Killing Effect of Bacillus Velezensis FZB42 on a Xanthomonas Campestris pv. Campestris (Xcc) Strain Newly Isolated from Cabbage Brassica Oleracea Convar. Capitata (L.): A Metabolomic Study
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
19-10907S
the Czech Science Foundation
No. CA16107
EU COST
IGA_PrF_2021_021
the internal grant agency of Palacký University
RVO 61388971
Institute of Microbiology of the CAS
PubMed
34210064
PubMed Central
PMC8303752
DOI
10.3390/microorganisms9071410
PII: microorganisms9071410
Knihovny.cz E-zdroje
- Klíčová slova
- Bacillus velezensis FZB42, Xanthomonas campestris pv. campestris, antagonism, cyclic lipopeptides, killing effect, metabolomic analysis, siderophore,
- Publikační typ
- časopisecké články MeSH
The potential use of Bacillus velezensis FZB42 for biological control of various phytopathogens has been documented over the past few years, but its antagonistic interactions with xanthomonads has not been studied in detail. Novel aspects in this study consist of close observation of the death of Xanthomonas campestris pv. campestris cells in a co-culture with B. velezensis FZB42, and quantification of lipopeptides and a siderophore, bacillibactin, involved in the killing process. A new robust Xcc-SU isolate tolerating high concentrations of ferric ions was used. In a co-culture with the antagonist, the population of Xcc-SU was entirely destroyed within 24-48 h, depending on the number of antagonist cells used for inoculation. No inhibitory effect of Xcc-SU on B. velezensis was observed. Bacillibactin and lipopeptides (surfactin, fengycin, and bacillomycin) were present in the co-culture and the monoculture of B. velezensis. Except for bacillibactin, the maximum contents of lipopeptides were higher in the antagonist monoculture compared with the co-culture. Scanning electron microscopy showed that the death of Xcc-SU bacteria in co-culture was caused by cell lysis, leading to an enhanced occurrence of distorted cells and cell ghosts. Analysis by mass spectrometry showed four significant compounds, bacillibactin, surfactin, fengycin, and bacillomycin D amongst a total of 24 different forms detected in the co-culture supernatant: Different forms of surfactin and fengycin with variations in their side-chain length were also detected. These results demonstrate the ability of B. velezensis FZB42 to act as a potent antagonistic strain against Xcc.
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Marin V.R., Ferrarez J.H., Vieira G., Sass D.C. Recent advances in the biocontrol of Xanthomonas spp. World J. Microbiol. Biotechnol. 2019;35:72. doi: 10.1007/s11274-019-2646-5. PubMed DOI
Liu K., Garret C., Fadamiro H., Kloepper J.W. Antagonism of black rot in cabbage by mixture of plant growth-promoting rhizobacteria (PGPR) BioControl. 2016;61:605–613. doi: 10.1007/s10526-016-9742-3. DOI
Bhattacharyya P.N., Goswami M.P., Bhattacharyya L.H. Perspective of beneficial microbes in agriculture under changing climatic scenario: A review. J. Phytol. 2016;8:26–41. doi: 10.19071/jp.2016.v8.3022. DOI
Fan B., Wang C., Song X., Ding X., Wu L., Wu H., Gao X., Borriss R. Bacillus velezensis FZB42 in 2018: The Gram-Positive Model Strain for Plant Growth Promotion and Biocontrol. Front. Microbiol. 2018;9:2491. doi: 10.3389/fmicb.2018.02491. PubMed DOI PMC
