Abstract
Due to food borne pathogen, maintaining the viability of fresh fruits and vegetable is a great concern. Several strategies including microbial and plant-based formulations to reduce their infection and maintain quality of the fresh food are in practice. Currently, Bacillus has gained significant traction as a biocontrol agent for regulating diseases affecting a variety of agricultural and horticultural crops. Food-grade citric acid and plant growth–promoting rhizobacteria (PGPR) were used as antimicrobial agent, MIC results showed that PGPR (14.87 mm) and CA (20.25 mm) exhibited notable antimicrobial activity against E. coli. Lettuce treated with PGPR showed reduction in E. coli contamination, E. coli was detected at 3.30, 3.68 in control, and 2.7 log CFU/g in random root injury lettuce inoculated with PGPR KACC 21110 respectively. Random root injury showed a trend toward increasing E. coli internalization. The strains exhibited resistance to multiple antibiotics, including Imipenem, tetracycline, ampicillin, cefotaxime, cefoxitin, and ceftriaxone. Comprehensive data analysis revealed the presence of ten putative bacteriocin or bacteriocin-like gene clusters. The structure of lipopeptide homologs was characterized by using QTOF-MS/MS. The mass ion peaks attributed to surfactin homologs, surfactin A ion at m/z 1008.66, surfactin B, C at m/z 1022.67 and 1036.69. In addition to surfactin, a polyketide oxydifficidin and lipopeptide NO were extracted and detected from the extract of B. velezensis. Both isolates are key biocontrol agents and have significant potential in combating foodborne pathogens and can be utilized to explore novel antibacterial products for preventing pathogens in fresh produce.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be made available on request.
Change history
20 November 2023
19573–3 should not have a comma.
References
Agersø Y, Bjerre K, Brockmann E, Johansen E, Nielsen B, Siezen R, Stuer-Lauridsen B, Wels M, Zeidan AA (2019) Putative antibiotic resistance genes present in extant Bacillus licheniformis and Bacillus paralicheniformis strains are probably intrinsic and part of the ancient resistome. PLoS ONE 14:e0210363. https://doi.org/10.1371/journal.pone.0210363
Alanber MN, Alharbi NS, Khaled JM (2020) Evaluation of multidrug-resistant Bacillus strains causing public health risks in powdered infant milk formulas. J Infect Public Health 13:1462–1468. https://doi.org/10.1016/j.jiph.2019.11.013
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:1–15. https://doi.org/10.1186/1471-2164-9-75
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, Van Wezel GP, Medema MH, Weber T (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35. https://doi.org/10.1093/nar/gkad344
Camilios-Neto D, Bonato P, Wassem R, Tadra-Sfeir MZ, Brusamarello-Santos LC, Valdameri G, Donatti L, Faoro H, Weiss VA, Chubatsu LS (2014) Dual RNA-seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genomics 15:1–13. https://doi.org/10.1186/1471-2164-15-378
Cao Y, Pi H, Chandrangsu P, Li Y, Wang Y, Zhou H, Xiong H, Helmann JD, Cai Y (2018) Antagonism of two plant-growth promoting Bacillus velezensis isolates against Ralstonia solanacearum and Fusarium oxysporum. Sci Rep 8:1–14. https://doi.org/10.1038/s41598-018-22782-z
Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71:158–229. https://doi.org/10.1128/mmbr.00036-06
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
Deng YJ, Chen Z, Ruan CQ, Xiao RF, Lian HP, Liu B, Chen MC, Wang JP (2023) Antifungal activities of Bacillus velezensis FJAT-52631 and its lipopeptides against anthracnose pathogen Colletotrichum acutatum. J Basic Microbiol 63:594–603. https://doi.org/10.1002/jobm.202200489
Durgadevi D, Harish S, Manikandan R, Prabhukarthikeyan S, Alice D, Raguchander T (2021) Proteomic profiling of defense/resistant genes induced during the tripartite interaction of Oryza sativa, Rhizoctonia solani AG1-1A, and Bacillus subtilis against rice sheath blight. Physiol Mol Plant Pathol 115:101669. https://doi.org/10.1016/j.pmpp.2021.101669
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 110:1007–1018. https://doi.org/10.1007/s10482-017-0874-y
Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500. https://doi.org/10.1080/23311932.2015.1127500
György É, Laslo É, Kuzman IH, Dezső András C (2020) The effect of essential oils and their combinations on bacteria from the surface of fresh vegetables. Food Sci Nutr 8:5601–5611. https://doi.org/10.1002/fsn3.1864
Han Y, Li X, Guo Y, Sun W, Zhang Q (2018) Co-production of multiple antimicrobial compounds by Bacillus amyloliquefaciens WY047, a strain with broad-spectrum activity. Trans Tianjin Univ 24:160–171. https://doi.org/10.1007/s12209-017-0097-3
