. And the current production and separation and purification process of surfactin are briefly described. This review also provides a scientific reference for promoting surfactin production and its applications in various fields.
This is a preview of subscription content, log in via an institution to check access.
Availability of data and materials
No data were used for the research described in the article.
References
Ali SAM, Sayyed RZ, Mir MI, Khan MY, Hameeda B, Alkhanani MF, Haque S, Al Tawaha ARM, Poczai P (2022) Induction of systemic resistance in maize and antibiofilm activity of surfactin from Bacillus velezensis MS20. Front Microbiol 13:879739. https://doi.org/10.3389/fmicb.2022.879739
Baker SC, Chen CY (2010) Enrichment and purification of lipopeptide biosurfactants. Biosurfactants 672:281–288
Baker MD, Neiditch MB (2011) Structural basis of response regulator inhibition by a bacterial anti-activator protein. Plos Biol 9(12):e1001226. https://doi.org/10.1371/journal.pbio.1001226
Bartal A, Huynh T, Kecskeméti A, Vörös M, Kedves O, Allaga H, Ma V, Kredics L, Vagvolgyi C, Szekeres A (2023) Identifications of surfactin-type biosurfactants produced by Bacillus Species isolated from rhizosphere of vegetables. Molecules 28(3):1172. https://doi.org/10.3390/molecules28031172
Boguslawski KM, Hill PA, Griffith KL (2015) Novel mechanisms of controlling the activities of the transcription factors Spo0A and ComA by the plasmid-encoded quorum sensing regulators Rap60-Phr60 in Bacillus subtilis. Mol Microbiol 96:325–348. https://doi.org/10.1111/mmi.12939
Chai Y, Chu F, Kolter R, Losick R (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67(2):254–263. https://doi.org/10.1111/j.1365-2958.2007.06040.x
Chen HL, Lee YS, Wei YH, Juang RS (2008) Purification of surfactin in pretreated fermentation broths by adsorptive removal of impurities. Biochem Eng J 40(3):452–459. https://doi.org/10.1016/j.bej.2008.01.020
Chen WC, Juang RS, Wei YH (2015) Applications of a lipopeptide biosurfactant, surfactin, produced by microorganisms. Biochem Eng J 103:158–169. https://doi.org/10.1016/j.bej.2015.07.009
Chen B, Wen J, Zhao X, Ding J, Qi G (2020a) Surfactin: a quorum-sensing signal molecule to relieve CCR in Bacillus amyloliquefaciens. Front Microbiol 11:631. https://doi.org/10.3389/fmicb.2020.00631
Chen L, Chong XY, Zhang YY, Lv YY, Hu YS (2020b) Genome shuffling of Bacillus velezensis for enhanced surfactin production and variation analysis. Curr Microbiol 77:71–78. https://doi.org/10.1007/s00284-019-01807-4
Chen XY, Zhao HY, Meng FQ, Zhou LB, Lu ZX, Lu YJ (2023) Surfactin alleviated hyperglycaemia in mice with type 2 diabetes induced by a high-fat diet and streptozotocin. Food Sci Hum Wellenss 12:2095–2110. https://doi.org/10.1016/j.fshw.2023.03.012
Chowdhury T, Baindara P, Mandal SM (2021) LPD-12: a promising lipopeptide to control COVID-19. Int J Antimicrob Ag 57(1):106218. https://doi.org/10.1016/j.ijantimicag.2020.106218
Christensen QH, Martin N, Mansilla MC, de Mendoza D, Cronan JE (2011) A novel amidotransferase required for lipoic acid cofactor assembly in Bacillus subtilis. Mol Microbiol 80(2):350–363. https://doi.org/10.1111/j.1365-2958.2011.07598.x
Chumsakul O, Takahashi H, Oshima T, Hishimoto T, Kanaya S, Ogasawara N, Ishikawa S (2011) Genome-wide binding profiles of the Bacillus subtilis transition state regulator AbrB and its homolog Abh reveals their interactive role in transcriptional regulation. Nucleic Acids Res 39(2):414–428. https://doi.org/10.1093/nar/gkq780
Ciurko D, Czyżnikowska Ż, Kancelista A, Łaba W, Janek T (2022) Sustainable production of biosurfactant from agro-industrial oil wastes by Bacillus subtilis and its potential application as antioxidant and ACE inhibitor. Int J Mol Sci 23(18):10824. https://doi.org/10.3390/ijrns231810824
