Controlling Soil-Borne Fungus Aspergillus niger in Groundnut By Optimizing The Function of Isolated Bacillus Bacteria

Nguyen Xuan Hieu; Nguyen Duc Huy; Tien Long Nguyen; Cao Thi Thuyet; Pham Thi Thuy Hoai; Nguyen Thi Thu  Thuy

doi:10.55230/mabjournal.v53i2.3012

Authors

Nguyen Xuan Hieu Institute of Biotechnology, Hue University, Thua Thien Hue 49000, Vietnam
Nguyen Duc Huy Institute of Biotechnology, Hue University, Thua Thien Hue 49000, Vietnam
Nguyen Tien Long https://csdlkhoahoc.hueuni.edu.vn/index.php/scientist/detail/id/2676
Cao Thi Thuyet University of Agriculture and Forestry, Hue University, Thua Thien Hue 49000, Vietnam
Pham Thi Thuy Hoai MienTrung Institute of Scientific Research, Vietnam National Museum of Nature, Vietnam; Academy of Science and Technology (VAST), Thua Thien Hue 49000, Vietnam
Nguyen Thi Thu Thuy
nguyenthithuthuy@huaf.edu.vn
Institute of Biotechnology, Hue University, Thua Thien Hue 49000, Vietnam

Keywords:

Aspergillus niger , Bacillus, biocontrol, collar rot disease, bambara groundnut

Abstract

Collar rot is a devastating disease caused by the soil-borne pathogen Aspergillus niger that greatly affects groundnut production worldwide. The long-term persistence of the fungus in the soil can reduce the effectiveness of synthetic fungicides. Recently, significant attention has been raised to the use of the biological control method such as the application of antagonistic microorganisms, which potentially decline the number of spores and eradicated A. niger from the soil. In the present study, three Bacillus strains (Bacillus siamensis 101, B. siamensis 112 and B. velezensis 137) isolated from the rhizosphere soil of groundnut cultivation farms were found to inhibit the growth of A. niger mycelia by 53.6% to 60.8% in vitro. In pot experiments, the supplementation of this mixture of three bacterial strains (namely BAZ04) strongly reduced the collar rot symptoms of groundnut with a biocontrol efficacy of 100% compared to nil (no treatment). Field trials demonstrated the efficiency of BAZ04 in controlling collar rot disease, which increased the yield by 20.5–22.7% compared to the untreated plots. These results suggest that BAZ04 is a potential biocontrol agent for collar rot disease.

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References

Ajuna, H.B., Lim, H.I., Moon, J.H., Won, S.J., Choub, V., Choi, S.I., Yun, J.Y. & Ahn, Y.S. 2023. The Prospect of hydrolytic enzymes from Bacillus species in the biological control of pests and diseases in forest and fruit tree production. International Journal of Molecular Sciences, 24(23): 16889. DOI: https://doi.org/10.3390/ijms242316889

Andric, S., Meyer, T. & Ongena, M. 2020. Bacillus responses to plant-associated fungal and bacterial communities. Frontiers in Microbiology, 11: 1350. DOI: https://doi.org/10.3389/fmicb.2020.01350

Anith, K., Nysanth, N. & Natarajan, C. 2021. Novel and rapid agar plate methods for in vitro assessment of bacterial biocontrol isolates antagonism against multiple fungal phytopathogens, Letters in Applied Microbiology. 73: 229-236. DOI: https://doi.org/10.1111/lam.13495

Arya, S.S., Salve, A.R. & Chauhan, S. 2016. Peanuts as functional food: A review, Journal of Food Science and Technology, 53(1): 31-41. DOI: https://doi.org/10.1007/s13197-015-2007-9

Bathke, K.J., Jochum, C.C. & Yuen, G.Y. 2022. Biological control of bacterial leaf streak of corn using systemic resistance-inducing Bacillus strains, Crop Protection, 155: 105932. DOI: https://doi.org/10.1016/j.cropro.2022.105932

Cao, Y. & Pi, H. 2018. Antagonism of two plant-growth promoting Bacillus velezensis isolates against Ralstonia solanacearum and Fusarium oxysporum. Scientific Reports, 8: 4360. DOI: https://doi.org/10.1038/s41598-018-22782-z