Monteiro L., Mariano R.L.R., Souto-Maior A.M. Antagonism of Bacillus spp. against Xanthomonas campestris pv. campestris. Brazil. Arch. Biol. Technol. 2005;48:23–29. doi: 10.1590/S1516-89132005000100004. DOI
Daungfu O., Youpensuk S., Lumyong S. Endophytic bacteria isolated from Citrus plants for biological control of citrus canker in lime plants. Trop. Life Sci. Res. 2019;30:73–88. doi: 10.21315/tlsr2019.30.1.5. PubMed DOI PMC
Li S.B., Fang M., Zhou R.C., Huang J. Characterization and evaluation of the endophyte Bacillus B014 as a potential biocontrol agent for the control of Xanthomonas axonopodis pv. dieffenbachiae—Induced blight of Anthurium. Biol. Control. 2012;63:9–16. doi: 10.1016/j.biocontrol.2012.06.002. DOI
Wulff E.G., Mguni C.M., Mansfeld-Giese K., Fels J., Lübeck M., Hockenhull J. Biochemical and molecular characterization of Bacillus amyloliquefaciens, B. subtilis and B. pumilus isolates with distinct antagonistic potential against Xanthomonas campestris pv. campestris. Plant. Pathol. 2002;51:574–584. doi: 10.1046/j.1365-3059.2002.00753.x. DOI
Issazadeh K., Rad S.K., Zarrabi S., Rahimibashar M.R. Antagonism of Bacillus species against Xanthomonas campestris pv. campestris and Pectobacterium carotovorum pv. carotovorum. Afr. J. Microbiol. Res. 2012;6:1615–1620. doi: 10.5897/AJMR12.075. DOI
Koumoutsi A., Chen X.H., Henne A., Liesegang H., Hitzeroth G., Franke P., Vater J., Borriss R. Structural and functional characterization of gene clusters directing nonribosomal synthesis of biactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J. Bacteriol. 2004;186:1084–1096. doi: 10.1128/JB.186.4.1084-1096.2004. PubMed DOI PMC
Chen X.H., Vater J., Piel J., Franke P., Scholz R., Schneider K., Koumoutsi A., Hitzeroth G., Grammel N., Strittmatter A.W., et al. Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB42. J. Bacteriol. 2006;188:4024–4036. doi: 10.1128/JB.00052-06. PubMed DOI PMC
Li B., Li Q., Xu Z., Zhang N., Shen Q., Zhang R. Responses of beneficial Bacillus amyloliquefaciens SQR9 to different soilborne fungal pathogens through the alteration of antifungal compounds production. Front. Microbiol. 2014;5:636. doi: 10.3389/fmicb.2014.00636. PubMed DOI PMC
Cawoy H., Debois D., Franzil L., De Pauw E., Thonart P., Ongena M. Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/amyloliquefaciens. Microb. Biotechnol. 2015;8:281–295. doi: 10.1111/1751-7915.12238. PubMed DOI PMC
Chowdhury S.P., Hartmann A., Gao X.W., Borriss R. Biocontrol mechanisms by root-associated Bacillus amyloliquefaciens FZB42—A review. Front. Microbiol. 2015;6:780. doi: 10.3389/fmicb.2015.00780. PubMed DOI PMC
Chen X.H., Scholz R., Borriss M., Junge H., Mögel G., Kunz S., Borriss R. Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J. Biotechnol. 2009;140:38–44. doi: 10.1016/j.jbiotec.2008.10.015. PubMed DOI
Bernheimer A.W., Avigad L.S. Nature and properties of a cytolytic agent produced by Bacillus subtilis. J. Gen. Microbiol. 1970;6:361–366. doi: 10.1099/00221287-61-3-361. PubMed DOI
Bais H.P., Fall R., Vivanco J.M. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant. Physiol. 2004;134:307–319. doi: 10.1104/pp.103.028712. PubMed DOI PMC
Preecha C., Sadowsy M.J., Prathuangwong S. Lipopeptide surfactin produced by Bacillus amyloliquefaciens KPS46 is required for biocontrol efficacy against Xanthomonas axonopodis pv. glycines. Kasetart J. 2010;44:84–99.
