Elucidating the contribution of microorganisms to the spontaneous fermentation and the quality of Ivorian cacao (Theobroma cacao) beans: The quality of Ivorian cacao (Theobroma cacao) beans
Main Article Content
Keywords
cacao beans, spontaneous fermentation, microorganisms, aroma precursors
Abstract
Cacao (Theobroma cacao) beans are among the most important ingredients in food and beverage industries. They are mainly produced in tropical and subtropical forests. Africa is the biggest producer of cacao bean providers in the world and the Ivory Coast remains the world leader with an estimated yearly production of 3 million tonnes. Cacao beans are used in many food items such as chocolate products, cocoa butter, confectionary products, iced drinks, cocoa powder, etc. The quality and organoleptic characteristics of these food products are strongly related to those of the cocoa beans obtained from different processing treatments. The pulps surrounding the cacao beans are rich in water, sugars, pectins, proteins, minerals, vitamins, citric acid, and phenolic compounds. Many different processing methods are utilized and fermentation is a crucial postharvest treatment having a great influence on the quality of cacao beans and their related products. Spontaneous fermentation is a common practice carried out by the cacao farmers in Ivory Coast. The microorganisms involved in this process are primarily the yeasts (anaerobic phase), which convert the pulps containing sugars into alcohol with a sporicidal temperature increase and then the lactic and acetic acid bacteria (aerobic phase) that produce lactic and acetic acids, respectively. The degradation of the substrates inside the cacao pulps results in the generation of aroma precursors and compounds. The goal of this review was to elucidate the factors affecting the spontaneous fermentation of Ivorian cacao beans and clarify the transformation of the raw material during fermentation.
References
Afoakwa, E.O., Paterson, A., Fowler, M. and Vieira, J., 2009b. Comparison of rheological models for determining dark chocolate viscosity. International Journal of Food Science and Technology 44(1): 162–167. 10.1111/j.1365-2621.2008.01710.x
Afoakwa, E.O., Quao, J., Budu, A.S., Takrama, J. and Saalia, F.K., 2011. Effect of pulp preconditioning on acidification, proteolysis, sugars and free fatty acids concentration during fermentation of cocoa (Theobroma cacao) beans. International Journal of Food Sciences and Nutrition 62(7): 755–764. 10.3109/09637486.2011.581224
Ardhana, M.M. and Fleet, G.H., 2003. The microbial ecology of cocoa bean fermentations in Indonesia. International Journal of Food Microbiology 86(1–2): 87–99. 10.1016/S0168-1605(03)00081-3
Aydin, S., Ilgaz, C. and Kadiroglu, P., 2021. Prediction of quality properties of carob fruit with FT-IR spectroscopy. Journal of Raw Materials to Processed Foods 2: 24–32.
Beckett, S., 2009. Chocolate manufacture.Ch.2. In: Talbot, G. (ed.), Science and technology of enrobed and filled chocolate, confectionery and bakery products. Woodhead Publishing, CRC Press, Cambridge, pp. 11–28.
Beg, M.S., Ahmad, S., Jan, K. and Bashir, K., 2017. Status, supply chain and processing of cocoa—a review. Trends in Food Science and Technology 66: 108–116. 10.1016/j.tifs.2017.06.007
Binh, P.T., Tru, N.V., Dung, V.T., Thoa, N.T. and Thao, P., 2017. Bacteria in wooden box fermentation of cocoa in Daklak, Vietnam. Journal of Microbiology and Experimentation 5(7): 176. 10.15406/jmen.2017.05.00176
Bonetti, F., Brombo, G. and Zuliani, G., 2017. Nootropics, functional foods, and dietary patterns for prevention of cognitive decline. In: Watson, R.R. (ed.), Nutrition and functional foods for healthy aging. Academic Press, Elsevier, London, pp. 211–232.
