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Bacillus licheniformis M2-7 Decreases Ochratoxin A Concentrations in Coffee Beans During Storage

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Abstract

Microbial contamination of coffee beans arises from various factors such as harvesting, handling, and storage practices, during which ochratoxin A (OTA)-producing fungi develop and proliferate. The presence of elevated concentrations of OTA poses a serious health risk to coffee consumers. Therefore, the implementation of a post-harvest treatment involving the use of bacteria known to antagonize OTA-producing fungi constitutes a safe alternative for reducing or eliminating the toxin’s concentration in coffee beans. In this study, coffee beans (Coffea arabica L.) were inoculated with Bacillus licheniformis M2-7, after which we monitored fungal growth, in vitro antagonism, and OTA concentration. Our findings demonstrated that coffee beans inoculated with this bacterial strain exhibited a significant decrease in fungal populations belonging to the genera Aspergillus and Penicillium, which are known to produce OTA. Moreover, strain M2-7 decreased the growth rates of these fungi from 67.8% to 95.5% (P < 0.05). Similarly, inoculation with B. licheniformis strain M2-7 effectively reduced the OTA concentration from 24.35 ± 1.61 to 5.52 ± 1.69 µg/kg (P < 0.05) in stored coffee beans. These findings suggest that B. licheniformis M2-7 holds promise as a potential post-harvest treatment for coffee beans in storage, as it effectively inhibits the proliferation of OTA-producing fungi and lowers the toxin’s concentration.

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References

  1. Mondani L, Palumbo R, Tsitsigiannis D, Perdikis D, Mazzoni E, Battilani P (2020) Pest management and ochratoxin A contamination in grapes: a review. Toxins 12(5):303. https://doi.org/10.3390/toxins12050303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Chen Y, Chen J, Zhu Q, Wan J (2022) Ochratoxin A in dry-cured ham: OTA-producing fungi, prevalence, detection methods, and biocontrol strategies—a review. Toxins 14(10):693. https://doi.org/10.3390/toxins14100693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Ganesan R, Mohan K, Karthick D, Pillay A, Palanisami T, Sathishkumar P, Conterno L (2022) Distribution, toxicity, interactive effects, and detection of ochratoxin and deoxynivalenol in food: a review. Food Chem 378:131978. https://doi.org/10.1016/j.foodchem.2021.131978

    Article  PubMed  CAS  Google Scholar 

  4. Van der Stegen H, Essens J, van der Lijn J (2001) Effect of roasting conditions on reduction of ochratoxin A in coffee. J Agric Food Chem 49(10):4713–4715. https://doi.org/10.1021/jf0105586

    Article  PubMed  CAS  Google Scholar 

  5. Liu C, Pushparaj K, Meyyazhagan A, Arumugam A, Pappuswamy M, Bhotla K, Baskaran R, Issara U, Balasubramanian B, Mousavi A (2022) Ochratoxin A as an alarming health threat for livestock and human: a review on molecular interactions, mechanism of toxicity, detection, detoxification, and dietary prophylaxis. Toxicon 213:59–75. https://doi.org/10.1016/j.toxicon.2022.04.012

    Article  PubMed  CAS  Google Scholar 

  6. Zhai Y, Feng M, Wang W, Yang L, Yang Y (2021) Ochratoxin A: its impact on poultry gut health and microbiota, an overview. Poultry Sci 100:101037. https://doi.org/10.1016/j.psj.2021.101037

    Article  CAS  Google Scholar 

  7. Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. http://data.europa.eu/eli/reg/2006/1881/oj. Accessed 1 Jan 2023

  8. Leitão L (2019) Occurrence of ochratoxin A in coffee: threads and solutions—a mini review. Beverages 5(2):36. https://doi.org/10.3390/beverages5020036

    Article  CAS  Google Scholar 

  9. IARC (2016) Agents classified by the IARC Monographs, vols 1–116. http://monographs.iarc.fr/ENG/Classification/. Accessed 25 Oct 2016

  10. De Melo P, Beux M, Pagnoncelli G, Soccol T, Rodrigues C, Soccol R (2016) Isolation, selection and evaluation of antagonistic yeasts and lactic acid bacteria against ochratoxigenic fungus Aspergillus westerdijkiae on coffee beans. Lett Appl Microbiol 62(1):96–101. https://doi.org/10.1111/lam.12520

    Article  CAS  Google Scholar 

  11. Peromingo B, Núñez F, Rodríguez A, Alía A, Andrade J (2018) Potential of yeasts isolated from dry-cured ham to control ochratoxin A production in meat models. Int J Food Microbiol 268:73–80. https://doi.org/10.1016/j.ijfoodmicro.2018.01.006

