Inhibición del crecimiento in vitro de Bacillus spp sobre hongos asociados al proceso de fermentación en cacao
Abstract
Los hongos productores de Ocratoxina A (OTA) en el cacao son un problema de seguridad alimentaria que afecta la calidad organoléptica del chocolate y a la salud humana. Dado que las cepas de Bacillus spp resultan ser efectivos controladores biológicos, el objetivo de este trabajo fue inhibir el crecimiento de hongos productores de OTA. Para ello, se ensayó el antagonismo in vitro de dosis de 100 y 200 µL de Bacillus spp contra hongos aislados de granos de cacao en proceso de fermentación: Aspergillus spp y Penicillium sp. Los resultados de este estudio demuestran que la cepa de B. subtilis 31BMC y B. licheniformis E-44 disminuyeron significativamente el crecimiento por aislados de Aspergillus spp y Penicillium sp, inhibiendo su crecimiento en un 74,43% y 81,52%, transcurridos tres días, respectivamente. Las cepas de Bacillus spp demostraron ser efectivas en la inhibición in vitro de hongos productores de OTA en granos de cacao.
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Almeida, O. G. G. D., Pinto, U. M., Matos, C. B., Frazilio, D. A., Braga, V. F., von Zeska-Kress, M. R., & De Martinis, E. C. P. (2020). Does quorum sensing play a role in microbial shifts along spontaneous fermentation of cocoa beans? An in silico perspective. Food Research International, 131, 109034. https://doi.org/10.1016/j.foodres.2020.109034
Astorga-Quirós, K., Meneses-Montero, K., Zúñiga-Vega, C., Brenes-Madriz, J. A., & Rivera-Méndez, W. (2014). Evaluación del antagonismo de Trichoderma sp. y Bacillus subtilis contra tres patógenos del ajo. Revista Tecnología En Marcha, 27(2), pág. 82–91. https://doi.org/10.18845/tm.v27i2.1929
Bharose, A., & Gajera, H. (2018). Antifungal Activity and Metabolites Study of Bacillus Strain Against Aflatoxin Producing Aspergillus. Journal of Applied Microbiology and Biochemistry, 02(02), https://doi.org/10.21767/2576-1412.100024
Bhushan, G., Chhangani, S., Singh, J., & Singh, A. P. (2013). Antagonistic Effects of Bacillus subtilis and Pseudomonas fluorescens Against Seed-Borne Mycoflora of Pennisetum Americanum. 1(3), 71-75.
Bonilla, J. (2013). Análisis de Ocratoxina en chocolate de hoja comercializado en los mercados de la ciudad de Cuenca [Tesis de maestría, Universidad del Azuay]. Repositorio Institucional Universidad del Azuay.
Cajiao, A. P. (2017). Aislamiento de hongos asociados al grano de café provenientes de zonas productoras en norte de Santander - Colombia. @limentech, Ciencia y Tecnología Alimentaria, 14(1), 50-58. https://doi.org/10.24054/16927125.v1.n1.2016.2125
Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C., & Mahillon, J. (2019). Overview of the Antimicrobial Compounds Produced by Members of the Bacillus subtilis Group. Frontiers in Microbiology, 10, 302. https://doi.org/10.3389/fmicb.2019.00302
Cawoy, H., Debois, D., Franzil, L., De Pauw, E., Thonart, P., & Ongena, M. (2015). Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/amyloliquefaciens: Lipopeptides as inhibitors of phytopathogens. Microbial Biotechnology, 8(2), 281-295. https://doi.org/10.1111/1751-7915.12238
Chitarra, G. S., Breeuwer, P., Nout, M. J. R., van Aelst, A. C., Rombouts, F. M., & Abee, T. (2003). An antifungal compound produced by Bacillus subtilis YM 10-20 inhibits germination of Penicillium roqueforti conidiospores. Journal of Applied Microbiology, 94(2), 159-166. https://doi.org/10.1046/j.1365-2672.2003.01819.x
Chowdhury, S. P., Hartmann, A., Gao, X., & Borriss, R. (2015). Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review. Frontiers in Microbiology, 6. https://doi.org/10.3389/fmicb.2015.00780
Copetti, M. V., Pereira, J. L., Iamanaka, B. T., Pitt, J. I., & Taniwaki, M. H. (2010). Ochratoxigenic fungi and ochratoxin A in cocoa during farm processing. International Journal of Food Microbiology, 143(1-2), 67-70.
Derya, I. C., Abuzer, C., & Canan, C. (2019). Relationship between soil composition, diversity and antifungal properties of Bacillus spp. Isolated from southeastern Anatolia. Biotechnology & Biotechnological Equipment, 33(1), 170-177. https://doi.org/10.1080/13102818.2018.1559095
Einloft, T. C., Oliveira, P. B. D., Veras, F. F., Welke, J. E., Mallmann, C. A., Dilkin, P., & Dionello, R. G. (2017). Effect of Bacillus spp. on Aspergillus westerdijkiae growth, sporulation and ochratoxin A production in green-coffee medium. Food Science and Technology, 37, 24-27.
