LUO Xiaojiao, SUN Jing, LU Yingjian. Research Progress in the Biosynthesis, Antimicrobial Mechanism, and Application of Lipopeptides in Bacillus amyloliquefaciens[J]. Science and Technology of Food Industry, 2022, 43(19): 462−470. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2021100259.
Citation: LUO Xiaojiao, SUN Jing, LU Yingjian. Research Progress in the Biosynthesis, Antimicrobial Mechanism, and Application of Lipopeptides in Bacillus amyloliquefaciens[J]. Science and Technology of Food Industry, 2022, 43(19): 462−470. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2021100259.

Research Progress in the Biosynthesis, Antimicrobial Mechanism, and Application of Lipopeptides in Bacillus amyloliquefaciens

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  • Received Date: October 25, 2021
  • Available Online: July 31, 2022
  • Bacillus amyloliquefaciens (B. amyloliquefaciens) is widely used as beneficial bacteria for biological control, and the main antimicrobial substances are lipopeptides. These lipopeptides have antimicrobial, anti-tumor, antiviral activities and other biological activities, and they are safe, broad-spectrum, efficient, non-toxic, and easily decomposed in the body. Therefore, B. amyloliquefaciens and its lipopeptide metabolites can be widely used in the biological control of crops, freshness and preservation of fruits and vegetables, as well as post-harvest microbial control, which have great prospects for development and application. This paper focuses on the types and biosynthesis of lipopeptides in B. amyloliquefaciens, the mechanism of microbial inhibition and their application prospects.
  • [1]
    冯蓉, 刘丽, 陈海念, 等. 解淀粉芽孢杆菌F11抗真菌活性研究[J]. 农业资源与环境学报,2021,38(5):849−857. [FENG R, LIU L, CHEN H N, et al. Study on antifungal activity of Bacillus amyloliquefaciens F11[J]. Journal of Agricultural Resources and Environment,2021,38(5):849−857.

    FENG R, LIU L, CHEN H N, et al. Study on antifungal activity of Bacillusamyloliquefaciens F11[J]. Journal of Agricultural Resources and Environment, 2021, 38(5): 849-857.
    [2]
    张荣胜, 王晓宇, 罗楚平, 等. 解淀粉芽孢杆菌Lx-11产脂肽类物质鉴定及表面活性素对水稻细菌性条斑病的防治作用[J]. 中国农业科学,2013,46(10):2014−2021. [ZHANG R S, WANG X Y, LUO C P, et al. Identification of lipopeptides from Bacillus amyloliquefaciens Lx-11 and biocontrol efficacy of surfactin against bacterial leaf streak[J]. Scientia Agricultura Sinica,2013,46(10):2014−2021.

    ZHANG R S, WANG X Y, LUO C P, et al. Identification of lipopeptides from Bacillus amyloliquefaciens Lx-11 and biocontrol efficacy of Surfactin against bacterial leaf streak[J]. Scientia Agricultura Sinica, 2013, 46(10): 2014-2021.
    [3]
    张静, 冉晓潇, 朱天辉, 等. 解淀粉芽孢杆菌对山茶灰斑病菌的抑制作用[J]. 东北林业大学学报,2014,42(7):122−125. [ZHANG J, RAN X X, ZHU T H, et al. Bacillus amyloliquefaciens antimicrobial effect on Pestalotiopsis guepini (Desm.)[J]. Journal of Northeast Forestry University,2014,42(7):122−125.

    ZHANG J, RAN X X, ZHU T H, et al. Bacillus amyloliquefaciens antimicrobial effect on Pestalotiopsis guepini (Desm. )[J]. Journal of Northeast Forestry University, 2014, 42(7): 122-125
    [4]
    YAN F, LI C, YE X, et al. Antifungal activity of lipopeptides from Bacillus amyloliquefaciens MG3 against Colletotrichum gloeosporioides in loquat fruits[J]. Biological Control,2020,146:104281. doi: 10.1016/j.biocontrol.2020.104281
    [5]
    BELTRAN-GRACIA E, MACEDO-RAYGOZA G, VILLAFAÑA-ROJAS J, et al. Production of lipopeptides by fermentation processes: Endophytic bacteria, fermentation strategies and easy methods for bacterial selection[M]. Fermentation Processes, 2017, 8: 1138.
    [6]
    PENHA R O, VANDENBERGHE L P S, FAULDS C, et al. Bacillus lipopeptides as powerful pest control agents for a more sustainable and healthy agriculture: Recent studies and innovations[J]. Planta,2020,251(3):70. doi: 10.1007/s00425-020-03357-7
    [7]
    YANG R, LEI S, XU X, et al. Key elements and regulation strategies of NRPSs for biosynthesis of lipopeptides by Bacillus[J]. Appl Microbiol Biotechnol,2020,104(19):8077−8087. doi: 10.1007/s00253-020-10801-x
    [8]
    DUNLAP C A, BOWMAN M J, ROONEY A P. Iturinic lipopeptide diversity in the Bacillus subtilis species group-important antifungals for plant disease biocontrol applications[J]. Front Microbiol,2019,10:1794. doi: 10.3389/fmicb.2019.01794
    [9]
    严婉荣, 肖敏, 陈圆, 等. 解淀粉芽孢杆菌抗菌脂肽研究进展[J]. 北方园艺,2018(7):162−167. [YAN W R, XIAO M, CHEN Y, et al. Research progress in antimicrobial lipopeptides of Bacillus amyloliquefaciens[J]. Northern Horticulture,2018(7):162−167.