    Article  PubMed  CAS  Google Scholar 

  12. Ragoubi C, Quintieri L, Greco D, Mehrez A, Maatouk I, D’Ascanio V, Landoulsi A, Avantaggiato G (2021) Mycotoxin removal by Lactobacillus spp. and their application in animal liquid feed. Toxins 13(3):185. https://doi.org/10.3390/toxins13030185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Nievierowski H, Veras F, Silveira D, Giocastro B, Aloisi I, Tranchida Q, Dugo P, Brandelli A, Zini A, Welke E (2023) A Bacillus-based biofungicide agent prevents ochratoxins occurrence in grapes and impacts the volatile profile throughout the Chardonnay winemaking stages. Int J Food Microbiol 389:110107. https://doi.org/10.1016/j.ijfoodmicro.2023.110107

    Article  PubMed  CAS  Google Scholar 

  14. Das K, Prasanna R, Saxena K (2017) Rhizobia: a potential biocontrol agent for soilborne fungal pathogens. Folia Microbiol 62(5):425–435. https://doi.org/10.1007/s12223-017-0513-z

    Article  CAS  Google Scholar 

  15. Albarrán-de la Luz L, Rodríguez-Barrera MA, Hernández-Flores G, Lopezaraiza M, Alemán L, Toribio-Jiménez J, Romero-Ramírez Y (2022) Antagonismo of Bacillus licheniformis M2-7 against phytopathogen fungi of Mangifera indica L. Rev Int Contam Ambie 38:1–10. https://doi.org/10.20937/RICA.54217

    Article  Google Scholar 

  16. Bahena-Oregón R, Rodríguez-Barrera MA, Rosas-Guerrero V, Méndez-Bahena A, Toledo-Hernández E, Toribio-Jiménez J, Návez-González D, Palemón-Alberto F, Ortega-Acosta SA, Romero-Ramírez Y (2022) Bacillus licheniformis M2-7 inhibits the growth and affects the structure of phytopathogenic fungi of Zea mays. In: Sotelo-Navarro PX, Tecorralco-Bobadilla AL, Escamilla-Alvarado C, Hernández-Flores G, Nava-Bravo I, López-Díaz JA, Poggi-Varaldo HM (eds) Ambiente y Bioenergía. Perspectivas y avances de la sostenibilidad. ABIAERA C, México City, México, pp 500–508

    Google Scholar 

  17. Guavara J, Serrano I, Rodríguez M, Hernández G, Toribio J, Toledo E, Romero Y (2022) Isolated bacteria from hot springs able to use hydrocarbons as carbon source. Rev Int Contam Ambient 38:68–77. https://doi.org/10.20937/RICA.54234

    Article  Google Scholar 

  18. Luna Y, Trigos Á (2010) Aislamiento de cepas de Aspergillus niger, productoras de ocratoxina A, en café verde (Coffea arábica) almacenado. Rev Mex Micol 32:63–68

    Google Scholar 

  19. Riddell W (1950) Permanent stained mycological preparations obtained by slide culture. Mycologic 42:265–270. https://doi.org/10.2307/3755439

    Article  Google Scholar 

  20. Barnett L, Hunter B (1998) Illustrated genera of imperfect fungi, 4th edn. APS Press, The American Phytopathological Society, St Paul, MN, p 218

    Google Scholar 

  21. Sanger F, Nicklen S, Coulson AR (1977) Sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467. https://doi.org/10.1073/pnas.74.12.5463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Sievers F, Higgins DG (2018) Clustal Omega for making accurate alignments of many protein sequences. Protein Sci 27:135–145

    Article  PubMed  CAS  Google Scholar 

  23. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Rapp BA, Wheeler DL (2000) GenBank. Nucleic Acids Res 28(1):15–18. https://doi.org/10.1093/nar/28.1.15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37(5):1530–1534. https://doi.org/10.1093/molbev/msaa015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  26. Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285

    PubMed  CAS  Google Scholar 

  27. Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylo-genetic tree display and annotation. Nucleic Acids Res 49:W293–W296. https://doi.org/10.1093/nar/gkab301

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Tejera M, Rojas M (2012) Antagonismo de Bacillus spp. frente a hongos fitopatógenos del cultivo del arroz (Oryza sativa L.). Rev Prot Veg 27(2):117–122

    Google Scholar 

  29. Estrada B, Salazar R, Ramirez M, Moreno JJ, Romero Y, González M, Alvarez P (2022) Influence of water activity on physical properties, fungal growth, and ochratoxin A production in dry cherries and green-coffee beans. J Food Process Preserv 46:16226. https://doi.org/10.1111/jfpp.16226

    Article  CAS  Google Scholar 

  30. Pleadin J, Frece J, Markov K (2019) Mycotoxins in food and feed. Adv Food Nutr Res 89:297–345. https://doi.org/10.1016/bs.afnr.2019.02.007

    Article  PubMed  CAS  Google Scholar 

  31. Mota L, Guadarrama S, Salas R, Escalante A, Montville Valadez R (2019) Adaptación de Bacillus licheniformis a Melazas para la Producción Mejorada de una Cepa Biofertilizante. Agrociencia 53(8):1183–1201

