ORIGINAL ARTICLE
Antifungal activity of Bacillus spp. against Fusarium oxysporum f. sp. lycopersici and Ascochyta sp.
| 1 | Department of Biology, University of Oran 1 Ahmed Ben Bella, Oran, Algeria |
| 2 | Department of Biotechnology, University of Science and Technology of Oran Mohamed Boudiaf, Oran, Algeria |
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
CORRESPONDING AUTHOR
Submission date: 2022-02-04
Acceptance date: 2022-04-19
Online publication date: 2022-08-11
Journal of Plant Protection Research 2022;62(3):247–257
HIGHLIGHTS
- Five strains of Bacillus spp. isolated from soil have the ability to inhibit two different phytopathogens Fusarium oxysporum f. sp. lycopersici and Ascochyta sp.
- Four of the five strains belong to the species B. halotolerans and one to the species B. cereus
- The cell-free filtrates and the volatiles compound produced by these strains slowed down the growth of the phytopathogens
KEYWORDS
TOPICS
ABSTRACT
The aim of this study is to find bacterial strains with antagonistic effects against Fusarium
oxysporum f. sp. lycopersici (Fol) and Ascochyta sp, which are phytopathogens responsible
for fusarium wilt of tomato and ascochyta blight of peas, respectively. One hundred thirty-
six bacteria isolated from the rhizosphere of tomatoes were screened. Five strains with
the largest inhibition zones were selected. These strains were identified by the phenotypic
method, later confirmed by sequencing of 16S rDNA. All strains belonged to the genus
Bacillus spp. Their inhibition capacity was evaluated by the direct method by doing a dual
culture, the inhibition rates ranged from 44.32 ± 0.8 to 61.36 ± 0.2 against Fol and 62.04 ± 0.8
to 74.1 ± 0.2% against Ascochyta sp. They were then evaluated by the indirect method by
evaluating, on one hand, the antifungal effect of the volatile compounds produced by the
strains and on the other hand, the antifungal effect of the filtrates. The results showed that
volatile compounds inhibited plant pathogens’ growth with average inhibition rates of
55% against Fol and 17% against Ascochyta. For filtrates, the average inhibition rates were
33.01% against Fol and 33.74% against Ascochyta sp. Finally, the plant growth promoting
rhizobacteria (PGPR) effect of B. halotolerans RFP57 was evaluated. This involved assessing
their ability to stimulate the germination of tomato seeds and the growth of their vegetative
organs. The results showed significant improvement in treated seedlings compared to
controls. All these results show that the strains selected for this study have the potential for
use as a biocontrol agent. However, it is clear that further in-depth studies are needed to
confirm their true potentiality.
RESPONSIBLE EDITOR
Sebastian Stenglein
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (53)
1.
Abdul-Baki A.A., Anderson J.D. 1973. Vigor determination in soybean seed by multiple criteria 1. Crop Science 13 (6): 630–633. DOI: https://doi.org/10.2135/cropsc....
2.
Almeida F., Rodrigues M.L., Coelho C. 2019. The still underestimated problem of fungal diseases worldwide. Frontiers in Microbiology 10: 214. DOI: https://doi.org/10.3389/fmicb.....
3.
Bhattacharjee R., Dey U. 2014. An overview of fungal and bacterial biopesticides to control plant pathogens/diseases. African Journal of Microbiology Research 8 (17): 1749–1762. DOI: https://doi.org/10.5897/AJMR20....
4.
Caulier S., Gillis A., Colau G., Licciardi F., Liépin M., Desoignies N., Modrie P., Legrève A., Mahillon J., Bragard C. 2018. Versatile antagonistic activities of soil-borne Bacillus spp. and Pseudomonas spp. against Phytophthora infestans and other potato pathogens. Frontiers in Microbiology 9: 143. DOI: https://doi.org/10.3389/fmicb.....
5.