Meena K.R., Sharma A., Kanwar S. Antitumoral and antimicrobial activity of surfactin extracted from Bacillus subtilis KLP2015. Int. J. Peptide Res. Therapeut. 2020;26:423–433. doi: 10.1007/s10989-019-09848-w. DOI
Horng Y.-B., Yu Y.-H., Dybus A., Hsiao F.S.-H., Cheng Y.-H. Antibacterial activity of Bacillus species-derived surfactin on Brachyspira hyodysenteriae and Clostridium perfringens. AMB Expr. 2019;9:188. doi: 10.1186/s13568-019-0914-2. PubMed DOI PMC
Torres M.J., Petroselli G., Daz M., Erra-Balsells R., Audisio M.C. Bacillus subtilis subsp. subtilis CBMDC3f with antimicrobial aktivity against Gram-positive foodborne pathogenic bacteria: UV-MALDI-TOF MS analysis of its bioactive compounds. World J. Microbiol. Biotechnol. 2015;31:929–940. doi: 10.1007/s11274-015-1847-9. PubMed DOI
Hanif A., Zhang F., Li P., Li C., Xu Y., Zubair M., Zhang M., Jia D., Zhao X., Liang J., et al. Fengycin produced by Bacillus amyloliquefaciens FZB42 inhibits Fusarium graminearum growth and mycotoxins biosynthesis. Toxins. 2019;11:295. doi: 10.3390/toxins11050295. PubMed DOI PMC
Hu L.B., Shi Z.Q., Zhang T., Yang Z.M. Fengycin antibiotics isolated from B-FS01 culture inhibit the growth of Fusarium moniliforme Sheldon ATCC 38932. FEMS Microbiol. Lett. 2007;272:91–98. doi: 10.1111/j.1574-6968.2007.00743.x. PubMed DOI
Desmyttere H., Deweer C., Muchembled J., Sahmer K., Jacquin J., Coutte F., Jacques P. Antifungal activities of Bacillus subtilis lipopeptides to two Venturia inaequalis strains possessing different tebuconazole sensitivity. Front. Microbiol. 2019;10:2327. doi: 10.3389/fmicb.2019.02327. PubMed DOI PMC
Romero D., de Vicente A., Rakotoaly R.H., Dufour S.E., Veening J.W., Arrebola E., Cazorla F., Kuipers O.P., Paquot M., Perez-Garcia A. The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol. Plant Microbe Interact. 2007;10:183–188. doi: 10.1094/MPMI-20-4-0430. PubMed DOI
Li Y., Heloir M.C., Zhang X., Geissler M., Trouvelot S., Jacquens L., Henkel M., Su X., Fang X., Wang Q., et al. Surfactin and fengycin contribute to the protection of a Bacillus subtilis strain against grape downy mildew by both direct effect and defence stimulation. Mol. Plant. Pathol. 2019;20:1037–1050. doi: 10.1111/mpp.12809. PubMed DOI PMC
Medeot D.B., Fernandez M., Morales G.M., Jofre E. Fengycins from Bacillus amyloliquefaciens MEP218 exhibit antibacterial activity by producing alterations on the cell surface of the pathogens Xanthomonas axonopodis pv. vesicatoria and Pseudomonas aeruginosa PA01. Front. Microbiol. 2020;10:3107. doi: 10.3389/fmicb.2019.03107. PubMed DOI PMC
Moyne A.L., Shelby R., Cleveland T.E., Tuzun S. Bacillomycin D: An iturin with antifungal activity against Aspergillus flavus. J. Appl. Microbiol. 2001;90:622–629. doi: 10.1046/j.1365-2672.2001.01290.x. PubMed DOI
Gong Q., Zhang C., Lu F., Zhao H., Bie X., Lu Z. Identification of bacillomycin D from Bacillus subtilis fmbj and its inhibition effects against Aspergillus flavus. Food. Control. 2014;36:8–14. doi: 10.1016/j.foodcont.2013.07.034. DOI
Jin P., Wang H., Tan Z., Xuan Z., Dahar G.Y., Li Q.X., Miao W., Liu W. Antifungal mechanism of bacillomycin D from Bacillus velezensis HN-2 against Colletotrichum gloeosporioides Penz. Pesticide Biochem. Physiol. 2019;163:102–107. doi: 10.1016/j.pestbp.2019.11.004. PubMed DOI
Tabbene O., Di Grazia A., Azaiez S., Ben Slimene I., Elkahoui S., Alfeddy M.N., Casciaro B., Luca V., Limam F., Mangoni M.L. Synergistic fungicidal aktivit of the lipopeptide bacillomycin D with amphotericin B against pathogenic Candida species. FEMS Yest Res. 2015;15:fov022. doi: 10.1093/femsyr/fov022. PubMed DOI
Rajaofera M.J.N., Kang X., Jin P.-F., Chen X., Li C.-C., Yin L., Liu L., Sun Q.H., Zhang N., Chen C.Z., et al. Antibacterial activity of bacillomycin D-like compounds isolated from Bacillus amyloliquefaciens HAB-2 against Burkholderia pseudomallei. Asian Pac. J. Trop. Biomed. 2020;10:183–188.