Fan, H., Zhang, Z., Li, Y., Zhang, X., Duan, Y., & Wang, Q. (2017). Biocontrol of Bacterial Fruit Blotch by Bacillus subtilis 9407 via Surfactin-Mediated Antibacterial Activity and Colonization. Frontiers in Microbiology, 8, 1973.
Figueiredo, J. E. F., Teixeira, M. A., Lima, G. V. C., Bressan, W., Pinto, N. F. J. de, & Casela, C. R. (2010). Atividade antagonista in vitro de Bacillus subtilis contra fungos fitopatogênicos do milho e sorgo. http://www.alice.cnptia.embrapa.br/handle/doc/865392
Florido, G. M., Rondón, A. J., Pérez, M., Arteaga, F., Bocourt, R., Portilla, Y., Rodríguez, M., Pérez, Y., Beruvides, A., & Laurencio, M. (2017). Methodology for the isolation, identification and selection of Bacillus spp. Strains for the preparation of animal additives. Cuban Journal of Agricultural Science, 51(2), 11.
Ghazaei C. (2022). Study of the Effect of Bacteriocin-producing Bacillus subtilis Strains on Beta-lactamase-producing Pathogenic Bacteria. J Clin Res Paramed Sci., 11(2), e130208. https://doi.org/10.5812/jcrps-130208.
He, S., Feng, K., Ding, T., Huang, K., Yan, H., Liu, X., & Zhang, Z. (2018). Complete genome sequence of Bacillus licheniformis BL-010. Microbial Pathogenesis, 118, 199-201. https://doi.org/10.1016/j.micpath.2018.03.037
He, Y., Zhu, M., Huang, J., Hsiang, T., & Zheng, L. (2019). Biocontrol potential of a Bacillus subtilis strain BJ-1 against the rice blast fungus Magnaporthe oryzae. Canadian Journal of Plant Pathology, 41(1), 47-59. https://doi.org/10.1080/07060661.2018.1564792
IARC, & WHO. (1993). Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins. Report IARC & WHO.
Kadjo, A. C., Beugre, G. C., Sess-Tchotch, D. A., Kedjebo, K. B. D., Mounjouenpou, P., Durand, N., ... & Guehi, S. T. (2023). Screening of anti-fungal Bacillus strains and influence of their application on cocoa beans fermentation and final bean quality. Journal of Advances in Microbiology, 23(1), 8-17.
Leelasuphakul, W., Hemmanee, P., & Chuenchitt, S. (2008). Growth inhibitory properties of Bacillus subtilis strains and their metabolites against the green mold pathogen (Penicillium digitatum Sacc.) of citrus fruit. Postharvest biology and technology, 48(1), 113-121.
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. https://doi.org/10.1371/journal.pone.0162125
Li, Z., Fernandez, K. X., Vederas, J. C., & Gänzle, M. G. (2023). Composition and activity of antifungal lipopeptides produced by Bacillus spp. in daqu fermentation. Food Microbiology, 111, 104211. https://doi.org/10.1016/j.fm.2022.104211
Malir, F., Ostry, V., Pfohl-Leszkowicz, A., & Novotna, E. (2013). Ochratoxin A: developmental and reproductive toxicity-an overview. Birth defects research. Part B, Developmental and reproductive toxicology, 98(6), 493–502. https://doi.org/10.1002/bdrb.21091
Manda, P., Dano, D. S., Kouadio, J. H., Diakité, A., Sangaré-Tigori, B., Ezoulin, M. J. M., Soumahoro, A., Dembele, A., & Fourny, G. (2009). Impact of industrial treatments on ochratoxin A content in artificially contaminated cocoa beans. Food Additives & Contaminants: Part A, 26(7), 1081-1088. https://doi.org/10.1080/02652030902894397
Muzaifa, M., Hasni, D., Febriani, Patria, A., & Abubakar, A. (2019). Fermentation of coffee beans with inoculation of bacillus subtilis and its impact on coffee sensory quality. IOP Conference Series: Earth and Environmental Science, 364, 012010.
NTP. (1988). NTP 488: Calidad de aire interior: Identificación de hongos. Notas técnicas preventivas. Gobierno de Costa Rica.
Palacios Gonzaga, M. F. (2021). Determinación de la actividad antifúngica de biomasa y lipopéptidos de un aislamiento de Bacillus subtilis durante la antibiosis contra hongos filamentosos de la poscosecha de cacao. [Tesis de grado]. Universidad de la Fuerza Armadas.
Palumbo, J. D., Baker, J. L., & Mahoney, N. E. (2006). Isolation of Bacterial Antagonists of Aspergillus flavus from Almonds. Microbial Ecology, 52(1), 45-52. https://doi.org/10.1007/s00248-006-9096-y
Podile AR, Prakash AP. (1996). Lysis and biological control of Aspergillus niger by Bacillus subtilis AF1. Can J Microbiol. Jun;42(6):533-8. doi: 10.1139/m96-072. PMID: 8801004.