Cossus L., Roux-Dalvai F., Kelly I., Nguyen T.T.A., Antoun H., Droit A., Tweddell R.J. 2021. Interactions with plant pathogens influence lipopeptides production and antimicrobial activity of Bacillus subtilis strain PTB185. Biological Control 154: 104497. DOI: https://doi.org/10.1016/j.bioc....
6.
De la Cruz-López N., Cruz-López L., Holguín-Meléndez F., Guillén-Navarro G.K., Huerta-Palacios G. 2022. Volatile organic compounds produced by cacao endophytic bacteria and their inhibitory activity on Moniliophthora roreri. Current Microbiology 79 (2): 35. DOI: https://doi.org/10.1007/s00284....
7.
Diabankana R.G.C., Afordoanyi D.M., Safin R.I., Nizamov R.M., Karimova L.Z., Validov S.Z. 2021. Antifungal properties, abiotic stress resistance, and biocontrol ability of Bacillus mojavensis PS17. Current Microbiology 78 (8): 3124–3132. DOI: https://doi.org/10.1007/s00284....
8.
Fan B., Wang C., Song X., Ding X., Wu L., Wu H., Gao X., Borriss R. 2018. Bacillus velezensis FZB42 in 2018: the grampositive model strain for plant growth promotion and biocontrol. Frontiers in Microbiology 9: 2491. DOI: https://doi.org/10.3389/fmicb.....
9.
FAO. 2021. News Article: New standards to curb the global spread of plant pests and diseases. (n.d.). Available on: https://www.fao.org/news/story... [Accessed: 11 December 2021].
10.
Gao Z., Zhang B., Liu H., Han J., Zhang Y. 2017. Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea. Biological Control 105: 27–39. DOI: https://doi.org/10.1016/j.bioc....
11.
Goldman E., Green L.H. (eds.). 2009. Practical Handbook of Microbiology. 2nd ed. CRC Press.
12.
He C.-N., Ye W.-Q., Zhu Y.-Y., Zhou W.-W. 2020. Antifungal activity of volatile organic compounds produced by Bacillus methylotrophicus and Bacillus thuringiensis against five common spoilage fungi on loquats. Molecules 25 (15): 3360. DOI: https://doi.org/10.3390/molecu....
13.
Ignjatov M., Milosevic D., Nikolic Z., Gvozdanovic-Varga J., Jovicic D., Zdjelar G. 2012. Fusarium oxysporum as causal agent of tomato wilt and fruit rot. Pesticidi i Fitomedicina 27 (1): 25–31. DOI: https://doi.org/10.2298/PIF120....
14.
Jangir M., Pathak R., Sharma S., Sharma S. 2018. Biocontrol mechanisms of Bacillus sp., isolated from tomato rhizosphere, against Fusarium oxysporum f. sp. lycopersici. Biological Control 123: 60–70. DOI: https://doi.org/10.1016/j.bioc....
15.
Jiménez-Gómez A., García-Estévez I., García-Fraile P., Escribano-Bailón M.T., Rivas R. 2020. Increase in phenolic compounds of Coriandrum sativum L. after the application of a Bacillus halotolerans biofertilizer. Journal of the Science of Food and Agriculture 100 (6): 2742–2749. DOI: https://doi.org/10.1002/jsfa.1....
16.
Keswani C., Singh H.B., García-Estrada C., Caradus J., He Y.-W., Mezaache-Aichour S., Glare T.R., Borriss R., Sansinenea E. 2020. Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides. Applied Microbiology and Biotechnology 104 (3): 1013–1034. DOI: https://doi.org/10.1007/s00253....
17.
Khan N., Martínez-Hidalgo P., Ice T.A., Maymon M., Humm E.A., Nejat N., Sanders E.R., Kaplan D., Hirsch A.M. 2018. Antifungal activity of Bacillus species against Fusarium and analysis of the potential mechanisms used in biocontrol. Frontiers in Microbiology 9: 2363. DOI: https://doi.org/10.3389/fmicb.....
18.
