Resumen
El objetivo de este trabajo fue aislar e identificar levaduras del lactosuero del queso Paipa y evaluar su potencial probiótico (in vitro) para su uso en alimentación animal. Las cepas se aislaron en caldo extracto de levadura-glucosa-cloranfenicol, se purificaron en agar PDA y se caracterizaron molecularmente. Se aislaron 10 cepas dentro de las que se encuentran Candida kefyr, Kluyveromyces marxianus, Pichia fermentans, entre otras. Las levaduras aisladas fueron evaluadas para evidenciar su uso potencial como probióticos en alimentación animal. Se determinó la resistencia a sales biliares (0,05, 0,1, 0,15, 0,20, 0,25 y 0,30 %), la estabilidad al pH del estómago (1,5, 2,0, 2,5, 3,0, 3,5 y 4,0) y resistencia al jugo gástrico (pH 1,5, NaCl de 0,2 % y pepsina de 0,32 %). En la prueba con diferentes concentraciones de sales biliares, las mejores cepas fueron K. marxianus (30_4) y P. fermentans (28_5). En la prueba de pH, el mejor desempeño lo tuvieron P. marxianus (30_4) y Yarrowia lipolytica. Finalmente, en la prueba de jugos gástricos se destacaron C. kefyr y K. marxianus (R_1). Las cepas que presentaron buen desempeño en casi todas las pruebas fueron K. marxianus (30_4) y P. fermentans (28_5), de tal forma que estas levaduras aisladas del lactosuero de queso Paipa tienen potencial en la aplicación como probióticos en la alimentación animal.
Bae, D., Kim, D., Chon, J., Song, K., & Seo, K. (2020). Synergistic effects of the early administration of Lactobacillus kefiranofaciens DN1 and Kluyveromyces marxianus KU140723-05 on the inhibition of Salmonella enteritidis colonization in young chickens. Poultry Science, 99(11), 5999-6006. https://doi.org/10.1016/j.psj.2020.07.032
Begley, M., Hill, C., & Gahan, C. (2006). Bile salt hydrolase activity in probiotics. Applied and Environmental Microbiology, 72(3), 1729-1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
Bertel, L., Betancur, C., & Oviedo, L. (2019). Identificación de Bacillus toyonensis en heces de ganado cebú en el Departamento de Sucre, Colombia. Revista Colombiana de Biotecnología, 21(2), 12-21. https://doi.org/10.15446/rev.colomb.biote.v21n2.69421
Canibe, N., & Borg, B. (2012). Fermented liquid feed—microbial and nutritional aspects and impact on enteric diseases in pigs. Animal Feed Science and Technology, 173(1-2), 17-40. https://doi.org/10.1016/j.anifeedsci.2011.12.021
Castellanos, J., Pérez, R., Grande, M., Lucas, R., & Gálvez, A. (2020). Analysis of the bacterial diversity of Paipa cheese (a traditional raw cow’s milk cheese from Colombia) by high-throughput sequencing. Microorganisms, 8(2), 218. https://doi.org/10.3390/microorganisms8020218
Castillo, P., Betancur, C., & Pardo, E. (2018). Caracterización de microorganismos con potencial probiótico aislados de estiércol de terneros Brahman en Sucre, Colombia. Revista de Investigaciones Veterinarias del Perú, 29(2), 438-448. https://doi.org/10.15381/rivep.v29i2.14482
Coloretti, F., Chiavari, C., Luise, D., Tofalo, R., Fasoli, G., Suzzi, G., & Grazia, L. (2017). Detection and identification of yeasts in natural whey starter for Parmigiano Reggiano cheese-making. International Dairy Journal, 66, 13-17. https://doi.org/10.1016/j.idairyj.2016.10.013
Cruz, A., Håkenåsen, M., Skugor, A., Mydland, L., Åkesson, C., Hellestveit, S., Sørby, R., Pressc, C., & Øverland, M. (2019). Candida utilis yeast as a protein source for weaned piglets: Effects on growth performance and digestive function. Livestock Science, 226, 31-39. https://doi.org/10.1016/j.livsci.2019.06.003
Díaz-Vergara, L., Pereyra, C., Montenegro, M., Pena, G., Aminahuel, C., & Cavaglieri, L. (2017). Encapsulated whey – native yeast Kluyveromyces marxianus as feed additive for animal production. Food Additives & Contaminants: Part A, 34(5), 750-759. https://doi.org/10.1080/19440049.2017.1290830