Castaldi, S., Masi, M., Sautua, F., Cimmino, A., Isticato, R., Carmona, M., Tuzi A. & Evidente, A. 2021. Pseudomonas fluorescens showing antifungal activity against Macrophomina phaseolina, a severe pathogenic fungus of Soybean, produces phenazine as the main active metabolite. Biomolecules, 11(11): 1728. DOI: https://doi.org/10.3390/biom11111728

Chen, L., Shi, H., Heng, J., Wang, D. & Bian, K. 2019. Antimicrobial, plant growth-promoting and genomic properties of the peanut endophyte Bacillus velezensis LDO2. Microbiological Research, 218: 41-48. DOI: https://doi.org/10.1016/j.micres.2018.10.002

Chowdhury, S.P., Dietel, K., Rändler, M., Schmid, M., Junge, H., Borriss, R., Hartmann, A. & Grosch, R. 2013. Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the Rhizosphere bacterial community. PLoS One, 8: e68818. DOI: https://doi.org/10.1371/journal.pone.0068818

Dadrasnia, M., Usman, M., Omar, R., Ismail, S. & Abdullah, R.J. 2020. Potential use of Bacillus genus to control of bananas diseases: Approaches toward high yield production and sustainable management. King Saud University, 32: 2336-2342. DOI: https://doi.org/10.1016/j.jksus.2020.03.011

Dong, W., Liu, H., Ning, Z., Bian, Z., Zeng L. & Xie D. 2023. Inoculation with Bacillus cereus DW019 modulates growth, yield and rhizospheric mcrobial community of cherry tomato. Agronomy, 13(6):1458. DOI: https://doi.org/10.3390/agronomy13061458

Fabra, A., Castro, S., Taurian, T., Angelini, J., Ibanez, F., Dardanelli, M., Tonelli, M., Bianucci, E. & Valetti, L. 2010. Interaction among Arachis hypogaea L. (peanut) and beneficial soil microorganisms: how much is it known? Critical Reviews in Microbiology, 36(3): 179-194. DOI: https://doi.org/10.3109/10408410903584863

Gajera, H., Rakholiya, K. & Vakharia, D. 2011. Bioefficacy of Trichoderma isolates against Aspergillus niger van Tieghem inciting collar rot in groundnut (Arachis hypogaea L.). Journal of Plant Protection Research, 51(3): 240-247. DOI: https://doi.org/10.2478/v10045-011-0040-x

Gikas, G.D., Parlakidis, P., Mavropoulos, T. & Vryzas, Z. 2022. Particularities of fungicides and factors affecting their fate and removal efficacy: A review. Sustainability (Switzerland), 14(5): 4056. DOI: https://doi.org/10.3390/su14074056

Guchi, E., Ayalew, A., Dejene, M., Ketema, M., Asalf, B. & Fininsa C. 2014. Occurrence of Aspergillus species in groundnut (Arachis hypogaea L.) along the value chain in different Aagro-ecological zones of eastern Ethiopia. Applied and Environmental Microbiology, 2(6): 309-317. DOI: https://doi.org/10.1186/s40550-015-0014-2

Haruna, A. & Yahaya S.M. 2021. Recent Advances in the Chemistry of bioactive compounds from plants and soil microbes: A review. Chemistry Africa, 8: 231-345. DOI: https://doi.org/10.1007/s42250-020-00213-9

Hashem, A., Tabassum, B. & Fathi Abd Allah E. 2019. Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi Journal of Biological Sciences, 26(6): 1291-1297. DOI: https://doi.org/10.1016/j.sjbs.2019.05.004

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.biocontrol.2018.04.018

Janila, P., Nigam, S.N., Pandey, M.K., Nagesh, P. & Varshney, R.K. 2013. Groundnut improvement: Use of genetic and genomic tools. Frontiers in Plant Science, 4: 23. DOI: https://doi.org/10.3389/fpls.2013.00023

Kim, H.S., Kim, S.W., Adhikari, M. & Lee, Y.S. 2021. Antagonistic effects and biochemical properties of bacteria isolated from soil. Journal of Agricultural, Life and Environmental Sciences, 33(2): 125-135.