Camu, N., González, A., De Winter, T., Van Schoor, A., De Bruyne, K., Vandamme, P., Takrama, J.S., Addo, S.K. and De Vuyst, L., 2008. Influence of turning and environmental contamination on the dynamics of populations of lactic acid and acetic acid bacteria involved in spontaneous cocoa bean heap fermentation in Ghana. Applied and Environmental Microbiology 74(1): 86–98. 10.1128/AEM.01512-07
Crafack, M., Mikkelsen, M.B., Saerens, S., Knudsen, M., Blennow, A., Lowor, S., Takrama, J., Swiegers, J.H., Petersen, G.B. and Heimdal, H., 2013. Influencing cocoa flavour using Pichia kluyveri and Kluyveromyces marxianus in a defined mixed starter culture for cocoa fermentation. International Journal of Food Microbiology 167(1): 103–116. 10.1016/j.ijfoodmicro.2013.06.024
D’Souza, R.N., Grimbs, A., Grimbs, S., Behrends, B., Corno, M., Ullrich, M.S. and Kuhnert, N., 2018. Degradation of cocoa proteins into oligopeptides during spontaneous fermentation of cocoa beans. Food Research International 109: 506-516. 10.1016/j.foodres.2018.04.068
da Veiga Moreira, I.M., Miguel, M.G.D.C.P., Duarte, W.F., Dias, D.R. and Schwan, R.F., 2013. Microbial succession and the dynamics of metabolites and sugars during the fermentation of three different cocoa (Theobroma cacao L.) hybrids. Food Research International 54(1): 9–17. 10.1016/j.foodres.2013.06.001
Daniel, H.-M., Vrancken, G., Takrama, J.F., Camu, N., De Vos, P. and De Vuyst, L., 2009. Yeast diversity of Ghanaian cocoa bean heap fermentations. FEMS Yeast Research 9(5): 774–783. 10.1111/j.1567-1364.2009.00520.x
De Bruyne, K., Camu, N., De Vuyst, L. and Vandamme, P., 2010. Weissella fabaria sp. nov., from a Ghanaian cocoa fermentation. International Journal of Systematic and Evolutionary Microbiology 60(9): 1999–2005. 10.1099/ijs.0.019323-0
de Melo Pereira, G.V., Magalhães, K.T., de Almeida, E.G., da Silva Coelho, I. and Schwan, R.F., 2013. Spontaneous cocoa bean fermentation carried out in a novel-design stainless steel tank: influence on the dynamics of microbial populations and physical–chemical properties. International Journal of Food Microbiology 161(2): 121–133. 10.1016/j.ijfoodmicro.2012.11.018
De Vuyst, L. and Weckx, S., 2016. The cocoa bean fermentation process: from ecosystem analysis to starter culture development. Journal of Applied Microbiology 121(1): 5–17. 10.1111/jam.13045
Elwers, S., Zambrano, A., Rohsius, C. and Lieberei, R., 2009. Differences between the content of phenolic compounds in Criollo, Forastero and Trinitario cocoa seed (Theobroma cacao L.). European Food Research and Technology 229(6): 937–948. 10.1007/s00217-009-1132-y
FAO (Food and Agriculture Organization of the United Nations), 2022. FAOSTAT database. Available at: http://www.fao.org/faostat/en/#data/RP (accessed on 15.05.2022).
Gálvez, S.L., Loiseau, G., Paredes, J.L., Barel, M. and Guiraud, J.-P., 2007. Study on the microflora and biochemistry of cocoa fermentation in the Dominican Republic. . International Journal of Food Microbiology 114(1): 124–130. 10.1016/j.ijfoodmicro.2006.10.041
Guehi, T.S., Konan, Y.M., Koffi-Nevry, R., N’dri, D.Y. and Manizan, N.P., 2007. Enumeration and identification of main fungal isolates and evaluation of fermentation’s degree of Ivorian raw cocoa beans. Australian Journal of Basic and Applied Sciences 1(4): 479–486. 10.1111/j.1365-2621.2010.02302.x
Guehi, T.S., Zahouli, I.B., Ban-Koffi, L., Fae, M.A. and Nemlin, J.G., 2010. Performance of different drying methods and their effects on the chemical quality attributes of raw cocoa material. Int J. Food Sci. Technol 45(8): 1564–1571.
Hamdouche, Y., Guehi, T., Durand, N., Kedjebo, K.B.D., Montet, D. and Meile, J.C., 2015. Dynamics of microbial ecology during cocoa fermentation and drying: towards the identification of molecular markers. Food Control 48: 117–122. 10.1016/j.foodcont.2014.05.031
Hamdouche, Y., Meile, J.C., Lebrun, M., Guehi, T., Boulanger, R., Teyssier, C. and Montet, D., 2019. Impact of turning, pod storage and fermentation time on microbial ecology and volatile composition of cocoa beans. Food Research International 119: 477–491. 10.1016/j.foodres.2019.01.001
Illeghems, K., De Vuyst, L., Papalexandratou, Z. and Weckx, S., 2012. Phylogenetic analysis of a spontaneous cocoa bean fermentation metagenome reveals new insights into its bacterial and fungal community diversity. PLoS One 7(5): 38040. 10.1371/journal.pone.0038040