Duncan, S., Scott, K., Ramsay, A., Harmsen, H., Welling, G., Stewart, C., & Flint, H. (2003). Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Applied and Environmental Microbiology, 69(2), 1136-1142. https://doi.org/10.1128/AEM.69.2.1136-1142.2003
Federación Colombiana de Ganaderos [Fedegan]. (2020). Balance y perspectivas del sector ganadero colombiano (2019-2020). https://estadisticas.fedegan.org.co/DOC/download.jsp?pRealName=Balance_Y_Perspectivas_2019_2020.pdf&iIdFiles=683
Greppi, A., Saubade, F., Botta, C., Humblot, C., Guyot, J., & Cocolin, L. (2017). Potential probiotic Pichia kudriavzevii strains and their ability to enhance folate content of traditional cereal-based African fermented food. Food Microbiology, 62, 169-177. https://doi.org/10.1016/j.fm.2016.09.016
Guel, G., Hernández, J., & Rodríguez, G. (2018). Uso de bacterias obtenidas a partir de suero de leche y su uso potencial como probióticos en la industria alimentaria. Revista Boliviana de Química, 35(1), 40-45. http://www.scielo.org.bo/pdf/rbq/v35n1/v35n1_a05.pdf
Gut, A., Vasiljevic, T., Yeager, T., & Donkor, O. (2019). Characterization of yeasts isolated from traditional kefir grains for potential probiotic properties. Journal of Functional Foods, 58, 56-66. https://doi.org/10.1016/j.jff.2019.04.046
Helmy, E., Soliman, S., Abdel-Ghany, T., & Ganash, M. (2019). Evaluation of potentially probiotic attributes of certain dairy yeast isolated from buffalo sweetened Karish cheese. Heliyon, 5(5), e01649. https://doi.org/10.1016/j.heliyon.2019.e01649
Huang, S., Rabah, H., Ferret-Bernard, S., Le Normand, L., Gaucherb, F., Guerind, S., Nogret, I., Le Loirb, Y., Dong, X., Janb, G., Boudry, G., & Jeantet, R. (2019). Propionic fermentation by the probiotic Propionibacterium freudenreichii to functionalize whey. Journal of Functional Foods, 52, 620-628. https://doi.org/10.1016/j.jff.2018.11.043
Hu, X., Liu, Q., Hu, J., Zhou, J., Zhang, X., Peng, S., Peng, L., & Wang, X. (2018). Identification and characterization of probiotic yeast isolated from digestive tract of ducks. Poultry Science, 97(8), 2902-2908. https://doi.org/10.3382/ps/pey152
Jurado, H., Aguirre, D., & Ramírez, C. (2009). Caracterización de bacterias probióticas aisladas del intestino grueso de cerdos como alternativa al uso de antibióticos. Revista MVZ Córdoba, 14(2), 1723-1735. https://doi.org/10.21897/rmvz.356
Kareb, O., & Aider, M. (2019). Whey and its derivatives for probiotics, prebiotics, synbiotics, and functional foods: a critical review. Probiotics Antimicrobial Proteins, 11, 348-369. https://doi.org/10.1007/s12602-018-9427-6
Karim, A., Gerliani, N., & Aider, M. (2020). Kluyveromyces marxianus: An emerging yeast cell factory for applications in food and biotechnology. International Journal of Food Microbiology, 333, 108818. https://doi.org/10.1016/j.ijfoodmicro.2020.108818
Keimer, B., Pieper, R., Simon, A., & Zentek, J. (2018). Effect of time and dietary supplementation with processed yeasts (Kluyveromyces fragilis) on immunological parameters in weaned piglets. Animal Feed Science and Technology, 245, 136-146. https://doi.org/10.1016/j.anifeedsci.2018.09.008
Khaire, R., & Gogate, P. (2020). Optimization of ultrafiltration of whey using Taguchi method for maximizing recovery of lactose. Separation and Purification Technology, 248, 117063. https://doi.org/10.1016/j.seppur.2020.117063
Knob, A., Izidoro, S., Tigre, L., Rodrigues, A., & Aparecido, V. (2020). A novel lipolytic yeast Meyerozyma guilliermondii: Efficient and low-cost production of acid and promising feed lipase using cheese whey. Biocatalysis and Agricultural Biotechnology, 24, 101565. https://doi.org/10.1016/j.bcab.2020.101565