    YAN W R, XIAO M, CHEN Y, et al. Research progress in antimicrobial lipopeptides of Bacillus amyloliquefaciens[J]. Northern Horticulture, 2018(7): 162-167.
    [10]
    刘昆昂, 郝楠, 李海立, 等. 生防解淀粉芽胞杆菌的研究进展[J]. 微生物学杂志,2017,37(5):98−102. [LIU K A, HAO N, LI H L, et al. Advances in Bacillus amyloliquefaciens for biocontrol[J]. Journal of Microbiology,2017,37(5):98−102.

    LIU K A, HAO N, LI H L, et al. Advances in Bacillus amyloliquefaciens for biocontrol[J]. Journal of Microbiology, 2017, 37(5): 98-102.
    [11]
    JIN P, WANG H, TAN Z, et al. Antifungal mechanism of bacillomycin D from Bacillus velezensis HN-2 against Colletotrichum gloeosporioides Penz[J]. Pesticide Biochemistry and Physiology,2020,163:102−107. doi: 10.1016/j.pestbp.2019.11.004
    [12]
    QIAN S, LU H, SUN J, et al. Antifungal activity mode of Aspergillus ochraceus by bacillomycin D and its inhibition of ochratoxin A (OTA) production in food samples[J]. Food Control,2016,60:281−288. doi: 10.1016/j.foodcont.2015.08.006
    [13]
    SUN J, LI W, LIU Y, et al. Growth inhibition of Fusarium graminearum and reduction of deoxynivalenol production in wheat grain by bacillomycin D[J]. Journal of Stored Products Research,2018,75:21−28. doi: 10.1016/j.jspr.2017.11.002
    [14]
    WU L, WU H, CHEN L, et al. Difficidin and bacilysin from Bacillus amyloliquefaciens FZB42 have antibacterial activity against xanthomonas oryzae rice pathogens[J]. Scientific Reports,2015,5:12975. doi: 10.1038/srep12975
    [15]
    汪静杰, 赵东洋, 刘永贵, 等. 解淀粉芽孢杆菌SWB16菌株脂肽类代谢产物对球孢白僵菌的拮抗作用[J]. 微生物学报,2014,54(7):778−785. [WANG J J, ZHAO D Y, LIU Y G, et al. Antagonism against Beauveria bassiana by lipopeptide metabolites produced by entophyte Bacillus amyloliquefaciens strain SWB16[J]. Acta Microbiologica Sinica,2014,54(7):778−785.