Pontón, J. (2008). La pared celular de los hongos y el mecanismo de acción de la anidulafungina. Revista Iberoamericana de Micología, 25(2), 78-82. https://doi.org/10.1016/S1130-1406(08)70024-X
Putri, R. E., Al-Faruq, M. M., Fahrurrozi, F., & Lisdiyanti, P. (2023, January). Exploration of antifungal activity from cacao seed coat slime-associated bacteria. In AIP Conference Proceedings (Vol. 2606, No. 1). AIP Publishing. https://doi.org/10.1063/5.0119481
Ramos, N. R., Castro, A., Juárez, J., Acha de la Cruz, O., Rodríguez, N., Blancas, J., Escudero, J., Escudero, J., & Navarro, A. (2016). Evaluación de ocratoxina a en Theobroma cacao L. “cacao blanco” durante el proceso de cosecha, fermentado, secado y almacenado. Revista de la Sociedad Química del Perú, 82(4), 431-439. https://doi.org/10.37761/rsqp.v82i4.133
Ravelo, A., Rubio, C., Gutiérrez, A., & Hardisson de la Torre, A. (2011). La ocratoxina A en alimentos de consumo humano: Revisión. Nutrición hospitalaria, 6, 1215-1226. https://doi.org/10.3305/nh.2011.26.6.5381
Sadfi, N., Chérif, M., Hajlaoui, M. R., Boudabbous, A., & Bélanger, R. (2002). Isolation and partial purification of antifungal metabolites produced by Bacillus cereus. Ann Microbiol, 52, 323-337.
Samson, R. A., Visagie, C. M., Houbraken, J., Hong, S.-B., Hubka, V., Klaassen, C. H. W., Perrone, G., Seifert, K. A., Susca, A., Tanney, J. B., Varga, J., Kocsubé, S., Szigeti, G., Yaguchi, T., & Frisvad, J. C. (2014). Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology, 78, 141-173. https://doi.org/10.1016/j.simyco.2014.07.004
Seifert, K. A., & Gams, W. (2011). The genera of Hyphomycetes - 2011 update. Persoonia, 27, 119–129. https://doi.org/10.3767/003158511X617435
Serra, J. L., Moura, F. G., de Melo Pereira, G. V., Soccol, C. R., Rogez, H., & Darnet, S. (2019). Determination of the microbial community in Amazonian cocoa bean fermentation by Illumina-based metagenomic sequencing. LWT, 106, 229-239. https://doi.org/10.1016/j.lwt.2019.02.038
Siahmoshteh, F., Hamidi-Esfahani, Z., Spadaro, D., Shams-Ghahfarokhi, M., & Razzaghi-Abyaneh, M. (2018). Unraveling the mode of antifungal action of Bacillus subtilis and Bacillus amyloliquefaciens as potential biocontrol agents against aflatoxigenic Aspergillus parasiticus. Food Control, 89, 300-307.
Sukkasem, P., Kurniawan, A., Kao, T.-C., & Chuang, H. (2018). A multifaceted rhizobacterium Bacillus licheniformis functions as a fungal antagonist and a promoter of plant growth and abiotic stress tolerance. Environmental and Experimental Botany, 155, 541-551. https://doi.org/10.1016/j.envexpbot.2018.08.005
Teixeira de Magalhães, J., Sodré, G. A., Viscogliosi, H., & Grenier-Loustalot, M.-F. (2011). Occurrence of Ochratoxin A in Brazilian cocoa beans. Food Control, 22(5), 744-748. https://doi.org/10.1016/j.foodcont.2010.11.006
Toaza, A. (2012). Evaluación de los niveles de Ocratoxina A en almendras de cacao, mediante el método de cromatografía líquida de alta eficiencia (HPLC), usando columnas de fase—Reversa (SPE) y caracterización al hongo productor de ocratoxina A. [Tesis de grado, Escuela Politécnica del Ejercito]. Repositorio Dspace http://repositorio.espe.edu.ec/xmlui/handle/21000/5868
Ul Hassan, Z., Al Thani, R., Alnaimi, H., Migheli, Q., & Jaoua, S. (2019). Investigation and application of Bacillus licheniformis volatile compounds for the biological control of toxigenic Aspergillus and Penicillium spp. ACS omega, 4(17), 17186-17193.
Wang, L., Hua, X., Shi, J., Jing, N., Ji, T., Lv, B., ... & Chen, Y. (2022). Ochratoxin A: Occurrence and recent advances in detoxification. Toxicon, 210, 11-18. https://doi.org/10.1016/j.toxicon.2022.02.010
Yi, P.-J., Pai, C.-K., & Liu, J.-R. (2011). Isolation and characterization of a Bacillus licheniformis strain capable of degrading zearalenone. World Journal of Microbiology and Biotechnology, 27(5), 1035-1043. https://doi.org/10.1007/s11274-010-0548-7.
Zhao, M., Liu, D., Liang, Z., Huang, K., & Wu, X. (2022). Antagonistic activity of Bacillus subtilis CW14 and its β-glucanase against Aspergillus ochraceus. Food Control, 131, 108475.
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