Harish S, Kavino M, Kumar N, Balasubramanian P, Samiyappan R (2009) Induction of defense-related proteins by mixtures of plant growth promoting endophytic bacteria against Banana bunchy top virus. BiolControl 51:16–25. https://doi.org/10.1016/j.biocontrol.2009.06.002
Hol WG, Bezemer TM, Biere A (2013) Getting the ecology into interactions between plants and the plant growth-promoting bacterium Pseudomonas fluorescens. Front Plant Sci 4:81. https://doi.org/10.3389/fpls.2013.00081
Im SM, Yu NH, Joen HW, Kim SO, Park HW, Park AR, Kim J-C (2020) Biological control of tomato bacterial wilt by oxydifficidin and difficidin-producing Bacillus methylotrophicus DR-08. Pestic Biochem Physi 163:130–137. https://doi.org/10.1016/j.pestbp.2019.11.007
Jones RN, Holliday NM, Rhomberg PR (2015) Validation of a commercial dry-form broth microdilution device (Sensititre) for testing tedizolid, a new oxazolidinone. J Clin Microbiol 53:657–659. https://doi.org/10.1128/jcm.02769-14
Kim K, Lee Y, Ha A, Kim J-I, Park AR, Yu NH, Son H, Choi GJ, Park HW, Lee CW (2017a) Chemosensitization of Fusarium graminearum to chemical fungicides using cyclic lipopeptides produced by Bacillus amyloliquefaciens strain JCK-12. Front Plant Sci 8:2010. https://doi.org/10.3389/fpls.2017.02010
Kim SY, Song H, Sang MK, Weon H-Y, Song J (2017b) The complete genome sequence of Bacillus velezensis strain GH1-13 reveals agriculturally beneficial properties and a unique plasmid. J Biotechnol 259:221–227. https://doi.org/10.1016/j.jbiotec.2017.06.1206
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645. https://doi.org/10.1101/gr.092759.109
Li X, Zhang Y, Wei Z, Guan Z, Cai Y, Liao X (2016) Antifungal activity of isolated Bacillus amyloliquefaciens SYBC H47 for the biocontrol of peach gummosis. PLoS ONE 11:e0162125. https://doi.org/10.1371/journal.pone.0162125
Li X, Munir S, Xu Y, Wang Y, He Y (2021) Combined mass spectrometry-guided genome mining and virtual screening for acaricidal activity in secondary metabolites of Bacillus velezensis W1. RSC Adv 11:25441–25449. https://doi.org/10.1039/D1RA01326B
Lin L-Z, Zheng Q-W, Wei T, Zhang Z-Q, Zhao C-F, Zhong H, Xu Q-Y, Lin J-F, Guo L-Q (2020) Isolation and characterization of fengycins produced by Bacillus amyloliquefaciens JFL21 and its broad-spectrum antimicrobial potential against multidrug-resistant foodborne pathogens. Front Microbiol 11:579621. https://doi.org/10.3389/fmicb.2020.579621
Liu K, Newman M, McInroy JA, Hu C-H, Kloepper JW (2017) Selection and assessment of plant growth-promoting rhizobacteria for biological control of multiple plant diseases. Phytopathology 107:928–936. https://doi.org/10.1094/PHYTO-02-17-0051-R
Lobova TI, Yemelyanova E, Andreeva IS, Puchkova LI, Repin VY (2015) Antimicrobial resistance and plasmid profile of bacterial strains isolated from the urbanized Eltsovka-1 River (Russia). Microb Drug Resist 21:477–490. https://doi.org/10.1089/mdr.2014.0203
Moriarty MJ, Semmens K, Bissonnette GK, Jaczynski J (2019) Internalization assessment of E. coli O157: H7 in hydroponically grown lettuce. LWT Food Sci 100:183–188. https://doi.org/10.1016/j.lwt.2018.10.060
Muriuki SW, Neondo JO, Budambula NL (2020) Detection and profiling of antibiotic resistance among culturable bacterial isolates in vended food and soil samples. Int J Microbiol 6572693. https://doi.org/10.1155/2020/6572693
Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny JL, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090. https://doi.org/10.1111/j.1462-2920.2006.01202.x
Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009
Poonguzhali S, Madhaiyan M, Sa T-M (2008) Isolation and identification of phosphate solubilizing bacteria from Chinese cabbage and their effect on growth and phosphorus utilization of plants. J Microbiol Biotechnol 18:773–777
Posada LF, Álvarez J, Romero-Tabarez M, de-Bashan L, Villegas-Escobar V (2018) Enhanced molecular visualization of root colonization and growth promotion by Bacillus subtilis EA-CB0575 in different growth systems. Microbiol Res 217:69–80. https://doi.org/10.1016/j.micres.2018.08.017
Prabhukarthikeyan S, Manikandan R, Durgadevi D, Keerthana U, Harish S, Karthikeyan G, Raguchander T (2017) Bio-suppression of turmeric rhizome rot disease and understanding the molecular basis of tripartite interaction among Curcuma longa, Pythium aphanidermatum and Pseudomonas fluorescens. Biol Control 111:23–31. https://doi.org/10.1016/j.biocontrol.2017.05.003
Prabhukarthikeyan S, Keerthana U, Baite M, Panneerselvam P, Mitra D, Kumar RN, Parameswaran C, Cayalvizhi B, Kumar A, Harish S, Prakash R (2022) Bacillus rhizobacteria: a versatile biostimulant for sustainable agriculture. In: New and future developments in microbial biotechnology and bioengineering, vol 2022. Elsevier, Amsterdam, The Netherlands, pp. 33–44. https://doi.org/10.1016/B978-0-323-85163-3.00009-0