Coutte F, Leclère V, Béchet M, Guez JS, Lecouturier D, Chollet-Imbert M, Dhulster P, Jacques P (2010) 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(2):480–491. https://doi.org/10.1111/j.1365-2672.2010.04683.x
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(8):1216–1234. https://doi.org/10.1002/biot.201400541
Dang Y, Zhao F, Liu X, Fan X, Huang R, Gao W, Wang SF, Yang C (2019) Enhanced production of antifungal lipopeptide iturin A by Bacillus amyloliquefaciens LL3 through metabolic engineering and culture conditions optimization. Microb Cell Fact 18(1):1–14. https://doi.org/10.1186/s12934-019-1121-1
de Araujo LV, Guimarães CR, da Silva Marquita RL, Santiago VM, de Souza MP, Nitschke M, Freire DMG (2016) Rhamnolipid and surfactin: anti-adhesion/antibiofilm and antimicrobial effects. Food Control 63:171–178. https://doi.org/10.1016/j.foodcont.2015.11.036
de Carvalho ST, Gomes WE, Tonon GC, Beatto TG, Spogis N, Cunha LHD, Lattaro BP, Nogueira AB, Mendes RK, Alvarenga DO, Etchegaray A (2021) Residual biomass from surfactin production is a source of arginase and adsorbed surfactin that is useful for environmental remediation. World J Microb Biot 37(7):1–12. https://doi.org/10.1007/s11274-021-03094-3
Dehghan-Noudeh G, Housaindokht M, Bazzaz BSF (2005) Isolation, characterization, and investigation of surface and hemolytic activities of a lipopeptide biosurfactant produced by Bacillus subtilis ATCC 6633. J Microbiol 43(3):272–276
Desai C, Patel P, Markande AR, Kamala K, Sivaperumal P (2020) Exploration of haloarchaea for their potential applications in food industry. Int J Environ Sci Technol 17(11):4455–4464. https://doi.org/10.1007/s13762-020-02773-2
Dhali D, Coutte F, Arias AA, Auger S, Bidnenko V, Chataigné G, Lalk M, Niehren J, de Sousa J, Versari C, Jacques P (2017) Genetic engineering of the branched fatty acid metabolic pathway of Bacillus subtilis for the overproduction of surfactin C14 isoform. Biotechnol J 12(7):1600574. https://doi.org/10.1002/biot.201600574
Dong F, Ren SY, Liu JC, Bilal M, Li B, Chen X, Liu XH, Zhong HJ, Zang SS, Yuan MX, Luo CP, Jiang J (2022) Transcriptome investigation on the multicellular behavior of Bacillus velezensis Bs916 anchoring surfactin. J Appl Microbiol 134:1–14. https://doi.org/10.1093/jambio/lxac016
Durval I, Rufino R, Sarubbo L (2021) Biosurfactant as an environmental remediation agent: toxicity, formulation, and application in the removal of petroderivate in sand and rock walls. Biointerface Res Appl Chem 12:34–48. https://doi.org/10.33263/BRIAC121.034048
Even-Tov E, Omer Bendori S, Pollak S, Eldar A (2016) Transient duplication-dependent divergence and horizontal transfer underlie the evolutionary dynamics of bacterial cell–cell signaling. PLoS Biol 14(12):e2000330. https://doi.org/10.1371/journal.pbio.2000330
Fagerlund A, Dubois T, Økstad OA, Verplaetse E, Gilois N, Bennaceur I, Stéphane P, Myriam G, Stéphane A, Anne-Brit K (2014) SinR controls enterotoxin expression in Bacillus thuringiensis biofilms. PLoS ONE 9(1):e87532. https://doi.org/10.1371/journal.pone.0087532
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 1044:214–224. https://doi.org/10.1016/j.jchromb.2016.11.013
Guo QG, Dong LH, Wang PP, Li SZ, Zhao WS, Lu XY, Zhang XY, Ma P (2018) The PhoR/PhoP two-component system regulates fengycin production in Bacillus subtilis NCD-2 under low-phosphate conditions. J Integr Agric 17(1):149–157. https://doi.org/10.1016/S2095-3119(17)61669-1
Hamoen LW, Venema G, Kuipers OP (2003) Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology 149(1):9–17. https://doi.org/10.1099/mic.0.26003-0
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(19):6659–6667. https://doi.org/10.1128/JB.187.19.6659-6667.2005
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(6):1714–1729. https://doi.org/10.1111/j.1365-2958.2006.05059.x