    WANG J J, ZHAO D Y, LIU Y G, et al. Antagonism against Beauveria bassiana by lipopeptide metabolites produced by entophyte Bacillus amyloliquefaciens strain SWB16[J]. Acta Microbiologica Sinica, 2014, 54(7): 778-785.
    [16]
    LIU Y, LU J, SUN J, et al. C16-Fengycin A affect the growth of Candida albicans by destroying its cell wall and accumulating reactive oxygen species[J]. Applied Biochemistry and Biotechnology,2019,103(21-22):8963−8975.
    [17]
    YUAN B, JIA H, BU W, et al. A new chitosan sub-micron and encapsulated iturin A with enhanced antifungal activity against Ceratocystis fimbriata and Rhizopus strolonifer[J]. Int J Biol Macromol,2020,159:995−1003. doi: 10.1016/j.ijbiomac.2020.05.116
    [18]
    SUN J, QIAN S, LU J, et al. Knockout of rapC improves the bacillomycin D yield based on de novo genome sequencing of Bacillus amyloliquefaciens fmbJ[J]. Journal of Agricultural and Food Chemistry,2018,66(17):4422−4430. doi: 10.1021/acs.jafc.8b00418
    [19]
    MOYNE A L, CLEVELAND T E, TUZUN S. Molecular characterization and analysis of the operon encoding the antifungal lipopeptide bacillomycin D[J]. FEMS Microbiol Lett,2004,234(1):43−49. doi: 10.1111/j.1574-6968.2004.tb09511.x
    [20]
    WANG Y, ZHANG C, LIANG J, et al. Iturin A extracted from Bacillus subtilis WL-2 affects phytophthora infestans via cell structure disruption, oxidative stress, and energy supply dysfunction[J]. Front Microbiol,2020,11:536083. doi: 10.3389/fmicb.2020.536083
    [21]
    AMBRICO A, TRUPO M, MAGARELLI R A. Influence of phenotypic dissociation in Bacillus subtilis Strain ET-1 on iturin A production[J]. Current Microbiology,2019,76(12):1487−1494. doi: 10.1007/s00284-019-01764-y
    [22]
    ZHANG L, GAO Z, ZHAO X, et al. A natural lipopeptide of surfactin for oral delivery of insulin[J]. Drug Deliv,2016,23(6):2084−2093. doi: 10.3109/10717544.2016.1153745
    [23]
    LIANG Z, QIAO J Q, LI P P, et al. A novel Rap-Phr system in Bacillus velezensis NAU-B3 regulates surfactin production and sporulation via interaction with ComA[J]. Appl Microbiol Biotechnol,2020,104(23):10059−10074. doi: 10.1007/s00253-020-10942-z
    [24]
    MONTASTRUC L, LIU T, GANCEL F, et al. Integrated process for production of surfactin Part 2. Equilibrium and kinetic study of surfactin adsorption onto activated carbon[J]. Biochemical Engineering Journal,2008,38(3):349−354. doi: 10.1016/j.bej.2007.07.023
    [25]
    ASATUROVA A, PAVLOVA M, ASATUROVA A, et al. Physiological and biochemical aspects of the fungicidal action of promising biocontrol Bacillus subtilis strains against phytopathogenic fungi Fusarium and Pyrenophora[J]. BIO Web of Conferences,2020,21:00016. doi: 10.1051/bioconf/20202100016
    [26]
    HANIF A, ZHANG F, LI P, et al. Fengycin produced by Bacillus amyloliquefaciens FZB42 inhibits Fusarium graminearum growth and mycotoxins biosynthesis[J]. Toxins (Basel),2019,11(5):295. doi: 10.3390/toxins11050295
    [27]
    YASEEN Y, GANCEL F, DRIDER D, et al. Influence of promoters on the production of fengycin in Bacillus spp[J]. Research in Microbiology,2016,167(4):272−281. doi: 10.1016/j.resmic.2016.01.008
    [28]
    WANG Y, ZHANG C, LIANG J, et al. Surfactin and fengycin B extracted from Bacillus pumilus W-7 provide protection against potato late blight via distinct and synergistic mechanisms[J]. Appl Microbiol Biotechnol,2020,104(17):7467−7481. doi: 10.1007/s00253-020-10773-y
    [29]
    CAULIER S, NANNAN C, GILLIS A, et al. Overview of the atimicrobial compounds produced by members of the Bacillus subtilis group[J]. Front Microbiol,2019,10:302. doi: 10.3389/fmicb.2019.00302
    [30]
    李红玲. 非核糖体肽合成酶结构研究进展[J]. 临床合理用药杂志,2013,6(28):180−181. [LI H L. Research progress on structure of non-ribosomal peptide synthase[J]. Chinese Journal of Clinical Rational Drug Use,2013,6(28):180−181.