Alvarez A.M. Black rot of crucifers. In: Slusarenko A.J., Fraser R.S.S., London L.C., editors. Mechanisms of Resistances to Plant Diseases. Kluwer Academic Publishers; Dordrecht, The Netherlands: 2000. pp. 21–52.
Pandey S.S., Patnana P.K., Rai R., Chatterjee S. Xanthoferrin, the α-hydroxycarboxylate-type siderophore of Xanthomonas campestris pv. campestris, is required for optimum virulence and growth inside cabbage. Mol. Plant. Pathol. 2017;18:949–962. doi: 10.1111/mpp.12451. PubMed DOI PMC
Rastogi G., Sbodio A., Tech J.J., Suslow T.V., Coaker G.L., Leveau J.H. Leaf microbiota in an agroecosystem: Spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 2012;6:1812–1822. doi: 10.1038/ismej.2012.32. PubMed DOI PMC
Deng Y., Wu J., Yin W., Li P., Zhou J., Chen S., He F., Cai J., Zhang L.H. Diffusible signal factor family signals provide a fitness advantage to Xanthomonas campestris pv. campestris in interspecies competition. Environ. Microbiol. 2016;18:1534–1545. doi: 10.1111/1462-2920.13244. PubMed DOI
Hert A.P., Marutani M., Momol M.T., Roberts P.D., Jones J.B. Analysis of pathogenicity mutants of a bacteriocin producing Xanthomonas perforans. Biol. Control. 2009;51:362–369. doi: 10.1016/j.biocontrol.2009.07.007. DOI
Royer M., Costet L., Vivien E., Bes M., Cousin A., Damais A., Pieretti I., Savin A., Megessier S., Viard M., et al. Albicidin pathotoxin produced by Xanthomonas albilineans is encoded by three large PKS and NRPS genes present in a gene cluster also containing several putative modifying, regulatory, and resistance genes. Mol. Plant-Microbe Interact. 2004;17:414–427. doi: 10.1094/MPMI.2004.17.4.414. PubMed DOI
Reva O.N., Swanevelder D.Z.H., Mwita L.A., Mwakilili A.D., Muzondiwa D., Joubert M., Chan W.Y., Lutz S., Ahrens C.H., Avdeeva L.V., et al. Genetic, epigenetic and phenotypic diversity of four Bacillus velezensis strains used for plant protection or as probiotics. Front. Microbiol. 2019;10:2610. doi: 10.3389/fmicb.2019.02610. PubMed DOI PMC
Novák J., Sokolová L., Lemr K., Pluháček T., Palyzová A., Havlíček V. Batch-processing of imaging or liquid-chromatography massspectrometry datasets and de novo sequencing of polyketide siderophores. Biochim. Biophys. Acta. 2017;1865:768–775. doi: 10.1016/j.bbapap.2016.12.003. PubMed DOI
Palyzová A., Svobodová K., Sokolová L., Novák J., Novotný Č. Metabolic profiling of Fusarium oxysporum f. sp. conglutinans race 2 in dual cultures with biocontrol agents Bacillus amyloliquefaciens, Pseudomonas aeruginosa, and Trichoderma harzianum. Folia Microbiol. 2019;64:779–787. doi: 10.1007/s12223-019-00690-7. PubMed DOI
Pi H., Helmann J.D. Sequential induction of Fur-regulated genes in response to iron limitation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA. 2017;114:12785–12790. doi: 10.1073/pnas.1713008114. PubMed DOI PMC
