Aspergillus species associated with grains of groundnuts (Arachis hypogaea L.) and common beans (Phaseolus vulgaris L.) cultivated in Costa Rica

Authors

  • Fabiola Carranza-Mesén Universidad de Costa Rica, Centro de Investigación en Granos y Semillas, San José, Costa Rica https://orcid.org/0000-0003-2959-7229
  • Mónica Blanco-Meneses Universidad de Costa Rica, Centro de Investigación en Protección de Cultivos, San José, Costa Rica https://orcid.org/0000-0003-2642-3899
  • Maria del Milagro Granados-Montero Universidad de Costa Rica, Fabio Baudrit Moreno Agricultural Experimental Station, Alajuela, Costa Rica. Centro de Investigaciones en Estructuras Microscópicas, C.P. 11501, Alajuela, Costa Rica https://orcid.org/0000-0002-0321-7729
  • Maria Vinas Meneses Universidad de Costa Rica, Centro de Investigación en Granos y Semillas, San José, Costa Rica

DOI:

https://doi.org/10.15517/am.v33iEspecial.50810

Keywords:

fungi, mycotoxins, postharvest, atoxigenic

Abstract

Introduction. Common beans (Phaseolus vulgaris L.) and peanuts (Arachis hypogaea L.) are legumes, widely consumed in developing countries. However, those grains could be contaminated with Aspergillus, a genus of fungus that includes mycotoxin-producing species. Objective. To identify the Aspergillus species that colonize the grains of common beans and peanuts in Costa Rica and to identify atoxigenic strains of A. flavusMaterials and methods. Eighty-three samples of common bean grains and nineteen samples of peanuts were collected during the years 2019 and 2020 in regions where those grains are produced in Costa Rica. All samples were used to isolate and identify Aspergillus species by partial sequences of ITS (internal transcribed spacer) and cmd (calmodulin) genes. Atoxigenic strains of A. flavus were also identified by chemical and molecular methods. Results. 46 % and 32 % of the collected common beans and peanuts samples, respectively, were contaminated with Aspergillus spp. In common beans, 85 isolates of Aspergillus were obtained, most of them belonging to A. flavus and A. niger species. Most of the A. flavus isolates were obtained from the Cabécar (fifteen isolates) and Nambí (seven isolates) common bean varieties, while A. niger was mostly isolated from the Cabécar variety (eleven isolates). In the case of peanuts, thirteen isolates were obtained, most of them identified as A. niger. No atoxigenic strains were found in peanuts, however, in common beans, five strains of A. flavus with this characteristic were found. Conclusions. The present study demonstrated the diversity of Aspergillus species that colonize the grains of common beans and peanuts in Costa Rica. Most of the species isolated are producers of mycotoxins that cause adverse effects on human health.

Downloads

Download data is not yet available.

References

Abdel-Azeem, A. M., Abdel-Azeem, M. A., Abdul-Hadi, S. Y., & Darwish, A. G. (2019). Aspergillus: Biodiversity, ecological significances, and industrial applications. In A. N. Yadav, S. Mishra, S. Singh, & A. Gupta (Eds.), Recent Advancement in White Biotechnology Through Fungi: Volume 1: Diversity and Enzymes Perspectives (pp. 121–179). Springer International Publishing. https://doi.org/10.1007/978-3-030-10480-1_4

Acuña-Gutiérrez, C., Schock, S., Jiménez, V. M., & Müller, J. (2021). Detecting fumonisin B1 in black beans (Phaseolus vulgaris L.) by near-infrared spectroscopy (NIRS). Food Control, 130, Article 108335. https://doi.org/10.1016/j.foodcont.2021.108335

Adeyeye, S. A. O. (2016). Fungal mycotoxins in foods: A review. Cogent Food & Agriculture, 2(1), Article 1213127. https://doi.org/10.1080/23311932.2016.1213127