Janek, K., Niewienda, A., Wöstemeyer, J. and Voigt, J., 2016. The cleavage specificity of the aspartic protease of cocoa beans involved in the generation of the cocoa-specific aroma precursors. Food Chemistry 211: 320–328. 10.1016/j.foodchem.2016.05.033
Jespersen, L., Nielsen, D.S., Hønholt, S. and Jakobsen, M., 2005. Occurrence and diversity of yeasts involved in fermentation of West African cocoa beans. FEMS Yeast Research 5(4–5): 441–453. 10.1016/j.femsyr.2004.11.002
Jinap, S., Dimick, P. and Hollender, R., 1995. Flavour evaluation of chocolate formulated from cocoa beans from different countries. Food Control 6(2): 105–110. 10.1016/0956-7135(95)98914-M
Kone, K., Akueson, K. and Norval, G., 2020. On the production of potassium carbonate from cocoa pod husks. Recycling 5(3): 23. 10.3390/recycling5030023
Koné, M.K., Guéhi, S.T., Durand, N., Ban-Koffi, L., Berthiot, L., Tachon, A.F., Brou, K., Boulanger, R. and Montet, D., 2016. Contribution of predominant yeasts to the occurrence of aroma compounds during cocoa bean fermentation. Food Research International 89: 910–917. 10.1016/j.foodres.2016.04.010
Kongor, J.E., Hinneh, M., Van de Walle, D., Afoakwa, E.O., Boeckx, P. and Dewettinck, K., 2016. Factors influencing quality variation in cocoa (Theobroma cacao) bean flavour profile— a review. Food Research International 82: 44–52. 10.1016/j.foodres.2016.01.012
Kostinek, M., Ban-Koffi, L., Ottah-Atikpo, M., Teniola, D., Schillinger, U., Holzapfel, W.H., and Franz, C.M., 2008. Diversity of predominant lactic acid bacteria associated with cocoa fermentation in Nigeria. Current Microbiology, 56(4): 306–314. 10.1007/s00284-008-9097-9
Kratzer, U., Frank, R., Kalbacher, H., Biehl, B., Wöstemeyer, J. and Voigt, J., 2009. Subunit structure of the vicilin-like globular storage protein of cocoa seeds and the origin of cocoa-and chocolate-specific aroma precursors. Food Chemistry 113(4):903–913. 10.1016/j.foodchem.2008.08.017
Lefeber, T., Janssens, M., Camu, N. and De Vuyst, L., 2010. Kinetic analysis of strains of lactic acid bacteria and acetic acid bacteria in cocoa pulp simulation media toward development of a starter culture for cocoa bean fermentation. Applied and Environmental Microbiology 76(23): 7708–7716. 10.1128/AEM.01206-10
Lefeber, T., Janssens, M., Moens, F., Gobert, W. and De Vuyst, L., 2011. Interesting starter culture strains for controlled cocoa bean fermentation revealed by simulated cocoa pulp fermentations of cocoa-specific lactic acid bacteria. Applied and Environmental Microbiology 77(18): 6694–6698. 10.1128/AEM.00594-11
Lima, L.J., Almeida, M.H., Nout, M.R. and Zwietering, M.H., 2011. Theobroma cacao L., “The food of the Gods”: quality determinants of commercial cocoa beans, with particular reference to the impact of fermentation. Critical Reviews in Food Science and Nutrition 51(8): 731–761. 10.1080/10408391003799913
Meersman, E., Steensels, J., Mathawan, M., Wittocx, P.-J., Saels, V., Struyf, N., Bernaert, H., Vrancken, G. and Verstrepen, K.J., 2013. Detailed analysis of the microbial population in Malaysian spontaneous cocoa pulp fermentations reveals a core and variable microbiota. PLoS One 8(12): 81559. 10.1371/journal.pone.0081559
Miguel, M.G.D.C.P., de Castro Reis, L.V., Efraim, P., Santos, C., Lima, N. and Schwan, R.F., 2017. Cocoa fermentation: microbial identification by MALDI-TOF MS and sensory evaluation of produced chocolate. LWT 77: 362–369. 10.1016/j.lwt.2016.11.076
Misnawi, J., Jinap, S., Jamilah, B. and Nazamid, S., 2003. Effects of incubation and polyphenol oxidase enrichment on colour, fermentation index, procyanidins and astringency of unfermented and partly fermented cocoa beans. International Journal of Food Science and Technology 38(3): 285–295. 10.1046/j.1365-2621.2003.00674.x
Mota-Gutierrez, J., Botta, C., Ferrocino, I., Giordano, M., Bertolino, M., Dolci, P., Cannoni, M. and Cocolin, L., 2018. Dynamics and biodiversity of bacterial and yeast communities during fermentation of cocoa beans. Applied and Environmental Microbiology 84(19): e01164–01118. 10.1128/AEM.01164-18
Ostovar, K. and Keeney, P., 1973. Isolation and characterization of microorganisms involved in the fermentation of Trinidad’s cacao beans. Journal of Food Science 38(4): 611–617. 10.1111/j.1365-2621.1973.tb02826.x