Rungsirivanich P, Inta A, Tragoolpua Y, Thongwai N (2019) Partial rpoB gene sequencing identification and probiotic potential of Floricoccus penangensis ML061–4 isolated from Assam tea (Camellia sinensis var. assamica). Sci Rep 9:16561. https://doi.org/10.1038/s41598-019-52979-9
Shafi J, Tian H, Ji M (2017) Bacillus species as versatile weapons for plant pathogens: a review. Biotechnol Biotechnol Equip 31:446–459. https://doi.org/10.1080/13102818.2017.1286950
Tan S, Yang C, Mei X, Shen S, Raza W, Shen Q, Xu Y (2013) The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl Soil Ecol 64:15–22. https://doi.org/10.1016/j.apsoil.2012.10.011
van Heel AJ, de Jong A, Song C, Viel JH, Kok J, Kuipers OP (2018) BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 46:W278–W281. https://doi.org/10.1093/nar/gky383
Wang Y-J, Deering JA, Kim H-J (2021) Effects of plant age and root damage on internalization of shiga toxin-producing Escherichia coli in leafy vegetables and herbs. Horticulturae 7:68. https://doi.org/10.3390/horticulturae7040068
Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T, Bun C, Conrad N, Dietrich EM, Disz T, Gabbard JL (2017) Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 45:D535–D542. https://doi.org/10.1093/nar/gkw1017
Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Müller R, Wohlleben W (2015) antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237–W243. https://doi.org/10.1093/nar/gkv437
Wilson KE, Flor JE, Schwartz RE, Joshua H, Smith JL, Pelak BA, Liesch JM, Hensens OD (1987) Difficidin and oxydifficidin: novel broad spectrum antibacterial antibiotics produced by bacillus subtilis II. isolation and physico-chemical characterization. J Antibiot 40:1682–1691. https://doi.org/10.7164/antibiotics.40.1682
Wright KM, Crozier L, Marshall J, Merget B, Holmes A, Holden NJ (2017) Differences in internalization and growth of Escherichia coli O157:H7 within the apoplast of edible plants, spinach and lettuce, compared with the model species Nicotiana benthamiana. Microb Biotechnol 10:555–569. https://doi.org/10.1111/1751-7915.12596
Wu L, Wu H, Chen L, Yu X, Borriss R, Gao X (2015) Difficidin and bacilysin from Bacillus amyloliquefaciens FZB42 have antibacterial activity against Xanthomonas oryzae rice pathogens. Sci Rep 5:12975. https://doi.org/10.1038/srep12975
Yuan B, Wang Z, Qin S, Zhao G-H, Feng Y-J, Wei L-H, Jiang J-H (2012) Study of the anti-sapstain fungus activity of Bacillus amyloliquefaciens CGMCC 5569 associated with Ginkgo biloba and identification of its active components. Bioresour Technol 114:536–541. https://doi.org/10.1016/j.biortech.2012.03.062
Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM, Shen Q (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Sci Rep 5:1–8. https://doi.org/10.1038/srep13438
Yuan J, Zhao M, Li R, Huang Q, Rensing C, Raza W, Shen Q (2016) Antibacterial compounds-macrolactin alters the soil bacterial community and abundance of the gene encoding PKS. Front Microbiol 7:1904. https://doi.org/10.3389/fmicb.2016.01904
Ziuzina D, Patil S, Cullen PJ, Keener K, Bourke P (2014) Atmospheric cold plasma inactivation of Escherichia coli, Salmonella enterica serovar Typhimurium and Listeria monocytogenes inoculated on fresh produce. Food Microbiol 42:109–116. https://doi.org/10.1016/j.fm.2014.02.007
Funding
This research work was carried out with the support of the “Research Program for Agriculture Science and Technology Development (Project No. PJ0155852023)” National Institute of Agricultural Science, Rural Development Administration (RDA), Republic of Korea.
Author information
Authors and Affiliations
Contributions
Husna performed the experimental work and wrote the original draft. Bo-eun Kim supervised the study and designed the project. Myeong-hee Won helped with the experiment and methodology. Myeong-In Jeong, Kwang-Kyo Oh, and Dong-Suk Park facilitated the study by providing valuable suggestions and engaging in discussions. All authors have read the manuscript and approved its final form.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent to publication.
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Diane Purchase
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Husna, Kim, BE., Won, MH. et al. Characterization and genomic insight of surfactin-producing Bacillus velezensis and its biocontrol potential against pathogenic contamination in lettuce hydroponics. Environ Sci Pollut Res 30, 121487–121500 (2023). https://doi.org/10.1007/s11356-023-30871-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-30871-4