Agbetiameh, D., Ortega-Beltran, A., Awuah, R. T., Atehnkeng, J., Islam, M.-S., Callicott, K. A., Cotty, P. J., & Bandyopadhyay, R. (2019). Potential of atoxigenic Aspergillus flavus vegetative compatibility groups associated with maize and groundnut in Ghana as biocontrol agents for aflatoxin management. Frontiers in Microbiology, 10, Article 2069. https://doi.org/10.3389/fmicb.2019.02069

Akram, N. A., Shafiq, F., & Ashraf, M. (2018). Peanut (Arachis hypogaea L.): A prospective legume crop to offer multiple health benefits under changing climate. Comprehensive Reviews in Food Science and Food Safety, 17(5), 1325–1338. https://doi.org/10.1111/1541-4337.12383

Asare Bediako, K., Ofori, K., Offei, S. K., Dzidzienyo, D., Asibuo, J. Y., & Adu Amoah, R. (2019). Aflatoxin contamination of groundnut (Arachis hypogaea L.): Predisposing factors and management interventions. Food Control, 98, 61–67. https://doi.org/10.1016/j.foodcont.2018.11.020

Bailly, S., Mahgubi, A. E., Carvajal-Campos, A., Lorber, S., Puel, O., Oswald, I. P., Bailly, J. D., & Orlando, B. (2018). Occurrence and identification of Aspergillus section Flavi in the context of the emergence of aflatoxins in French maize. Toxins, 10(12), Article 525. https://doi.org/10.3390/toxins10120525

Blair, M. W., González, L. F., Kimani, P. M., & Butare, L. (2010). Genetic diversity, inter-gene pool introgression and nutritional quality of common beans (Phaseolus vulgaris L.) from Central Africa. Theoretical and Applied Genetics, 121(2), 237–248. https://doi.org/10.1007/s00122-010-1305-x

Brandfass, C., & Karlovsky, P. (2008). Upscaled CTAB-based DNA extraction and real-time PCR assays for Fusarium culmorum and F. graminearum DNA in plant material with reduced sampling error. International Journal of Molecular Sciences, 9(11), 2306–2321. https://doi.org/10.3390/ijms9112306

Caceres, I., Al Khoury, A., El Khoury, R., Lorber, S., Oswald, I. P., El Khoury, A., Atoui, A., Puel, O., & Bailly, J. D. (2020). Aflatoxin biosynthesis and genetic regulation: A review. Toxins, 12(3), Article 150. https://doi.org/10.3390/toxins12030150

Chang, P. K., Yu, J., & Yu, J. H. (2004). AflT, a MFS transporter-encoding gene located in the aflatoxin gene cluster, does not have a significant role in aflatoxin secretion. Fungal Genetics and Biology, 41(10), 911–920. https://doi.org/10.1016/j.fgb.2004.06.007

Chávez-Servia, J., Heredia-García, E., Mayek-Pérez, N., Aquino-Bolaños, E. N., Hernández-Delgado, S., Carrillo-Rodríguez, J. C., Gill-Langarica, H. R., & Vera-Guzmán, A. M. (2016). Diversity of common bean (Phaseolus vulgaris L.) landraces and the nutritional value of their grains. In A. Kumar Goyal (Ed.), Grain legumes. IntechOpen. https://doi.org/10.5772/63439

Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2016). GenBank. Nucleic Acids Research, 44(D1), D67–D72. https://doi.org/10.1093/nar/gkv1276

Consejo Nacional de Producción. (2017, febrero 24). Uso de semilla certificada de frijol continúa ascenso. elmundo.cr. https://www.elmundo.cr/costa-rica/uso-de-semilla-certificada-de-frijol-continua-en-ascenso/

Eskola, M., Kos, G., Elliott, C. T., Hajšlová, J., Mayar, S., & Krska, R. (2020). Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%. Critical Reviews in Food Science and Nutrition, 60(16), 2773–2789. https://doi.org/10.1080/10408398.2019.1658570

Frisvad, J. C., Larsen, T. O., Thrane, U., Meijer, M., Varga, J., Samson, R. A., & Nielsen, K. F. (2011). Fumonisin and ochratoxin production in industrial Aspergillus niger strains. PLOS ONE, 6(8), Article e23496. https://doi.org/10.1371/journal.pone.0023496