Ouattara, H.D., Ouattara, H.G., Droux, M., Reverchon, S., Nasser, W. and Niamke, S.L., 2017. Lactic acid bacteria involved in cocoa beans fermentation from Ivory Coast: species diversity and citrate lyase production. International Journal of Food Microbiology 256: 11–19. 10.1016/j.ijfoodmicro.2017.05.008
Ouattara, H.G. and Niamké, S.L., 2021. Mapping the functional and strain diversity of the main microbiota involved in cocoa fermentation from Cote d’Ivoire. Food Microbiology 98: 103767. 10.1016/j.fm.2021.103767
Ouattara, H.G., Reverchon, S., Niamke, S.L. and Nasser, W., 2010. Biochemical properties of pectate lyases produced by three different Bacillus strains isolated from fermenting cocoa beans and characterization of their cloned genes. Applied and Environmental Microbiology 76(15): 5214–5220. 10.1128/AEM.00705-10
Papalexandratou, Z., Cleenwerck, I., De Vos, P. and De Vuyst, L., 2009. (GTG) 5-PCR reference framework for acetic acid bacteria. FEMS Microbiology Letters 301(1): 44–49. 10.1111/j.1574-6968.2009.01792.x
Papalexandratou, Z., Falony, G., Romanens, E., Jimenez, J.C., Amores, F., Daniel, H.-M. and De Vuyst, L., 2011. Species diversity, community dynamics, and metabolite kinetics of the microbiota associated with traditional Ecuadorian spontaneous cocoa bean fermentations. Applied and Environmental Microbiology 77(21): 7698–7714. 10.1128/AEM.05523-11
Pereira, G.V.D.M., Miguel, M.G.D.C.P., Ramos, C.L. and Schwan, R.F., 2012. Microbiological and physicochemical characterization of small-scale cocoa fermentations and screening of yeast and bacterial strains to develop a defined starter culture. Applied and Environmental Microbiology 78(15): 5395–5405. 10.1128/AEM.01144-12
Polat, S., Guclu, G., Kelebek, H., Keskin, M. and Selli, S., 2021. Comparative elucidation of colour, volatile and phenolic profiles of black carrot (Daucus carota L.) pomace and powders prepared by five different drying methods. Food Chemistry 369: 130941. 10.1016/j.foodchem.2021.130941
Powis, T.G., Cyphers, A., Gaikwad, N.W., Grivetti, L. and Cheong, K., 2011. Cacao use and the San Lorenzo Olmec. Proceedings of the National Academy of Sciences 108(21): 8595–8600. 10.1073/pnas.1100620108
Rodriguez-Campos, J., Escalona-Buendía, H., Orozco-Avila, I., Lugo-Cervantes, E. and Jaramillo-Flores, M.E., 2011. Dynamics of volatile and non-volatile compounds in cocoa (Theobroma cacao L.) during fermentation and drying processes using principal components analysis. Food Research International 44(1): 250–258. 10.1016/j.foodres.2010.10.028
Rusconi, M. and Conti, A., 2010. Theobroma cacao L., the food of the gods: a scientific approach beyond myths and claims. Pharma-cological Research 61(1): 5–13. 10.1016/j.phrs.2009.08.008
Saltini, R., Akkerman, R. and Frosch, S., 2013. Optimizing chocolate production through traceability: a review of the influence of farming practices on cocoa bean quality. Food Control 29(1): 167–187. 10.1016/j.foodcont.2012.05.054
Samagaci, L., Ouattara, H.G., Goualié, B.G. and Niamke, S.L., 2014. Growth capacity of yeasts potential starter strains under cocoa fermentation stress conditions in Ivory Coast. Emirates Journal of Food and Agriculture 26(10): 861–870. 10.9755/ejfa.v26i10.18114
Schwan, R.F., 1998. Cocoa fermentations conducted with a defined microbial cocktail inoculum. Applied and Environ-mental Microbiology 64(4): 1477–1483. 10.1128/AEM.64.4.1477-1483.1998
Soumahoro, S., Ouattara, H.G., Droux, M., Nasser, W., Niamke, S.L. and Reverchon, S., 2020. Acetic acid bacteria (AAB) involved in cocoa fermentation from Ivory Coast: species diversity and performance in acetic acid production. Journal of Food Science and Technology 57(5): 1904–1916. 10.1007/s13197-019-04226-2
Thompson, S.S., Miller, K.B., Lopez, A.S. and Camu, N., 2012. Cocoa and coffee. In: Doyle, M.P., Buchanan, R.L., (eds.) Food Microbiology: Fundamentals and Frontiers, ASM Press, Washington, pp. 881–899. 10.1128/9781555818463.ch35
Villeneuve, F., Cros, E., Vincent, J.C. and Macheix, J.J., 1989. Recherche d’un indice de fermentation du cacao, 3: Evolution des flavan-3-ols de la feve. Café, Cacao, Thé (Francia) 33(3): 165–170.
Wood, G.A.R., and Lass, R.A. (2008). Cocoa. 4th Edition. John Wiley & Sons, Oxford.