Knežević M.M., Stajković-Srbinović O.S., Assel M., Milić M.D., Mihajlovski K.R., Delić D.I., Buntić A.V. 2021. The ability of a new strain of Bacillus pseudomycoides to improve the germination of alfalfa seeds in the presence of fungal infection or chromium. Rhizosphere 18: 100353. DOI: https://doi.org/10.1016/j.rhis....
19.
Kumar J., Ramlal A., Mallick D., Mishra V. 2021. An overview of some biopesticides and their importance in plant protection for commercial acceptance. Plants 10 (6): 1185. DOI: https://doi.org/10.3390/plants....
20.
Lee H., Churey J.J., Worobo R.W. 2008. Purification and structural characterization of bacillomycin F produced by a bacterial honey isolate active against Byssochlamys fulva H25. Journal of Applied Microbiology 105 (3): 663–673. DOI: https://doi.org/10.1111/j.1365....
21.
Lim S.M., Yoon M.-Y., Choi G.J., Choi Y.H., Jang K.S., Shin T.S., Park H.W., Yu N.H., Kim Y.H., Kim J.-C. 2017. Diffusible and volatile antifungal compounds produced by an antagonistic Bacillus velezensis G341 against various phytopathogenic fungi. The Plant Pathology Journal 33 (5): 488–498. DOI: https://doi.org/10.5423/PPJ.OA....
22.
Liu N., Xu S., Yao X., Zhang G., Mao W., Hu Q., Feng Z., Gong Y. 2016. Studies on the control of Ascochyta blight in field peas (Pisum sativum L.) caused by Ascochyta pinodes in Zhejiang province, China. Frontiers in Microbiology 7. DOI: https://doi.org/10.3389/fmicb.....
23.
Logan N.A., Vos P.D. 2015. Bacillus. In: “Bergey’s Manual of Systematics of Archaea and Bacteria” (M.E. Trujillo, S. Dedysh, P. DeVos, B. Hedlund, P. Kämpfer, F.A. Rainey, W.B. Whitman, eds.). DOI: https://doi.org/10.1002/978111....
24.
Masmoudi F., Abdelmalek N., Tounsi S., Dunlap C.A., Trigui M. 2019. Abiotic stress resistance, plant growth promotion and antifungal potential of halotolerant bacteria from a Tunisian solar saltern. Microbiological Research 229: 126331. DOI: https://doi.org/10.1016/j.micr....
25.
Massawe V.C., Hanif A., Farzand A., Mburu D.K., Ochola S.O., Wu L., Tahir H.A.S., Gu Q., Wu H., Gao X. 2018. Volatile compounds of endophytic Bacillus spp. have biocontrol activity against Sclerotinia sclerotiorum. Phytopathology 108 (12): 1373–1385. DOI: https://doi.org/10.1094/PHYTO-....
26.
Mehmood Z., Ahmad I., Mohammad F., Ahmad S. 1999. Indian medicinal plants: a potential source for anticandidal drugs. Pharmaceutical Biology 37 (3): 237–242. DOI: https://doi.org/10.1076/phbi.3....
27.
Mobin S., Usmani M.K. 2017. Consequences of pesticides on environment: a review. G-Journal of Environmental Science and Technology 5 (2): 26–28. Available on: https://gjestenv. com/index.php/gjest/article/view/82 [Accessed: 21 December 2021].
28.
Oldenburg K.R., Vo K.T., Ruhland B., Schatz P.J., Yuan Z. 1996. A dual culture assay for detection of antimicrobial activity. Journal of Biomolecular Screening 1 (3): 123–130. DOI: https://doi.org/10.1177/108705....
29.
Pande S., Siddique K.H.M., Kishore G.K., Bayaa B., Gaur P.M., Gowda C.L.L., Bretag T.W., Crouch J.H. 2005. Ascochyta blight of chickpea (Cicer arietinum L.): a review of biology, pathogenicity, and disease management. Australian Journal of Agricultural Research 56 (4): 317. DOI: https://doi.org/10.1071/AR0414....
30.