Kumari, M. & Singh, M. 2017. Management of collar rot disease of groundnut (Arachis hypogaea L.) caused by Aspergillus niger through bio-agents. International Journal of Chemical Studies, 5(4): 73-76.

Kuzina, A.I, Tagaevb, A.A., Ovchinnikovab, T.V., Kuznetsovaa, N.I., Nikolaenkoa, M.A., Morozovac, O.A. & Azizbekyana, R.R. 2019. Study of the strain Bacillus pumilus B-13176 and its metabolites with fungicidal and antibacterial activities against Aspergillus niger and Staphylococcus aureus (MRSA. Applied Biochemistry and Microbiology, 55(7): 748-755. DOI: https://doi.org/10.1134/S0003683819070056

Le, C.N., Hoang, T.K., Thai, T.H., Tran, T.L., Phan, T.P.N. & Raaijmakers, J.M. 2018. Isolation, characterization and comparative analysis of plant-associated bacteria for suppression of soil-borne diseases of field-grown groundnut in Vietnam. Biological Control, 121: 256-262. DOI: https://doi.org/10.1016/j.biocontrol.2018.03.014

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(9): e0162125. DOI: https://doi.org/10.1371/journal.pone.0162125

Lora, S. & Begum, T. 2019. Managing of collar rot disease in groundnut (Arachis hypogaea L.) by few chemicals. International Journal of Research in BioSciences, 6(3): 133-136. DOI: https://doi.org/10.26438/ijsrbs/v6i3.133136

Mirskaya, G.V., Khomyakov, Y.V., Rushina, N.A., Vertebny, V.E., Chizhevskaya, E.P., Chebotar, V.K., Chesnokov, Y.V. & Pishchik, V.N. 2022. Plant development of early-maturing spring wheat (Triticum aestivum L.) under inoculation with Bacillus sp. V2026, Plants, 11(14): 1817. DOI: https://doi.org/10.3390/plants11141817

Mohammed, A. & Chala, A. 2014. Incidence of Aspergillus contamination of groundnut (Arachis hypogaea L.) in Eastern Ethiopia. African Journal of Microbiology Research, 8(8): 759-765. DOI: https://doi.org/10.5897/AJMR12.2078

Nathawat, B.D.S., Singh, N., Singh, S.P., Kumar, D., Shivran, H. & Shekhawat, D.S. 2021. Screening of groundnut cultivars against collar rot (Aspergillus niger van Tiegham). International Journal of Current Microbiology and Applied Sciences, 10(2): 1912-1917. DOI: https://doi.org/10.20546/ijcmas.2021.1002.228

Navale, V., Vamkudoth, K.R., Ajmera, S. & Dhuri, V. 2021. Aspergillus derived mycotoxins in food and the environment: Prevalence, detection, and toxicity. Toxicology Reports, 8: 1008-1030. DOI: https://doi.org/10.1016/j.toxrep.2021.04.013

Nguyen, M.N., Nguyen, X.H., Nguyen, T.L., Nguyen, D.H. & Nguyen T.T.T. 2024. Isolation and characterization of antagonistic bacterial strains for biocontrol of collar rot (Aspergillus niger) in groundnut (Arachis hypogaea L.). Chiang Mai Journal of Science, 51(2): e 2024022.

Nguyen, X.H., Nguyen, T.M.N., Nguyen, D.H., Nguyen, Q.C., Cao, T.T., Pham, T.T.H. & Nguyen T.T.T. 2023. Identification and characterization of Aspergillus niger causing collar rot of groundnut (Arachis hypogaea). Biodiversitas, 24(5): 2556-2562. DOI: https://doi.org/10.13057/biodiv/d240507

Okigbo, R.N. 2016. Healthy plants today for healthy man tomorrow. An Inaugural Lecture of Nnamdi Azikwe University, Awka. Noble Press Ltd. pp. 68.

