C17-fengycin B, produced by deep-sea-derived Bacillus subtilis, possessing a strong antifungal activity against Fusarium solani -- Journal of Oceanology and Limnology,2021,39(5):1938-1947

	Cite this paper:
	Weixiang LIU, Chaomin SUN. C₁₇-fengycin B, produced by deep-sea-derived Bacillus subtilis, possessing a strong antifungal activity against Fusarium solani[J]. Journal of Oceanology and Limnology, 2021, 39(5): 1938-1947

C₁₇-fengycin B, produced by deep-sea-derived Bacillus subtilis, possessing a strong antifungal activity against Fusarium solani

Weixiang LIU^1,2, Chaomin SUN^1,2

1 CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Center for Ocean MegaScience, Chinese Academy of Sciences, Qingdao 266071, China;
2 Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China

Abstract:

Root rot disease caused by Fusarium solani is the most devastating disease of the tomato and legume crops in China. The metabolites of Bacillus species can inhibit many fungal diseases. In this study, the metabolites of deep-sea-derived bacterium Bacillus subtilis 2H11 can significantly inhibit the growth of F. solani. The metabolite C₁₇-fengycin B, one of the cyclic lipopeptides, was identified by the combination of silica column chromatography, high-performance liquid chromatography (HPLC), high-energy collision induced dissociation mass spectrometry (HCD-MS) and tandem mass spectrometry (HCD-MS/MS). The results of scanning electron microscopy (SEM) and transmission electron microscopy (TEM) showed that C₁₇-fengycin B could destroy the structure of the hyphae and spores of F. solani. The antifungal activities of C₁₇-fengycin B against F. solani were tested at concentrations ranging from 0.05 mg/mL to 0.20 mg/mL. The results indicated that C₁₇-fengycin B inhibited the growth of F. solani with antifungal index of 89.80% at 0.20 mg/mL, and the antifungal activity of C₁₇-fengycin B was further verified by the pot experiment. In addition, the cytotoxicity experiment showed that C₁₇-fengycin B had good biocompatibility and was a potential candidate for the development of biocontrol pesticide in the future.