Rodriguez H., Aguilar L., LaO M. Variations in xanthan production by antibiotic resistant mutants of Xanthomonas campestris. Appl. Microbiol. Biotechnol. 1997;48:626–629. doi: 10.1007/s002530051106. DOI
Rojas M., Pena M., Pena-Vera M.J., Sulbaran M., Perez E., Velasquez C.L. Characterization and determination of antimicrobial and metal resistant profiles of Xanthomonas strains isolated from natural environments. J. Anal Pharm. Res. 2019;8:55–60. doi: 10.15406/japlr.2019.08.00312. DOI
Marquett M., Mikolajezak M., Throne L., Pollock T.J. Improved strains for production of xanthan gum by fermentation of Xanthomonas campestris. J. Ind. Microbiol. 1989;4:53–64.
R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2021. [(accessed on 18 May 2021)]. Available online: https://www.R-project.org/
Mihalache G., Balaes T., Gostin I., Stefan M., Coutte F., Krier F. Lipopetides produced by Bacillus subtilis as new biocontrol products against fusariosis in ornamental plants. Environ. Sci. Pollut. Res. 2017;25:29784–29793. doi: 10.1007/s11356-017-9162-7. PubMed DOI
Borriss R. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. In: De Bruijn F.J., editor. Molecular Microbial Ecology of the Rhizosphere. Wiley Blackwell Hoboken; Hoboken, NJ, USA: 2013. p. 98.
Dertz E.A., Stintzi A., Raymond K.N. Siderophore-mediated iron transport in Bacillus subtilis and Corynebacterium glutamicum. J. Biol. Inorg. Chem. 2006;11:1087–1097. doi: 10.1007/s00775-006-0151-4. PubMed DOI
Khare A., Tavazoie S. Multifactorial competition and resistance in a two-species bacterial system. PLoS Genet. 2015;11:e1005715. doi: 10.1371/journal.pgen.1005715. PubMed DOI PMC
Chen Y., Liu S.A., Mou H., Ma Y., Li M., Hu X. Characterization of Lipopeptide Biosurfactants Produced by Bacillus licheniformis MB01 from Marine Sediments. Front. Microbiol. 2017;8:871. doi: 10.3389/fmicb.2017.00871. PubMed DOI PMC
Ramachandran R., Shrivastava M., Narayanan N.N., Thakur R.L., Chakrabarti A., Roy U. Evaluation of Antifungal Efficacy of Three New Cyclic Lipopeptides of the Class Bacillomycin from Bacillus subtilis RLID 12.1. Antimicrob. Agents Chemother. 2018;62:e01457-17. doi: 10.1128/AAC.01457-17. PubMed DOI PMC
Pretorius D., van Rooyen J., Clarke K.G. Enhanced production of antifungal lipopeptides by Bacillus amyloliquefaciens for biocontrol of postharvest disease. New Biotechnol. 2015;32:243–252. doi: 10.1016/j.nbt.2014.12.003. PubMed DOI
Kirk S., Avignone-Rosa C.A., Bushell M.E. Growth limiting substrate affects antibiotic production and associated metabolic fluxes in Streptomyces clavuligerus. Biotechnol. Lett. 2000;22:1803–1809. doi: 10.1023/A:1005670603596. DOI
Zhi Y., Wu Q., Xu Y. Genome and transcriptome analysis of surfactin biosynthesis in Bacillus amyloliquefaciens MT45. Sci. Rep. 2017;7:40976. doi: 10.1038/srep40976. PubMed DOI PMC