    LI H L. Research progress on structure of non-ribosomal peptide synthase[J]. Chinese Journal of Clinical Rational Drug Use, 2013, 6(28): 180-181.
    [31]
    ONGENA M, JACQUES P. Bacillus lipopeptides: Versatile weapons for plant disease biocontrol[J]. Trends Microbiol,2008,16(3):115−125. doi: 10.1016/j.tim.2007.12.009
    [32]
    ZHANG Z, DING Z T, ZHONG J, et al. Improvement of iturin A production in Bacillus subtilis ZK0 by overexpression of the comA and sigA genes[J]. Lett Appl Microbiol,2017,64(6):452−458. doi: 10.1111/lam.12739
    [33]
    JIN H, LI K, NIU Y, et al. Continuous enhancement of iturin A production by Bacillus subtilis with a stepwise two-stage glucose feeding strategy[J]. BMC Biotechnol,2015,15(1):1−9. doi: 10.1186/s12896-015-0115-2
    [34]
    LU J Y, ZHOU K, HUANG W T, et al. A comprehensive genomic and growth proteomic analysis of antitumor lipopeptide bacillomycin Lb biosynthesis in Bacillus amyloliquefaciens X030[J]. Applied Microbiology and Biotechnology,2019,103(18):7647−7662. doi: 10.1007/s00253-019-10019-6
    [35]
    RAJENDRAN, NARAYANAN, A M. Multifunctional peptide synthetases required for nonribosomal biosynthesis of peptide antibiotics[J]. Chemistry, Molecular Sciences and Chemical Engineering,1999,4:195−220.
    [36]
    SAMEL S A, WAGNER B, MARAHIEL M A, et al. The thioesterase domain of the fengycin biosynthesis cluster: A structural base for the macrocyclization of a non-ribosomal lipopeptide[J]. Journal of Molecular Biology,2006,359(4):876−889. doi: 10.1016/j.jmb.2006.03.062
    [37]
    DENG Q, WANG R D, SUN D F, et al. Complete genome of Bacillus velezensis CMT-6 and comparative genome analysis reveals lipopeptide diversity[J]. Biochemical Genetics,2020,58(1):1−15. doi: 10.1007/s10528-019-09927-z
    [38]
    LYU J, DA R, CHENG Y, et al. Mechanism of antibacterial activity of Bacillus amyloliquefaciens C-1 lipopeptide toward anaerobic Clostridium difficile[J]. Biomed Res Int,2020,2020:3104613.
    [39]
    SCHOFIELD B J, SKARSHEWSKI A, LACHNER N, et al. Near complete genome sequence of the animal feed probiotic, Bacillus amyloliquefaciens H57[J]. Stand Genomic Sci,2016,11(1):60. doi: 10.1186/s40793-016-0189-z
    [40]
    贺海滨, 苏峻冬, 滕凯, 等. 解淀粉芽孢杆菌研究进展[J]. 现代农业科技,2021(2):101−104. [HE H B, SU J D, TENG K, et al. Research progresson Bacillus amyloliquefaciens[J]. Modern Agricultural Science and Technology,2021(2):101−104.

    HE H B, SU J D, TENG K, et al. Research Progresson Bacillus amyloliquefaciens[J]. Modern Agricultural Science and Technology, 2021, (2): 101-104.
    [41]
    SUCHODOLSKI J, DERKACZ D, MURASZKO J, et al. Fluconazole and lipopeptide surfactin interplay during Candida albicans plasma membrane and cell wall remodeling increases fungal immune system exposure[J]. Pharmaceutics,2020,12(4):314. doi: 10.3390/pharmaceutics12040314
    [42]
    YAMASAKI R, KAWANO A, YOSHIOKA Y, et al. Rhamnolipids and surfactin inhibit the growth or formation of oral bacterial biofilm[J]. BMC Microbiol,2020,20(1):358. doi: 10.1186/s12866-020-02034-9
    [43]
    FARZAND A, MOOSA A, ZUBAIR M, et al. Suppression of sclerotinia sclerotiorum by the induction of systemic resistance and regulation of antioxidant pathways in tomato using fengycin produced by Bacillus amyloliquefaciens FZB42[J]. Biomolecules,2019,9(10):613. doi: 10.3390/biom9100613
    [44]
    GOND S K, BERGEN M S, TORRES M S, et al. Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize[J]. Microbiol Res,2015,172:79−87. doi: 10.1016/j.micres.2014.11.004
    [45]
    MOOSA A, FARZAND A, SAHI S T, et al. Transgenic expression of antifungal pathogenesis-related proteins against phytopathogenic fungi-15 years of success[J]. Israel Journal of Plant Sciences,2018,65(1-2):38−54.
    [46]
    COZZOLINO M E, DISTEL J S, GARCÍA P A, et al. Control of postharvest fungal pathogens in pome fruits by lipopeptides from a Bacillus sp. isolate SL-6[J]. Scientia Horticulturae,2020,261:108957. doi: 10.1016/j.scienta.2019.108957
    [47]
    MNIF I, GRAU-CAMPISTANY A, CORONEL-LEON J, et al. Purification and identification of Bacillus subtilis SPB1 lipopeptide biosurfactant exhibiting antifungal activity against Rhizoctonia bataticola and Rhizoctonia solani[J]. Environ Sci Pollut Res Int,2016,23(7):6690−6699. doi: 10.1007/s11356-015-5826-3
    [48]
    JANEK T, RODRIGUES L R, CZYŻNIKOWSKA Ż. Study of metal-lipopeptide complexes and their self-assembly behavior, micelle formation, interaction with bovine serum albumin and biological properties[J]. Journal of Molecular Liquids,2018,268:743−753. doi: 10.1016/j.molliq.2018.07.118
    [49]
    KANG B R, PARK J S, JUNG W J. Antifungal evaluation of fengycin isoforms isolated from Bacillus amyloliquefaciens PPL against Fusarium oxysporum f. sp. lycopersici[J]. Microb Pathog,2020,149:104509. doi: 10.1016/j.micpath.2020.104509
    [50]
    马天祥. 生物合成脂肽的研究进展及展望[J]. 炼油与化工,2020,31(5):7−9. [MA T X. Research progress and prospect of biosynthetic lipopeptide[J]. Refining and Chemical Industry,2020,31(5):7−9.