Omugo, J.E., Amadi, J.E., Okere, C.S., Kemka-Evans, C.I. & Nguma, M.O. 2018. Fungal isolates of groundnut (Arachis hypogaea L) seeds in Owerri metropolis, Nigeria. Nigerian Journal of Mycology, 10: 31-45.

Putri, B.R., Santoso I. & Yasman Y. 2020. Antagonistic potential of Bacillus siamensis LDR against Aspergillus niger ABP and ART. AIP Conference Proceedings, 050017: 22-42. DOI: https://doi.org/10.1063/5.0012314

Rao, A.P. & Nnaji, P.T. 2017. Antagonistic potential of soil bacteria against plant pathogenic fungi: Aspergillus niger. Microbiology Research Journal International, 19(5): 1-7. DOI: https://doi.org/10.9734/MRJI/2017/29725

Sayyed, R.Z., Gangurde, N.S., Patel, P.R., Joshi, S.A. & Chincholkar, S.B. 2010. Siderophore production by Alcaligenes faecalis and its application for growth promotion in Arachis hypogaea. Indian Journal of Biotechnology, 9: 302-307.

Shakeel, Q., Lyu, A., Zhang, J., Wu, M., Li, G., Hsiang, T. & Yang, L. 2018. Biocontrol of Aspergillus flavus on peanut kernels using Streptomyces yanglinensis 3-10. Frontiers in Microbiology, 9: 1049. DOI: https://doi.org/10.3389/fmicb.2018.01049

Sharma, A., Kaushik, N., Sharma, A., Bajaj, A., Rasane, M., Shouche, Y.S., Marzouk, T. & Djébali, N. 2021. Screening of tomato seed bacterial endophytes for antifungal activity reveals lipopeptide producing Bacillus siamensis strain NKIT9 as a potential bio-control agent. Frontiers in Microbiology, 12: 609482. DOI: https://doi.org/10.3389/fmicb.2021.609482

Soliman, S.A., Abdelhameed, R.E. & Metwally, R.A. 2023. In vivo and In vitro evaluation of the antifungal activity of the PGPR Bacillus amyloliquefaciens RaSh1 (MZ945930) against Alternaria alternata with growth promotion influences on Capsicum annuum L. plants. Microbial Cell Factories, 22(70): 1-20. DOI: https://doi.org/10.1186/s12934-023-02080-8

Wei, S., Hu, C., Zhang, Y., Lv, Y., Zhang, S., Zhai, H. & Hu, Y. 2023. An Azf1 acts as a positive regulator of ochratoxin A biosynthesis in Aspergillus niger. Applied Microbiology and Biotechnology, 107(7-8): 2501-2514. DOI: https://doi.org/10.1007/s00253-023-12404-8

Xu, T., Zhu, T. & Li, S. 2016. β-1,3-1,4-glucanase gene from Bacillus velezensis ZJ20 exerts Antifungal effect on plant pathogenic fungi. World Journal of Microbiology and Biotechnology, 32(2): 26. DOI: https://doi.org/10.1007/s11274-015-1985-0

Yadav, D.K., Devappa, V., Kashyap, A.S., Kumar, N., Rana, V.S., Sunita, K. & Singh, D. 2023. Boosting the biocontrol efficacy of Bacillus amyloliquefaciens DSBA-11 through physical and chemical mutagens to control bacterial wilt disease of tomato caused by Ralstonia solanacearum. Microorganisms, 11(7): 1790. DOI: https://doi.org/10.3390/microorganisms11071790

Yánez-Mendizábal, V. & Falconí, C.E. 2021. Bacillus subtilis CtpxS2-1 induces systemic resistance against anthracnose in Andean lupin by lipopeptide production. Biotechnology Letters, 43: 719-728. DOI: https://doi.org/10.1007/s10529-020-03066-x

Zhang, Q., Stummer, B.E., Guo, Q., Zhang, W., Zhang, X., Zhang, L. & Harvey, P.R. 2021. Quantification of Pseudomonas protegens FD6 and Bacillus subtilis NCD-2 in soil and the wheat rhizosphere and suppression of root pathogenic Rhizoctonia solani AG-8. Biological Control, 154: 104504. DOI: https://doi.org/10.1016/j.biocontrol.2020.104504