Hofemeister J, Conrad B, Adler B, Hofemeister B, Feesche J, Kucheryava N, Steinborn G, Franke P, Grammel N, Zwintscher A, Leenders F, Hitzeroth G, Vater J (2004) Genetic analysis of the biosynthesis of non-ribosomal peptide- and polyketide-like antibiotics, iron uptake and biofilm formation by Bacillus subtilis a1/3. Mol Genet Genomics 272(4):363–378. https://doi.org/10.1007/s00438-004-1056-y
Hoffmann M, Mück D, Grossmann L, Greiner L, Klausmann P, Henkel M, Lilge L, Weiss J, Hausmann R (2021) Surfactin from Bacillus subtilis displays promising characteristics as O/W-emulsifier for food formulations. Colloid Surface B 203:111749. https://doi.org/10.1016/j.colsurfb.2021.111749
Hu FX, Liu YY, Li S (2019) Rational strain improvement for surfactin production: enhancing the yield and generating novel structures. Microb Cell Fact 18(1):1–13. https://doi.org/10.1186/s12934-019-1089-x
Hu FX, Liu YY, Lin JZ, Wang WD, Li S (2020) Efficient production of surfactin from xylose-rich corncob hydrolysate using genetically modified Bacillus subtilis 168. Appl Microbiol Biot 104(9):4017–4026. https://doi.org/10.1007/s00253-020-10528-9
Hwang MH, Kim MH, Gebru E, Jung BY, Lee SP, Park SC (2008) Killing rate curve and combination effects of surfactin C produced from Bacillus subtilis complex BC1212 against pathogenic Mycoplasma hyopneumoniae. World J Microbiol Biotechnol 24(10):2277–2282. https://doi.org/10.1007/s11274-008-9752-0
Isa MHM, Frazier RA, Jauregi P (2008) A further study of the recovery and purification of surfactin from fermentation broth by membrane filtration. Sep Purif Technol 64:176–182. https://doi.org/10.1016/j.seppur.2008.09.008
Ishikawa F, Konno S, Uchida C, Suzuki T, Takashima K, Dohmae N, Kakeya H, Tanabe G (2022) Chemoproteomics profiling of surfactin-producing nonribosomal peptide synthetases in living bacterial cells. Cell Chem Biol 29(1):145–156. https://doi.org/10.1016/j.chembiol.2021.05.014
Islam T, Rabbee MF, Choi J, Baek KH (2022) Biosynthesis, molecular gegulation, and application of bacilysin produced by Bacillus species. Metabolites 12(5):397. https://doi.org/10.3390/metabo12050397
Jasim B, Sreelakshmi KS, Mathew J, Radhakrishnan EK (2016) Surfactin, iturin, and fengycin biosynthesis by endophytic Bacillus sp. from Bacopa monnieri. Microb Ecol 72:106–119. https://doi.org/10.1007/s00248-016-0753-5
Jiang J, Gao L, Bie XM, Lu ZX, Liu HX, Zhang C, Lu FX, Zhao HZ (2016) Identification of novel surfactin derivatives from NRPS modification of Bacillus subtilis and its antifungal activity against Fusarium moniliforme. BMC Microbiol 16(1):1–14. https://doi.org/10.1186/s12866-016-0645-3
Jiao S, Li X, Yu H, Yang HM, Li X, Shen ZY (2017) In situ enhancement of surfactin biosynthesis in Bacillus subtilis using novel artificial inducible promoters. Biotechnol Bioeng 114(4):832–842. https://doi.org/10.1002/bit.26197
Jimoh AA, Lin J (2019) Biosurfactant: a new frontier for greener technology and environmental sustainability. Ecotox Environ Safe 184:109607. https://doi.org/10.1016/j.ecoenv.2019.109607
Jing YF, Wei HX, Liu FF, Liu YF, Zhou L, Liu JF, Yang SZ, Zhang HZ, Mu BZ (2022) Genetic engineering of the branched-chain fatty acid biosynthesis pathway to enhance surfactin production from Bacillus subtilis. Biotechnol Appl Biochem 70:238–248. https://doi.org/10.1002/bab.2346
Johnson A, Kong FB, Miao S, Thomas S, Ansar S, Kong ZL (2021) In-vitro antibacterial and anti-inflammatory effects of surfactin-loaded nanoparticles for periodontitis treatment. Nanomateri-Basel 11(2):356. https://doi.org/10.3390/nano11020356
Kalamara M, Spacapan M, Mandic-Mulec I, Stanley-Wall NR (2018) Social behaviours by Bacillus subtilis: quorum sensing, kin discrimination and beyond. Mol Microbiol 110(6):863–878. https://doi.org/10.1111/mmi.14127