    MA T X. Research progress and prospect of biosynthetic lipopeptide[J]. Refining and Chemical Industry, 2020, 31(5): 7-9.
    [51]
    王晓琼, 毕秀芳, 谢晓凤, 等. 伊枯草菌素A对草莓腐败菌的抑制效果研究[J]. 天然产物研究与开发,2020,32(11):1889−1895. [WANG X Q, BI X F, XIE X F. et al. Antibacterial effect of Iturin a strawberry spoilage mold[J]. Natural Product Research and Development,2020,32(11):1889−1895.

    WANG X Q, BI X F, XIE X F. et al. Antibacterial effect of Iturin a strawberry spoilage mold[J]. Natural Product Research and Development, 2020, 32(11), 1889-1895.
    [52]
    SAŁEK K, EUSTON S R. Sustainable microbial biosurfactants and bioemulsifiers for commercial exploitation[J]. Process Biochemistry,2019,85:143−155. doi: 10.1016/j.procbio.2019.06.027
    [53]
    ALGBURI A, AL-HASANI H M, ISMAEL T K, et al. Antimicrobial activity of Bacillus subtilis KATMIRA1933 and Bacillus amyloliquefaciens B-1895 against staphylococcus aureus biofilms isolated from wound infection[J]. Probiotics Antimicrob Proteins,2021,13(1):125−134. doi: 10.1007/s12602-020-09673-4
    [54]
    XIONG Y, KONG J, YI S, et al. Surfactin ameliorated the internalization and inhibitory performances of bleomycin family compounds in tumor cells[J]. Mol Pharm,2020,17(6):2125−2134. doi: 10.1021/acs.molpharmaceut.0c00281
    [55]
    CAROLIN C F, KUMAR P S, NGUEAGNI P T. A review on new aspects of lipopeptide biosurfactant: Types, production, properties and its application in the bioremediation process[J]. J Hazard Mater,2021,407:124827. doi: 10.1016/j.jhazmat.2020.124827
    [56]
    HAN Q, WU F, WANG X, et al. The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen-associated molecular pattern-triggered immunity[J]. Environ Microbiol,2015,17(4):1166−1188. doi: 10.1111/1462-2920.12538
    [57]
    LIN F, YANG J, MUHAMMAD U, et al. Bacillomycin D-C16 triggers apoptosis of gastric cancer cells through the PI3K/Akt and FoxO3a signaling pathways[J]. Anticancer Drugs,2019,30(1):46−55. doi: 10.1097/CAD.0000000000000688
    [58]
    LIN F, HUANG Z, CHEN Y, et al. Effect of combined bacillomycin D and chitosan on growth of Rhizopus stolonifer and Botrytis cinerea and cherry tomato preservation[J]. Science of Food and Agriculture,2021,101(1):229−239. doi: 10.1002/jsfa.10635
    [59]
    WU T, CHEN M, ZHOU L, et al. Bacillomycin D effectively controls growth of Malassezia globosa by disrupting the cell membrane[J]. Applied Microbial and Cell Physiology,2020,104(8):3529−3540.
    [60]
    LIU Q, FAN W, ZHAO Y, et al. Probing and engineering the fatty acyl substrate selectivity of starter condensation domains of nonribosomal peptide synthetases in lipopeptide biosynthesis[J]. Journal of Biotechnology,2020,15(2):e1900175. doi: 10.1002/biot.201900175
    [61]
    周伟, 郑维, 陶思美. 芽胞杆菌产生的环脂肽类物质的研究进展[J]. 微生物学杂志,2015,35(4):80−86. [ZHOU W, ZHENG W, TAO S M. Advance incyclic lipopeptide substances from Bacillus subtilis[J]. Journal of Microbiology,2015,35(4):80−86. doi: 10.3969/j.issn.1005-7021.2015.04.014

    ZHOU W, ZHENG W, TAO S M. Advance incyclic lipopeptide substances from Bacillus subtilis[J]. Journal of Microbiology, 2015, 35(4): 80-86. doi: 10.3969/j.issn.1005-7021.2015.04.014
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