Ramírez V., Martínez J., Bustillos-Cristales M.R., Catañeda-Antonio D., Munive J.-A., Baez A. 2022. Bacillus cereus MH778713 elicits tomato plant protection against Fusarium oxysporum. Journal of Applied Microbiology 132 (1): 470–482. DOI: https://doi.org/10.1111/jam.15....
31.
Ramírez-Cariño H.F., Guadarrama-Mendoza P.C., Sánchez-López V., Cuervo-Parra J.A., Ramírez-Reyes T., Dunlap C.A., Valadez-Blanco R. 2020. Biocontrol of Alternaria alternata and Fusarium oxysporum by Trichoderma asperelloides and Bacillus paralicheniformis in tomato plants. Antonie van Leeuwenhoek 113 (9): 1247–1261. DOI: https://doi.org/10.1007/s10482....
32.
Rani L., Thapa K., Kanojia N., Sharma N., Singh S., Grewal A.S., Srivastav A.L., Kaushal J. 2021. An extensive review on the consequences of chemical pesticides on human health and environment. Journal of Cleaner Production 283: 124–657. DOI: https://doi.org/10.1016/j.jcle....
33.
Raza W., Ling N., Yang L., Huang Q., Shen Q. 2016. Response of tomato wilt pathogen Ralstonia solanacearum to the volatile organic compounds produced by a biocontrol strain Bacillus amyloliquefaciens SQR-9. Scientific Reports 6 (1): 24856. DOI: https://doi.org/10.1038/srep24....
34.
Santoyo G., Orozco-Mosqueda Ma. del C., Govindappa M. 2012. Mechanisms of biocontrol and plant growth-promoting activity in soil bacterial species of Bacillus and Pseudomonas: a review. Biocontrol Science and Technology 22 (8): 855–872. DOI: https://doi.org/10.1080/095831....
35.
Sarwar S., Khaliq A., Yousra M., Sultan T., Ahmad N., Khan M.Z. 2020. Screening of siderophore-producing PGPRs isolated from groundnut (Arachis hypogaea L.) rhizosphere and their influence on iron release in soil. Communications in Soil Science and Plant Analysis 51 (12): 1680–1692. DOI: https://doi.org/10.1080/001036....
36.
Shafi J., Tian H., Ji M. 2017. Bacillus species as versatile weapons for plant pathogens: a review. Biotechnology & Biotechnological Equipment 31 (3): 446–459. DOI: https://doi.org/10.1080/131028....
37.
Slama H.B., Cherif-Silini H., Chenari Bouket A., Qader M., Silini A., Yahiaoui B., Alenezi F.N., Luptakova L., Triki M.A., Vallat A., Oszako T., Rateb M.E., Belbahri L. 2019. Screening for Fusarium antagonistic bacteria from contrasting niches designated the endophyte Bacillus halotolerans as plant warden against Fusarium. Frontiers in Microbiology 9. DOI: https://doi.org/10.3389/fmicb.....
38.
Spadaro D., Gullino M.L. 2005. Improving the efficacy of biocontrol agents against soilborne pathogens. Crop Protection 24 (7): 601–613. DOI: https://doi.org/10.1016/j.crop....
39.
Stenberg J.A., Sundh I., Becher P.G., Björkman C., Dubey M., Egan P.A., Friberg H., Gil J.F., Jensen D.F., Jonsson M., Karlsson M., Khalil S., Ninkovic V., Rehermann G., Vetukuri R.R., Viketoft M. 2021. When is it biological control? A framework of definitions, mechanisms, and classifications. Journal of Pest Science 94 (3): 665–676. DOI: https://doi.org/10.1007/s10340....
40.
Ting A.S.Y., Mah S.W., Tee C.S. 2011. Detection of potential volatile inhibitory compounds produced by endobacteria with biocontrol properties towards Fusarium oxysporum f. sp. cubense race 4. World Journal of Microbiology and Biotechnology 27 (2): 229–235. DOI: https://doi.org/10.1007/s11274....
41.