Kaur G, Wang HM, To MH, Roelants SLKW, Soetaert W, Lin CSK (2019) Efficient sophorolipids production using food waste. J Clean Prod 232:1–11. https://doi.org/10.1016/j.jclepro.2019.05.326
Keller K, Friedmann T, Boxman A (2001) The bioseparation needs for tomorrow. Trends Biotechnol 19(11):438–441. https://doi.org/10.1016/S0167-7799(01)01803-0
Kisil OV, Trefilov VS, Sadykova VS, Zvereva ME, Kubareva EA (2023) Surfactin: its biological activity and possibility of application in agriculture. Appl Biochem Microbiol 59(1):1–13. https://doi.org/10.1134/S0003683823010027
Klausmann P, Hennemann K, Hoffmann M, Treinen C, Aschern M, Lilge L, Heravi KM, Henkel M, Hausmann R (2021a) Bacillus subtilis high cell density fermentation using a sporulation-deficient strain for the production of surfactin. Appl Microbiol Biotechnol 105(10):4141–4151. https://doi.org/10.1007/s00253-021-11330-x
Klausmann P, Lilge L, Aschern M, Hennemann K, Henkel M, Hausmann R, Heravi KM (2021b) Influence of B. subtilis 3NA mutations in spo0A and abrB on surfactin production in B. subtilis 168. Microbiol Cell Fact 20(1):1–15. https://doi.org/10.1186/s12934-021-01679-z
Kraas FI, Helmetag V, Wittmann M, Strieker M, Marahiel MA (2010) Functional dissection of surfactin synthetase initiation module reveals insights into the mechanism of lipoinitiation. Chem Biol 17(8):872–880. https://doi.org/10.1016/j.chembiol.2010.06.015
Kracht M, Rokos H, Ozel M, Kowall M, Pauli G, Vater J (1999) Antiviral and hemolytic activities of surfactin isoforms and their methyl ester derivatives. J Antibiot 52(7):613–619. https://doi.org/10.7164/antibiotics.52.613
Lazazzera BA, Solomon JM, Grossman AD (1997) An exported peptide functions intracellularly to contribute to cell density signaling in B. subtilis. Cell 89:917–925. https://doi.org/10.1016/S0092-8674(00)80277-9
Li YM, Yang SZ, Mu BZ (2010) The surfactin and lichenysin isoforms produced by Bacillus licheniformis HSN 221. Anal Lett 43(6):929–940. https://doi.org/10.1080/00032710903491047
Li X, Yang H, Zhang DL, Li X, Yu HM, Shen ZY (2015) Overexpression of specific proton motive force-dependent transporters facilitate the export of surfactin in Bacillus subtilis. J Ind Microbiol Biotechnol 42(1):93–103. https://doi.org/10.1007/s10295-014-1527-z
Li DM, Wang Y, Chen C, Zeng MB, Li QR, Jia QY, Liu XL, Hou YY, Fan CM, Chen YH, Hu ZM (2022) Advances in several important antimicrobial lipopeptids from Bacillus spp. Chin J Biotechnol 38(5):1768–1783. https://doi.org/10.13345/j.cjb.220001
Liang Z, Qiao JQ, Li PP, Zhang LL, Qiao ZX, Lin L, Yu CJ, Yang Y, Zubair M, Gu Q, Wu HJ, Borriss R, Gao XW (2020) A novel Rap-Phr system in Bacillus velezensis NAU-B3 regulates surfactin production and sporulation via interaction with ComA. Appl Microbiol Biotechnol 104:10059–10074. https://doi.org/10.1007/s00253-020-10942-z
Liu JF, Yang J, Yang SZ, Ye RQ, Mu BZ (2012) Effects of different amino acids in culture media on surfactin variants produced by Bacillus subtilis TD7. Appl Biochem Biotechnol 166(8):2091–2100. https://doi.org/10.1007/s12010-012-9636-5
Liu N, Chen B, Zhao XY, Wen JH, Qi GF (2022a) Cations and surfactin serving as signal molecules trigger quorum sensing in Bacillus amyloliquefaciens. J Basic Microbiol 62(1):35–47. https://doi.org/10.1002/jobm.202100315
Liu W, Li Y, Du CM (2022b) Biosynthesis and molecular regulation of microbial lipopeptides. J Biochem Mol Biol 38:1630–1639. https://doi.org/10.13865/j.cnki.cjbmb.2022.05.1571
Long XW, Ne N, He YK, Jiang JJ, Wu TY (2017) Biosurfactant surfactin with pH-regulated emulsification activity for efficient oil separation when used as emulsifier. Bioresour Technol 241:200–206. https://doi.org/10.1016/j.biortech.2017.05.120
Lopez D, Vlamakis H, Losick R, Kolter R (2009) Paracrine signaling in a bacterium. Gene Dev 23(14):1631–1638. https://doi.org/10.1101/gad.1813709