Key words: Bacillus species|lipopeptide|fengycin|antifungal|pesticide

Received: 2020-06-02 Revised: 2020-09-22

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References:
Al-Mughrabi K I, Vikram A, Peters R D, Howard R J, Grant L, Barasubiye T, Lynch K, Poirier R, Drake K A, Macdonald I K, Lisowski S L I, Jayasuriya K E. 2013. Efficacy of Pseudomonas syringae in the management of potato tuber diseases in storage. Biological Control, 64(3):315-322.
Azizbekyan R R. 2019. Biological preparations for the protection of agricultural plants (Review). Applied Biochemistry and Microbiology, 55(8):816-823.
Benaouali H, Hamini-Kadar N, Bouras A, Benichou S L, Kihal M, Henni J E. 2014. Isolation, pathogenicity test and physicochemical studies of Fusarium oxysporum f.sp radicis lycopersici. Advances in Environmental Biology, 8(10):36-49.
Blunt J W, Carroll A R, Copp B R, Davis R A, Keyzers R A, Prinsep M R. 2018. Marine natural products. Natural Product Reports, 35(1):8-53.
Bonilla-Landa I, de la Cruz O L, Sanchéz-Rangel D, OrtízCastro R, Rodriguez-Haas B, Barrera-Méndez F, de León Gómez R E D, Javier Enríquez-Medrano F, Luis OlivaresRomero J. 2018. Design, synthesis and biological evaluation of novel fungicides for the management of Fusarium DieBack disease. Journal of the Mexican Chemical Society, 62(3):86-98.
Carroll A R, Copp B R, Davis R A, Keyzers R A, Prinsep M R. 2020. Marine natural products. Natural Product Reports, 37(2):175-223.
Chang X L, Dai H, Wang D P, Zhou H H, He W Q, Fu Y, Ibrahim F, Zhou Y, Gong G S, Shang J, Yang J Z, Wu X L, Yong T W, Song C, Yang W Y. 2018. Identification of Fusarium species associated with soybean root rot in Sichuan Province, China. European Journal of Plant Pathology, 151(3):563-577.
Chen L L, Wang N, Wang X M, Hu J C, Wang S J. 2010. Characterization of two anti-fungal lipopeptides produced by Bacillus amyloliquefaciens SH-B10. Bioresource Technology, 101(22):8 822-8 827.
Chittem K, Mathew F M, Gregoire M, Lamppa R S, Chang Y W, Markell S G, Bradley C A, Barasubiye T, Goswami R S. 2015. Identification and characterization of Fusarium spp. associated with root rots of field pea in North Dakota. European Journal of Plant Pathology, 143(4):641-649.
Coetzee M P A, Wingfield B D, Wingfield M J. 2018. Armillaria root-rot pathogens:species boundaries and global distribution. Pathogens, 7(4):83, https://doi.org/10.3390/pathogens7040083.
Cui J Q, Wang Y, Han J, Cai B Y. 2016. Analyses of the community compositions of root rot pathogenic fungi in the soybean rhizosphere soil. Chilean Journal of Agricultural Research, 76(2):179-187.
da Rosa P D, Ramirez-Castrillon M, Borges R, Aquino V, Fuentefria A M, Goldani L Z. 2019. Epidemiological aspects and characterization of the resistance profile of Fusarium spp. in patients with invasive fusariosis. Journal of Medical Microbiology, 68(10):1 489-1 496.
D'Agostino M, Lemmet T, Dufay C, Luc A, Frippiat J P, Machouart M, Debourgogne A. 2018. Overinduction of CYP51A gene after exposure to azole antifungals provides a first clue to resistance mechanism in Fusarium solani species complex. Microbial Drug Resistance, 24(6):768-773.
de Rodríguez D J, Hernández-Castillo D, Rodríguez-García R, Angulo-Sánchez J L. 2005. Antifungal activity in vitro of Aloe vera pulp and liquid fraction against plant pathogenic fungi. Industrial Crops and Products, 21(1):81-87.
Egamberdieva D, Wirth S J, Shurigin V V, Hashem A, Abd Allah E F. 2017. Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Frontiers in Microbiology, 8:1 887, https://doi.org/10.3389/fmicb.2017.01887.
Hu W C, Wang G C, Li P X, Wang Y N, Si C L, He J, Long W, Bai Y J, Feng Z S, Wang X F. 2014. Neuroprotective effects of macranthoin G from Eucommia ulmoides against hydrogen peroxide-induced apoptosis in PC12 cells via inhibiting NF-κB activation. Chemico-Biological Interactions, 224:108-116.
Kobayashi J I. 2016. Search for new bioactive marine natural products and application to drug development. Chemical & Pharmaceutical Bulletin, 64(8):1 079-1 083.
Kordali S, Cakir A, Ozer H, Cakmakci R, Kesdek M, Mete E. 2008. Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and pcymene. Bioresource Technology, 99(18):8 788-8 795.
Lewis K A, Tzilivakis J, Warner D J, Green A. 2016. An international database for pesticide risk assessments and management. Human and Ecological Risk Assessment:an International Journal, 22(4):1 050-1 064.
Li D H, Carr G, Zhang Y H, Williams D E, Amlani A, Bottriell H, Mui A L F, Andersen R J. 2011. Turnagainolides A and B, cyclic depsipeptides produced in culture by a Bacillus sp.:Isolation, structure elucidation, and synthesis. Journal of Natural Products, 74(5):1 093-1 099.