Hong, S. B., Go, S. J., Shin, H. D., Frisvad, J. C., & Samson, R. A. (2005). Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia, 97(6), 1316–1329. https://doi.org/10.1080/15572536.2006.11832738

Houbraken, J., Kocsubé, S., Visagie, C. M., Yilmaz, N., Wang, X. C., Meijer, M., Kraak, B., Hubka, V., Bensch, K., Samson, R. A., & Frisvad, J. C. (2020). Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): An overview of families, genera, subgenera, sections, series and species. Studies in Mycology, 95, 5–169. https://doi.org/10.1016/j.simyco.2020.05.002

Instituto Meteorológico Nacional. (s.f.). Pronóstico del tiempo por regiones. Datos climáticos. Recuperado el 8 de agosto, 2022 de https://www.imn.ac.cr/es/web/imn/mapa#A5280:form:panelInfo

Jayaprakash, A., Thanmalagan, R. R., Roy, A., Arunachalam, A., & Lakshmi, P. (2019). Strategies to understand Aspergillus flavus resistance mechanism in Arachis hypogaea L. Current Plant Biology, 20, Article 100123. https://doi.org/10.1016/j.cpb.2019.100123

Katsurayama, A. M., Martins, L. M., Iamanaka, B. T., Fungaro, M. H. P., Silva, J. J., Frisvad, J. C., Pitt, J. I., & Taniwaki, M. H. (2018). Occurrence of Aspergillus section Flavi and aflatoxins in Brazilian rice: From field to market. International Journal of Food Microbiology, 266, 213–221. https://doi.org/10.1016/j.ijfoodmicro.2017.12.008

Khan, R., Ghazali, F. M., Mahyudin, N. A., & Samsudin, N. I. P. (2021). Aflatoxin biosynthesis, genetic regulation, toxicity, and control strategies: A review. Journal of Fungi, 7(8), Article 606. https://doi.org/10.3390/jof7080606

Klich, M. A. (2002). Identification of common Aspergillus species (1st ed.). Centraalbureau Voor Schimmelcultures.

Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096

Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual (1st ed.). John Wiley & Sons.

López Sedo, V. (2017, marzo 1). Una variedad de frijol resistente al cambio climático llega a Costa Rica. Ojo al Clima. https://ojoalclima.com/cientificos-ucr-participan-creacion-variedad-frijol-resistente-al-cambio-climatico/

Marchese, S., Polo, A., Ariano, A., Velotto, S., Costantini, S., & Severino, L. (2018). Aflatoxin B1 and M1: Biological properties and their involvement in cancer development. Toxins, 10(6), Article 214. https://doi.org/10.3390/toxins10060214

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. https://doi.org/10.5897/AJMR12.2078

Moretti, A., & Susca, A. (Eds.). (2017). Mycotoxigenic fungi: Methods and protocols (Vol. 1542). Springer New York. https://doi.org/10.1007/978-1-4939-6707-0

Omotayo, O. P., Omotayo, A. O., Mwanza, M., & Babalola, O. O. (2019). Prevalence of mycotoxins and their consequences on human health. Toxicological Research, 35(1), 1–7. https://doi.org/10.5487/TR.2019.35.1.001

Ostry, V., Malir, F., Toman, J., & Grosse, Y. (2017). Mycotoxins as human carcinogens-the IARC Monographs classification. Mycotoxin Research, 33, 65–73. https://doi.org/10.1007/s12550-016-0265-7

Palencia, E. R., Hinton, D. M., & Bacon, C. W. (2010). The black Aspergillus species of maize and peanuts and their potential for mycotoxin production. Toxins, 2(4), 399–416. https://doi.org/10.3390/toxins2040399

Perrone, G., & Gallo, A. (2017). Aspergillus species and their associated mycotoxins. In A. Moretti, & A. Susca (Eds.), Mycotoxigenic fungi: Methods and protocols (pp. 33–49). Springer. https://doi.org/10.1007/978-1-4939-6707-0_3