Lv ZT, Qian C, Liu YN, Lv YH, Liu XW (2022) Optical tracking of surfactant-tuned bacterial adhesion: a single-cell imaging study. Appl Environ Microbiol 88(23):ce0162622. https://doi.org/10.1128/aem.01626-22
Manoj SR, Karthik C, Kadirvelu K, Arulselvi PI, Shanmugasundaram T, Bruno B, Rajkumar M (2020) Understanding the molecular mechanisms for the enhanced phytoremediation of heavy metals through plant growth promoting rhizobacteria: a review. J Environ Manag 254:109779. https://doi.org/10.1016/j.jenvman.2019.109779
Marlow VL, Porter M, Hobley L, Kiley TB, Swedlow JR, Davidson FA, Stanley-Wall NR (2014) Phosphorylated DegU manipulates cell fate differentiation in the Bacillus subtilis biofilm. J Bacteriol 196(1):16–27. https://doi.org/10.1128/JB.00930-13
Matsuoka H, Hirooka K, Fujita Y (2007) Organization and function of the YsiA regulon of Bacillus subtilis involved in fatty acid degradation. J Biol Chem 282(8):5180–5194. https://doi.org/10.1074/jbc.M606831200
Miras M, Dubnau D (2016) A DegU-P and DegQ-dependent regulatory pathway for the K-state in Bacillus subtilis. Front Microbiol 7:1868. https://doi.org/10.3389/fmicb.2016.01868
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(12):3055–3064. https://doi.org/10.1002/jsfa.6139
Mubarak MQE, Hassan AR, Hamid AA, Khalil S, Isa MHM (2015) A simple and effective isocratic HPLC method for fast identification and quantification of surfactin. Sains Malays 44(1):115–120. https://doi.org/10.17576/jsm-2015-4401-16
Mülner P, Schwarz E, Dietel K, Junge H, Herfort S, Weydmann M, Lasch P, Cernava T, Berg G, Vater J (2020) Profiling for bioactive peptides and volatiles of plant growth promoting strains of the Bacillus subtilis complex of industrial relevance. Front Microbiol 11:1432. https://doi.org/10.3389/fmicb.2020.01432
Park JH, Lee SY (2010) Metabolic pathways and fermentative production of L-aspartate family amino acids. Biotechnol J 5(6):560–577. https://doi.org/10.1002/biot.201000032
Pedreira T, Elfmann C, Stülke J (2022) The current state of SubtiWiki, the database for the model organism Bacillus subtilis. Nucleic Acids Res 50:D875–D882. https://doi.org/10.1093/nar/gkab943
Peng XX, Wang SS, Fu C, Hu CH, Liao GJ (2018) Current status and future perspectives of daptomycin development. Acta Pharm Sin 53(6):839–844. https://doi.org/10.16438/j.0513-4870.2018-0096
Phulpoto IA, Yu ZS, Hu BW, Wang YF, Ndayisenga F, Li JM, Liang HX, Qazi MA (2020) Production and characterization of surfactin-like biosurfactant produced by novel strain Bacillus nealsonii S2MT and it’s potential for oil contaminated soil remediation. Microb Cell Fact 19(1):1–12. https://doi.org/10.1186/s12934-020-01402-4
Qin YX, Angelini LL, Chai YR (2022) Bacillus subtilis cell differentiation, biofilm formation and environmental prevalence. Microorganisms 10(6):1108. https://doi.org/10.3390/microorganisms10061108
Rahman FB, Sarkar B, Moni R, Rahman MS (2021) Molecular genetics of surfactin and its effects on different sub-populations of Bacillus subtilis. Biotechnol Rep 32:e00686. https://doi.org/10.1016/j.btre.2021.e00686
Rivardo F, Turner RJ, Allegrone G, Ceri H, Martinotti MG (2009) Anti-adhesion activity of two biosurfactants produced by Bacillus spp. prevents biofilm formation of human bacterial pathogens. AMI 83:541–553. https://doi.org/10.1007/s00253-009-1987-7
Robbel L, Marahiel MA (2010) Daptomycin, a bacterial lipopeptide synthesized by a nonribosomal machinery. J Bio Chem 285(36):27501–27508. https://doi.org/10.1074/jbc.R110.128181
Roongsawang N, Washio K, Morikawa M (2010) Diversity of nonribosomal peptide synthetases involved in the biosynthesis of lipopeptide biosurfactants. Int J Mol Sci 12(1):141–172. https://doi.org/10.3390/ijms12010141