    Google Scholar 

  32. Ossa A, Vanegas C, Badillo M (2010) Evaluación de la melaza de caña como sustrato para el crecimiento de Lactobacillus plantarum. Rev UDCA Act Div Cient 13(1):97–104

    Google Scholar 

  33. Cotty J, Jaime R (2007) Influences of climate on aflatoxin producing fungi and aflatoxin contamination. Int J Food Microbiol 119(1–2):109–115. https://doi.org/10.1016/j.ijfoodmicro.2007.07.060

    Article  PubMed  CAS  Google Scholar 

  34. Hu L, Van J, Gruben S, Wösten B, Gu JD, De Vries P (2011) Improved enzyme production by co-cultivation of Aspergillus and Aspergillus oryzae and with other fungi. Int Biodeterior Biodegrad 65:248–252. https://doi.org/10.1016/j.ibiod.2010.11.008

    Article  CAS  Google Scholar 

  35. Morales Y, Hernández J, Ramos G, Pérez R, Muñoz R, Muñoz J (2016) Cuantificación de Penicillium sp. por el método de goteo en placa. Rev Iberoam Cienc 3(2):13–19

    Google Scholar 

  36. Castro O, Kenneth Ramirez A, Blanco MM (2018) Morphological and molecular characterization of Fusarium oxysporum f. sp. Apii associated with celery wilt in Costa Rica. Costa Rican Agron 42(1):115–126. https://doi.org/10.15517/rac.v42i1.32199

    Article  Google Scholar 

  37. Requena S, Morales P, Gómez S, Boga A, Peláez T (2020) Micosis cutánea por Curvularia pallescens en un paciente trasplantado pulmonar: primer caso descrito en España. Rev Iberoam Micol 37(2):58–62. https://doi.org/10.1016/j.riam.2020.03.005

    Article  Google Scholar 

  38. Álvarez P, Ramírez R, López L, Moreno MaE (2016) Micotoxinas en Guerrero: presencia de Ocratoxina A en granos de café de Atoyac de Álvarez. Rev Simul Lab 2:12–16 (ISSN: 2410-3462)

    Google Scholar 

  39. Perrone G, Susca A (2017) Penicillium species and their associated mycotoxins. Methods Mol Biol (Clifton, NJ) 1542:107–119. https://doi.org/10.1007/978-1-4939-6707-0_5

    Article  CAS  Google Scholar 

  40. Wang L, Zhuang WY (2007) Phylogenetic analyses of penicillia based on partial calmodulin gene sequences. Biosystems 88:113–126. https://doi.org/10.1016/j.biosystems.2006.04.008

    Article  PubMed  CAS  Google Scholar 

  41. Pierzgalski A, Bryła M, Kanabus J, Modrzewska M, Podolska G (2021) Updated review of the toxicity of selected fusarium toxins and their modified forms. Toxins 13(11):768. https://doi.org/10.3390/toxins13110768

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Wang S, Lu Z, Lang B, Wang X, Li Y, Chen J (2022) Curvularia lunata and Curvularia leaf spot of maize in China. ACS Omega 7(51):47462–47470. https://doi.org/10.1021/acsomega.2c03013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Khruengsai S, Pripdeevech P, Tanapichatsakul C, Srisuwannapa C, D’Souza E, Panuwet P (2021) Antifungal properties of volatile organic compounds produced by Daldinia eschscholtzii MFLUCC 19-0493 isolated from Barleria prionitis leaves against Colletotrichum acutatum and its post-harvest infections on strawberry fruits. PeerJ 9:e11242. https://doi.org/10.7717/peerj.11242

    Article  PubMed  PubMed Central  Google Scholar 

  44. Bressani P, Martínez J, Sarmento B, Borém M, Schwan F (2020) Organic acids produced during fermentation and sensory perception in specialty coffee using yeast starter culture. Food Res Int 128:108773. https://doi.org/10.1016/j.foodres.2019.108773

    Article  PubMed  CAS  Google Scholar 

  45. Rojas-Pablo M, Romero-Ramírez Y (2022) El Café te Mejora la Vida, pero sin Ocratoxina. Bol SCME 2(4):80–87

    Google Scholar 

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Acknowledgements

This work was supported by grants 1056878 from CONACyT. Maria Rojas Pablo thanks CONACyT for PhD scholarships.

Funding

This work was supported by grants 1056878 from CONACyT.

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All authors contributed to the study conception and design. Investigation and Methodology: MR-P, AB-D and PÁ-F, Data curation: ET-H, Formal Analysis: VMR-G, Supervision: CT-R and SAS-S. The first draft of the manuscript was written by MAR-B and JT-J and Writing—review and editing: YR-R.

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Correspondence to Yanet Romero-Ramírez.

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Rojas-Pablo, M., Toledo-Hernández, E., Rodríguez-Barrera, M.A. et al. Bacillus licheniformis M2-7 Decreases Ochratoxin A Concentrations in Coffee Beans During Storage. Curr Microbiol 81, 62 (2024). https://doi.org/10.1007/s00284-023-03575-8

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