Rao, K. R., Vipin, A. V., & Venkateswaran, G. (2020). Molecular profile of non-aflatoxigenic phenotype in native strains of Aspergillus flavus. Archives of Microbiology, 202(5), 1143–1155. https://doi.org/10.1007/s00203-020-01822-1

Rawal, V., & Navarro, D. K. (2019). The global economy of pulses. Food and Agriculture Organization. https://doi.org/10.4060/I7108EN

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

Santos-Ciscon, B. A., van Diepeningen, A., Machado, J. da C., Dias, I. E., & Waalwijk, C. (2019). Aspergillus species from Brazilian dry beans and their toxigenic potential. International Journal of Food Microbiology, 292, 91–100. https://doi.org/10.1016/j.ijfoodmicro.2018.12.006

Sinkovič, L., Pipan, B., Sinkovič, E., & Meglič, V. (2019). Morphological seed characterization of common (Phaseolus vulgaris L.) and runner (Phaseolus coccineus L.) bean germplasm: A Slovenian gene bank example. BioMed Research International, 2019, Article e6376948. https://doi.org/10.1155/2019/6376948

Somma, S., Perrone, G., & Logrieco, A. F. (2012). Diversity of black Aspergini and mycotoxin risks in grape, wine and dried vine fruits. Phytopathologia Mediterranea, 51(1), 131–147.

Srour, A. Y., Fakhoury, A. M., & Brown, R. L. (2017). Targeting aflatoxin biosynthetic genes. In A. Moretti, & A. Susca (Eds.), Mycotoxigenic fungi: Methods and protocols (pp. 159–171). Springer. https://doi.org/10.1007/978-1-4939-6707-0_10

Stalker, H. T. (1997). Peanut (Arachis hypogaea L.). Field Crops Research, 53(1), 205–217. https://doi.org/10.1016/S0378-4290(97)00032-4

Streit, E., Naehrer, K., Rodrigues, I., & Schatzmayr, G. (2013). Mycotoxin occurrence in feed and feed raw materials worldwide: Long-term analysis with special focus on Europe and Asia. Journal of the Science of Food and Agriculture, 93(12), 2892–2899. https://doi.org/10.1002/jsfa.6225

Telles, A. C., Kupski, L., & Furlong, E. B. (2017). Phenolic compound in beans as protection against mycotoxins. Food Chemistry, 214, 293–299. https://doi.org/10.1016/j.foodchem.2016.07.079

Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673–4680. https://doi.org/10.1093/nar/22.22.4673

Toffa, D. D., Mahnine, N., Ouaffak, L., El Abidi, A., El Alaoui Faris, F. Z., & Zinedine, A. (2013). First survey on the presence of ochratoxin A and fungi in raw cereals and peanut available in the Republic of Niger. Food Control, 32(2), 558–562. https://doi.org/10.1016/j.foodcont.2013.01.028

Wei, D., Zhou, L., Selvaraj, J. N., Zhang, C., Xing, F., Zhao, Y., Wang, Y., & Liu, Y. (2014). Molecular characterization of atoxigenic Aspergillus flavus isolates collected in China. Journal of Microbiology, 52(7), 559–565. https://doi.org/10.1007/s12275-014-3629-8

Yin, G., Hua, S. S. T., Pennerman, K. K., Yu, J., Bu, L., Sayre, R. T., & Bennett, J. W. (2018). Genome sequence and comparative analyses of atoxigenic Aspergillus flavus WRRL 1519. Mycologia, 110(3), 482–493. https://doi.org/10.1080/00275514.2018.1468201

Published

2022-09-06

How to Cite

Carranza-Mesén, F., Blanco-Meneses, M., Granados-Montero, M. del M., & Vinas Meneses, M. (2022). Aspergillus species associated with grains of groundnuts (Arachis hypogaea L.) and common beans (Phaseolus vulgaris L.) cultivated in Costa Rica. Agronomía Mesoamericana, 33(Especial), 50810. https://doi.org/10.15517/am.v33iEspecial.50810