Salzberg LI, Botella E, Hokamp K, Antelmann H, Maaß S, Becher D, Noone D, Devine KM (2015) Genome-wide analysis of phosphorylated PhoP binding to chromosomal DNA reveals several novel features of the PhoPR-mediated phosphate limitation response in Bacillus subtilis. J Bacteriol 197(8):1492–1506. https://doi.org/10.1128/JB.02570-14
Sarubbo LA, Silva MDC, Durval IJB, Bezerra KGO, Ribeiro BG, Silva IA, Twigg MS, Banat IM (2022) Biosurfactants: production, properties, applications, trends, and general perspectives. Biochem Eng J 181:108377. https://doi.org/10.1016/j.bej.2022.108377
Schneider A, Stachelhaus T, Marahiel MA (1998) Targeted alteration of the substrate specificity of peptide synthetases by rational module swapping. Mol Gen Genet 257(3):308–318. https://doi.org/10.1007/s004380050652
Selvam R, Maheswari P, Kavitha P, Ravichandran M, Sas B, Ramchand CN (2009) Effect of Bacillus subtilis PB6, a natural probiotic on colon mucosal inflammation and plasma cytokines levels in inflammatory bowel disease. Indian J Biochem Bio 46(1):79–85
Seydlová G, Svobodová J (2008) Review of surfactin chemical properties and the potential biomedical applications. Cent Eur J Med 3(2):123–133. https://doi.org/10.2478/s11536-008-0002-5
Sharma P, Rekhi P, Kumari S, Debnath M (2022) Deciphering the molecular diversity of related halophilic Bacillus sp. isolated from Sambhar Lake and the functional characterizations of surfactin. J Surfactants Deterg 25:757–774. https://doi.org/10.1002/jsde.12611
Shivers RP, Sonenshein AL (2004) Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol Microbiol 53(2):599–611. https://doi.org/10.1111/j.1365-2958.2004.04135.x
Silva MTS, Soares CMF, Lima AS, Santana CC (2015) Integral production and concentration of surfactin from Bacillus sp. ITP-001 by semi-batch foam fractionation. Biochem Eng J 104:91–97. https://doi.org/10.1016/j.bej.2015.04.010
Sonenshein AL (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5(12):917–927. https://doi.org/10.1038/nrmicro1772
Sun J, Qian SQ, Lu J, Liu YN, Lu FX, Bie XM, Lu ZX (2018) Knockout of rapC improves the bacillomycin D yield based on de novo genome sequencing of Bacillus amyloliquefaciens fmbJ. J Agr Food Chem 66:4422–4430. https://doi.org/10.1021/acs.jafc.8b00418
Sun J, Liu Y, Lin F, Lu Z, Lu Y (2021) CodY, ComA, DegU and Spo0A controlling lipopeptides biosynthesis in Bacillus amyloliquefaciens fmbJ. J Appl Microbiol 131(3):1289–1304. https://doi.org/10.1111/jam.15007
Taira T, Yanagisawa S, Imura T (2021) Influence of inorganic and organic counter-cations on the surface properties and self-assembly of cyclic lipopeptide surfactin. Colloid Surface A 626:126973. https://doi.org/10.1021/acs.jafc.8b00418
Tolibia SEM, Pacheco AD, Balbuena SYG, Rocha J, Lopez VE (2023) Engineering of global transcription factors in Bacillus, a genetic tool for increasing product yields: a bioprocess overview. World J Microd Biotechnol 39(1):12. https://doi.org/10.1007/s11274-022-03460-9
Tsuge K, Ano T, Shoda M (1996) Isolation of a gene essential for biosynthesis of the lipopeptide antibiotics plipastatin B1 and surfactin in Bacillus subtilis YB8. Arch Microbiol 165(4):243–251. https://doi.org/10.1007/s002030050322
Vahidinasab M, Lilge L, Reinfurt A, Pfannstiel J, Henkel M, Heravi KM, Hausmann R (2020) Construction and description of a constitutive plipastatin mono-producing Bacillus subtilis. Microb Cell Fact 19(1):1–12. https://doi.org/10.1186/s12934-020-01468-0
Vo TTT, Liu JF, Wu CZ, Lin WN, Chen YL, Lee IT (2020) Surfactin from Bacillus subtilis induces apoptosis in human oral squamous cell carcinoma through ROS-regulated mitochondrial pathway. J Cancer 11(24):7253. https://doi.org/10.7150/jca.50835
Wang D, Wang Q, Qiu YM, Nomura CT, Li JH, Chen SW (2017) Untangling the transcription regulatory network of the bacitracin synthase operon in Bacillus licheniformis DW2. Res Microbiol 168(6):515–523. https://doi.org/10.1016/j.resmic.2017.02.010