Sen R. Response surface optimization of the critical media components for the production of surfactin. J. Chem. Technol. Biotechnol. 1997;68:263–270. doi: 10.1002/(SICI)1097-4660(199703)68:3<263::AID-JCTB631>3.0.CO;2-8. DOI
Wei Y.H., Chu I.M. Enhancement of surfactin production in iron-entiched media by Bacillus subtilis ATCC21332. Enzyme Microb Technol. 1998;22:724–728. doi: 10.1016/S0141-0229(98)00016-7. DOI
Manickam N., Misra R., Mayilraj S. A novel pathway for the biodegradation of γ-hexachlorocyclohexane by a Xanthomonas sp. strain ICH12. J. Appl. Microbiol. 2007;102:1468–1478. doi: 10.1111/j.1365-2672.2006.03209.x. PubMed DOI
Rayu S., Nielsen U.N., Nazaries L., Singh B.K. Isolation and molecular characterization of novel chlorpyrifos and 3,5,6-trichloro-2-pyridinol-degrading bacteria from sugarcane farm soils. Front Microbiol. 2017;8:518. doi: 10.3389/fmicb.2017.00518. PubMed DOI PMC
Szulc A., Ambrożewicz D., Sydow M., Ławniczak Ł., Piotrowska-Cyplik A., Marecik R., Chrzanowski Ł. The influence of bioaugmentation and biosurfactant addition on bioremediation efficiency of diesel-oil contaminated soil: Feasibility during field studies. J. Environ. Manag. 2014;132:121–128. doi: 10.1016/j.jenvman.2013.11.006. PubMed DOI
Dow M.D., Clarke B.R., Milligan D.E., Tang J.-L., Daniels M.J. Extracellular proteases from Xanthomonas campestris pv. campestris, the black rot pathogen. Appl. Environ. Microbiol. 1990;56:2994–2998. doi: 10.1128/aem.56.10.2994-2998.1990. PubMed DOI PMC
Ayed H.N., Hmidet N., Bechet M., Chollet M., Chataigne G., Leclere V., Jacques P., Nasri M. Identification and biochemical characteristics of lipopeptides from Bacillus mojavensis A21. Process Biochem. 2014;49:1699–1707. doi: 10.1016/j.procbio.2014.07.001. DOI
Gu Q., Yang Y., Yuan Q., Shi G., Wu L., Lou Z., Huo R., Wu H., Borriss R., Gao X. Bacillomycin D produced by Bacillus amyloliquefaciens is involved in the antagonistic interaction with the plant-pathogenic fungus Fusarium graminearum. Appl. Environ. Microbiol. 2017;83:e01075-17. doi: 10.1128/AEM.01075-17. PubMed DOI PMC
Shafi J., Tian H., Mingshan J. Bacillus species as versatile weapons for plant pathogens: A review. Biotechnol. Biotechnol. Equip. 2017;31:446–459. doi: 10.1080/13102818.2017.1286950. DOI
Maget-Dana R., Ptak M., Peypoux F., Michel G. Pore-forming properties of iturin A, a lipopeptide antibiotic. Biochim. Biophys. Acta. 1985;815:405–409. doi: 10.1016/0005-2736(85)90367-0. PubMed DOI
Li X., Zhang Y., Wei Z., Guan Z., Cai Y., Liao X. Antifungal activity of isolated Bacillus amyloliquefaciens BC H47 for the biocontrol of peach gummosis. PLoS ONE. 2016;11:e0162125. doi: 10.1371/journal.pone.0162125. PubMed DOI PMC