Toral L., Rodríguez M., Béjar V., Sampedro I. 2018. Antifungal activity of Lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Frontiers in Microbiology 9: 1315. DOI: https://doi.org/10.3389/fmicb.....
42.
Valencia-Cantero E., Hernández-Calderón E., Velázquez-Becerra C., López-Meza J.E., Alfaro-Cuevas R., López-Bucio J. 2007. Role of dissimilatory fermentative iron-reducing bacteria in Fe uptake by common bean (Phaseolus vulgaris L.) plants grown in alkaline soil. Plant and Soil 291 (1): 263–273. DOI: https://doi.org/10.1007/s11104....
43.
Velho R.V., Medina L.F.C., Segalin J., Brandelli A. 2011. Production of lipopeptides among Bacillus strains showing growth inhibition of phytopathogenic fungi. Folia Microbiologica 56 (4): 297–303. DOI: https://doi.org/10.1007/s12223....
44.
Wang H., Hwang S.F., Chang K.F., Turnbull G.D., Howard R.J. 2003. Suppression of important pea diseases by bacterial antagonists. BioControl 48 (4): 447–460. DOI: https://doi.org/10.1023/A:1024....
45.
Weller D.M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology 26 (1): 379–407. DOI: https://doi.org/10.1146/annure....
46.
Wu X., Wu H., Wang R., Wang Z., Zhang Y., Gu Q., Farzand A., Yang X., Semenov M., Borriss R., Xie Y., Gao X. 2021. Genomic features and molecular function of a novel stresstolerant Bacillus halotolerans strain isolated from an extreme environment. Biology 10 (10): 1030. DOI: https://doi.org/10.3390/biolog....
47.
Xu W., Wang K., Wang H., Liu Z., Shi Y., Gao Z., Wang Z. 2020. Evaluation of the biocontrol potential of Bacillus sp. WB against Fusarium oxysporum f. sp. niveum. Biological Control 147: 104288. DOI: https://doi.org/10.1016/j.bioc....
48.
Yao D., Ji Z., Wang C., Qi G., Zhang L., Ma X., Chen S. 2012. Coproducing iturin A and poly-γ-glutamic acid from rapeseed meal under solid state fermentation by the newly isolated Bacillus subtilis strain 3-10. World Journal of Microbiology and Biotechnology 28 (3): 985–991. DOI: https://doi.org/10.1007/s11274....
49.
Yu X., Ai C., Xin L., Zhou G. 2011. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. European Journal of Soil Biology 47 (2): 138–145. DOI: https://doi.org/10.1016/j.ejso....
50.
Zhang D., Yu S., Yang Y., Zhang J., Zhao D., Pan Y., Fan S., Yang Z., Zhu J. 2020. Antifungal effects of volatiles produced by Bacillus subtilis against Alternaria solani in potato. Frontiers in Microbiology 11: 1196. DOI: https://doi.org/10.3389/fmicb.....
51.
Zhao Y., Selvaraj J.N., Xing F., Zhou L., Wang Y., Song H., Tan X., Sun L., Sangare L., Folly Y.M.E., Liu Y. 2014. Antagonistic action of Bacillus subtilis strain SG6 on Fusarium graminearum. PLoS ONE 9 (3): e92486. DOI: https://doi.org/10.1371/journa....
52.
Zhu J., Tan T., Shen A., Yang X., Yu Y., Gao C., Li Z., Cheng Y., Chen J., Guo L., Sun X., Yan Z., Li J., Zeng L. 2020. Biocontrol potential of Bacillus subtilis IBFCBF-4 against Fusarium wilt of watermelon. Journal of Plant Pathology 102 (2): 433–441. DOI: https://doi.org/10.1007/s42161....
53.
Zouari I., Masmoudi F., Medhioub K., Tounsi S., Trigui M. 2020. Biocontrol and plant growth-promoting potentiality of bacteria isolated from compost extract. Antonie van Leeuwenhoek 113 (12): 2107–2122. DOI: https://doi.org/10.1007/s10482....
Share
RELATED ARTICLE
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.