Wang Q, Yu HM, Wang MM, Yang H, Shen ZY (2018) Enhanced biosynthesis and characterization of surfactin isoforms with engineered Bacillus subtilis through promoter replacement and Vitreoscilla hemoglobin co-expression. Process Biochem 70:36–44. https://doi.org/10.1016/j.procbio.2018.04.003
Wang CY, Cao YX, Wang YP, Sun LM, Song H (2019a) Enhancing surfactin production by using systematic CRISPRi repression to screen amino acid biosynthesis genes in Bacillus subtilis. Microb Cell Fact 18:1–13. https://doi.org/10.1186/s12934-019-1139-4
Wang M, Yu HM, Shen ZY (2019b) Antisense RNA-based strategy for enhancing surfactin production in Bacillus subtilis TS1726 via overexpression of the unconventional biotin Carboxylase II to enhance ACCase activity. Acs Synth Biol 8(2):251–256. https://doi.org/10.1021/acssynbio.8b00459
Wang XY, Chen ZY, Feng H, Chen X, Wei LH (2019c) Genetic variants of the oppA gene are involved in metabolic regulation of surfactin in Bacillus subtilis. Microb Cell Fact 18:1–12. https://doi.org/10.1186/s12934-019-1176-z
Wang MM, Yu HM, Li X, Shen ZY (2020a) Single-gene regulated non-spore-forming Bacillus subtilis: construction, transcriptome responses and applications for producing enzymes and surfactin. Metab Eng 62:235–248. https://doi.org/10.1016/j.ymben.2020.08.008
Wang MM, Yu HM, He X, Li YM, Yang HY (2020b) Construction and optimization of engineered Bacillus subtilis for surfactin production. Chin J Biotechnol 36(11):2377–2386. https://doi.org/10.13345/j.cjb.200156
Wang XW, Cai T, Wen WT, Ai JZ, Ai JY, Zhang ZH, Zhu L, George SC (2020c) Surfactin for enhanced removal of aromatic hydrocarbons during biodegradation of crude oil. Fuel 267:117272. https://doi.org/10.1016/j.fuel.2020.117272
Wen J, Zhao X, Si F, Qi G (2021) Surfactin, a quorum sensing signal molecule, globally affects the carbon metabolism in Bacillus amyloliquefaciens. Metab Eng Commun 12:e00174. https://doi.org/10.1016/j.mec.2021.e00174
Willenbacher J, Rau JT, Rogalla J, Syldatk C, Hausmann R (2015) Foam-free production of surfactin via anaerobic fermentation of Bacillus subtilis DSM 10(T). AMB Express 5:21. https://doi.org/10.1186/s13568-015-01352-21
Wolf D, Rippa V, Mobarec JC, Sauer P, Adlung L, Kolb P, Bischofs IB (2016) The quorum-sensing regulator ComA from Bacillus subtilis activates transcription using topologically distinct DNA motifs. Nucleic Acids Res 44(5):2160–2172. https://doi.org/10.1093/nar/gkv1242
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. https://doi.org/10.1016/j.ymben.2018.11.004
Xia L, Wen JP (2022) Available strategies for improving the biosynthesis of surfactin: a review. Crit Rev Biotechnol. https://doi.org/10.1080/07388551.2022.2095252
Xiong Y, Kong JQ, Yi SR, Feng XQ, Duan YW, Zhu XC (2020) Surfactin ameliorated the internalization and inhibitory performances of bleomycin family compounds in tumor cells. Mol Pharmaceut 17(6):2125–2134. https://doi.org/10.1021/acs.molpharmaceut.0c00281
Xu Y, Wu JY, Liu QJ, Xue JY (2023) Genome-wide identification and evolutionary analyses of SrfA operon genes in Bacillus. Genes-Basel 14(2):422. https://doi.org/10.3390/genes14020422
Yang RR, Lei SZ, Xu XG, Jin H, Sun H, Zhao XX, Pang B, Shi JL (2020a) Key elements and regulation strategies of NRPSs for biosynthesis of lipopeptides by Bacillus. Appl Microbiol Biotechnol 104(19):8077–8087. https://doi.org/10.1007/s00253-020-10801-x
Yang ZY, Zu YQ, Zhu JS, Jin MJ, Cui TY, Long XW (2020b) Application of biosurfactant surfactin as a pH-switchable biodemulsifier for efficient oil recovery from waste crude oil. Chemosphere 240:124946. https://doi.org/10.1016/j.chemosphere.2019.124946