Ma Z W, Hu J C, Wang X M, Wang S J. 2014. NMR spectroscopic and MS/MS spectrometric characterization of a new lipopeptide antibiotic bacillopeptin B1 produced by a marine sediment-derived Bacillus amyloliquefaciens SH-B74. The Journal of Antibiotics, 67(2):175-178.
Matheron M E, Porchas M. 2000. Impact of azoxystrobin, dimethomorph, fluazinam, fosetyl-Al, and metalaxyl on growth, sporulation, and zoospore cyst germination of three Phytophthora spp. Plant Disease, 84(4):454-458.
Nam J, Jung M Y, Kim P I, Lee H B, Kim S W, Lee C W. 2015. Structural characterization and temperature-dependent production of C₁₇-fengycin B derived from Bacillus amyloliquefacienssubsp. plantarum BC32-1.Biotechnology and Bioprocess Engineering, 20(4):708-713.
Nile A S, Kwon Y D, Nile S H. 2019. Horticultural oils:possible alternatives to chemical pesticides and insecticides. Environmental Science and Pollution Research, 26(21):21 127-21 139.
Patzke H, Zimdars S, Schulze-Kaysers N, Schieber A. 2017. Growth suppression of Fusarium culmorum, Fusarium poae and Fusarium graminearum by 5-n-alk(en) ylresorcinols from wheat and rye bran. Food Research International, 99:821-827.
Pecci Y, Rivardo F, Martinotti M G, Allegrone G. 2010. LC/ESI-MS/MS characterisation of lipopeptide biosurfactants produced by the Bacillus licheniformis V9T14 strain. Journal of Mass Spectrometry, 45(7):772-778.
Ramachandran R, Shrivastava M, Narayanan N N, Thakur R L, Chakrabarti A, Roy U. 2017. Evaluation of antifungal efficacy of three new cyclic lipopeptides of the class bacillomycin from Bacillus subtilis RLID 12.1. Antimicrobial Agents and Chemotherapy, 62(1):e01457-17, https://doi.org/10.1128/AAC.01457-17.
Ramos L S, Prohaska P G. 1981. Sephadex LH-20 chromatography of extracts of marine sediment and biological samples for the isolation of polynuclear aromatic hydrocarbons. Journal of Chromatography A, 211(2):284-289.
Rofeal M, El-Malek A F. 2020. Valorization of lipopeptides biosurfactants as anticancer agents. International Journal of Peptide Research and Therapeutics, https://doi.org/10.1007/s10989-020-10105-8.
Sav H, Rafati H, Oz Y, Dalyan-Cilo B, Ener B, Mohammadi F, Ilkit M, van Diepeningen A D, Seyedmousavi S. 2018. Biofilm formation and resistance to fungicides in clinically relevant members of the fungal genus Fusarium. Journal of Fungi (Basel, Switzerland), 4(1):16, https://doi.org/10.3390/jof4010016.
Schroers H J, Samuels G J, Zhang N, Short D P G, Juba J, Geiser D M. 2016. Epitypification of Fusisporium(Fusarium) solani and its assignment to a common phylogenetic species in the Fusarium solani species complex. Mycologia, 108(4):806-819.
Schut F, De vries E J, Gottschal J C, Robertson B R, Harder W, Prins R A, Button D K. 1993. Isolation of typical marine bacteria by dilution culture:growth, maintenance, and characteristics of isolates under laboratory conditions.
Applied and Environmental Microbiology, 59(7):2 150-2 160. Shafi J, Tian H, Ji M S. 2017. Bacillus species as versatile weapons for plant pathogens:a review. Biotechnology & Biotechnological Equipment, 31(3):446-459.
Shugart L. 2017. Special Issue:emerging advances and challenges in pesticide ecotoxicology. Ecotoxicology, 26(3):293-294.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6:molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12):2 725-2 729.
Thiericke R, Rohr J. 1993. Biological variation of microbial metabolites by precursor-directed biosynthesis. Natural Product Reports, 10(3):265-289.
Von Schrenk H, Spaulding P. 1902. The bitter rot disease of apples. Science, 16(408):669-670.
Wiggell P, Simpson C J. 1969. Observations on the control of phomopsis root rot of cucumber. Plant Pathology, 18(2):71-77, https://doi.org/10.1111/j.1365-3059.1969.tb00469.x.
Xing X Y, Zhao X Y, Ding J, Liu D M, Qi G F. 2018. Entericcoated insulin microparticles delivered by lipopeptides of iturin and surfactin. Drug Delivery, 25(1):23-34.
Yin H P, Guo C L, Wang Y, Liu D, Lv Y B, Lv F X, Lu Z X. 2013. Fengycin inhibits the growth of the human lung cancer cell line 95D through reactive oxygen species production and mitochondria-dependent apoptosis. AntiCancer Drugs, 24(6):587-598.
Zeigler D R, Nicholson W L. 2017. Experimental evolution of Bacillus subtilis. Environmental Microbiology, 19(9):3 415-3 422.
Zhang L, Sun C. 2018. Fengycins, cyclic lipopeptides from marine Bacillus subtilis strains, kill the plant-pathogenic fungus Magnaporthe grisea by inducing reactive oxygen species production and chromatin condensation. Applied and Environmental Microbiology, 84(18):e00445-18, https://doi.org/10.1128/aem.00445-18.