Yaseen Y, Gancel F, Drider D, Béchet M, Jacques P (2016) Influence of promoters on the production of fengycin in Bacillus spp. Res Microbiol 167(4):272–281. https://doi.org/10.1016/j.resmic.2016.01.008
Yaseen Y, Diop A, Gancel F, Béchet M, Jacques P, Drider D (2018) Polynucleotide phosphorylase is involved in the control of lipopeptide fengycin production in Bacillus subtilis. Arch Microbiol 200(5):783–791. https://doi.org/10.1007/s00203-018-1483-5
Yi GB, Liu Q, Lin JZ, Wang WD, Huang H, Li S (2017) Repeated batch fermentation for surfactin production with immobilized Bacillus subtilis BS-37: two-stage pH control and foam fractionation. J Chem Technol Biot 92(3):530–535. https://doi.org/10.1002/jctb.5028
Zanotto AW, Valerio A, de Andrade CJ, Pastore GM (2019) New sustainable alternatives to reduce the production costs for surfactin 50 years after the discovery. Appl Microbiol Biotechnol 103:8647–8656. https://doi.org/10.1007/s00253-019-10123-7
Zhang L, Xing XY, Ding J, Zhao XY, Qi GF (2017) Surfactin variants for intra-intestinal delivery of insulin. Eur J Pharm Biopharm 115:218–228. https://doi.org/10.1016/j.ejpb.2017.03.005
Zhang F, Huo KY, Song XY, Quan YF, Wang SF, Zhang ZL, Gao WX, Yang C (2020) Engineering of a genome-reduced strain Bacillus amyloliquefaciens for enhancing surfactin production. Microb Cell Fact 19:1–13. https://doi.org/10.1186/s12934-020-01485-z
Zhang Y, Qi JS, Wang YQ, Wen JH, Zhao XY, Qi GF (2022) Comparative study of the role of surfactin-triggered signalling in biofilm formation among different Bacillus species. Microbiol Res 254:126920. https://doi.org/10.1016/j.micres.2021.126920
Zhen C, Ge XF, Lu YT, Liu WZ (2023) Chemical structure, properties and potential applications of surfactin, as well as advanced strategies for improving its microbial production. AIMS Microbiol 9(2):195–217. https://doi.org/10.3934/microbiol.2023012
Zhi Y, Wu Q, Xu Y (2017) Genome and transcriptome analysis of surfactin biosynthesis in Bacillus amyloliquefaciens MT45. Sci Rep-Uk 7:1–13. https://doi.org/10.1038/srep40976
Zhou DY, Hu FX, Lin JZ, Wang WD, Li S (2019) Genome and transcriptome analysis of Bacillus velezensis BS-37, an efficient surfactin producer from glycerol, in response to d-/l-leucine. MicrobiologyOpen 8(8):e00794. https://doi.org/10.1002/mbo3.794
Zhou YJ, Yang XX, Li Q, Peng Z, Li JH, Zhang J (2023) Optimization of fermentation conditions for surfactin production by B. subtilis YPS-32. BMC Microbiol 23(1):1–12. https://doi.org/10.1186/s12866-023-02838-5
Zhuravleva OI, Afiyatullov SS, Ermakova SP, Nedashkovskaya OI, Dmitrenok PS, Denisenko VA, Kuznetsova TA (2010) New C 14-surfactin methyl ester from the marine bacterium Bacillus pumilus KMM 456. Russ Chem B+ 59(11):2137–2142. https://doi.org/10.1007/s11172-010-0369-8
Zouari R, Besbes S, Ellouze-Chaabouni S, Ghribi-Aydi D, Ellouze-Chaabouni S (2016) Cookies from composite wheat–sesame peels flours: dough quality and effect of Bacillus subtilis SPB1 biosurfactant addition. Food Chem 194:758–769. https://doi.org/10.1016/j.foodchem.2015.08.064
Funding
This research was supported by the National Natural Science Foundation of China (Project No. 32172468) and Heilongjiang University Graduate Innovation Research Project (YJSCX2022-092HLJU).
Author information
Authors and Affiliations
Contributions
XQ (conceptualization, writing—original draft), WL (conceptualization, writing—original draft), XH (writing—review and editing), CD (conceptualization, writing—review and editing).
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Ethics approval
Not applicable.
Additional information
Communicated by Yusuf Akhter.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Qi, X., Liu, W., He, X. et al. A review on surfactin: molecular regulation of biosynthesis. Arch Microbiol 205, 313 (2023). https://doi.org/10.1007/s00203-023-03652-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03652-3