López, R., Becerra, M., & Borrás, L. (2018). Caracterización físico-química y microbiológica del lactosuero del queso Paipa. Ciencia y Agricultura, 15(2), 99-106. http://doi.org/10.19053/01228420.v15.2
Louasté, B., & Eloutassi, N. (2020). Succinic acid production from whey and lactose by Actinobacillus succinogenes 130Z in batch fermentation. Biotechnology Reports, 27, e00481. https://doi.org/10.1016/j.btre.2020.e00481
Markowiak, P., & Śliżewska, K. (2018). The role of probiotics, prebiotics and symbiotic in animal nutrition. Gut Pathogens, 10, 1-21. https://doi.org/10.1186/s13099-018-0250-0
Mendoza, A. (2013). Caracterización de la levadura Kluyveromyces marxianus como microorganismo probiótico [Tesis de Maestría, Universidad Autónoma del Estado de Hidalgo, México]. Repositorio UAEH. https://repository.uaeh.edu.mx/bitstream/handle/123456789/14791
Ministerio de Agricultura y Desarrollo Rural [MADR]. (2016). Implementación política para mejorar la competitividad del sector lácteo nacional. Gobierno de Colombia. https://www.minagricultura.gov.co/ministerio/direcciones/Documents/INFORME%20UE%20FASE%202%20- SEGUNDO%20TRAMO%20VARIABLE%20%28MARZO%202016%29.pdf
Missotten, J., Michiels, J., Degroote, J., & De Smet, S. (2015). Fermented liquid feed for pigs: an ancient technique for the future. Journal of Animal Science and Biotechnology, 6, Art. ID 4. https://doi.org/10.1186/2049-1891-6-4
Mitchell, L., & Heinrichs, A. (2020). Feeding various forages and live yeast culture on weaned dairy calf intake, growth, nutrient digestibility, and ruminal fermentation. Journal of Dairy Science, 103(10), 8880-8897. https://doi.org/10.3168/jds.2020-18479
Moser, S., & Savage, D. (2001). Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in Lactobacilli. Applied and Environmental Microbiology, 67(8), 3476-3480. https://doi.org/10.1128/AEM.67.8.3476-3480.2001
Mortada, M., Cosby, D., Shanmugasundaram, S., & Selvaraj, R (2020). In vivo and in vitro assessment of commercial probiotic and organic acid feed additives in broilers challenged with Campylobacter coli. Journal of Applied Poultry Research, 29(2), 435-446. https://doi.org/10.1016/j.japr.2020.02.001
Ohgaki, R., Nakamura, N., Mitsui, K., & Kanazawa, H. (2005). Characterization of the ion transport activity of the budding yeast Na+/H+ antiporter, Nha1p, using isolated secretory vesicles. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1712(2), 185-196. https://doi.org/10.1016/j.bbamem.2005.03.011
Pal, M., & Kumar, R. (2018). Exoelectrogenic response of Pichia fermentans influenced by mediator and reactor design. Journal of Bioscience and Bioengineering, 127(6), 714-720. https://doi.org/10.1016/j.jbiosc.2018.11.004
Pereira, R., Naves, C., Genisheva, A., Freitas, R., & Ferreira, W. (2017). Yeasts from Canastra cheese production process: isolation and evaluation of their potential for cheese whey fermentation. Food Research International, 91, 72-79. https://doi.org/10.1016/j.foodres.2016.11.032
Poloni, V., Salvato, L., Pereyra, C., Oliveira, A., Rosa, C., Cavaglieri, L., & Moura, K. (2020). Bakery by-products based feeds borne-Saccharomyces cerevisiae strains with probiotic and antimycotoxin effects plus antibiotic resistance properties for use in animal production. Food and Chemical Toxicology, 107(Part B), 630-636. https://doi.org/10.1016/j.fct.2017.02.040
Ravasio, D., Carlin, S., Boekhout, T., Groenewald, M., Vrhovsek, U., Walther, A., & Wendland, J. (2018). Adding flavor to beverages with non-conventional yeasts. Fermentation, 4(1), 15. https://doi.org/10.3390/fermentation4010015
Rehman, A., Arif, M., Sajjad, N., Al-Ghadi, M., Alagawany, M., Abd El-Hack, M., Al-Himadi, A., Elnesr, S., Almutairi, B., Amran, R., & Swelum, A. (2020). Dietary effect of probiotic and prebiotic on broiler performance, carcass and immunity. Poultry Science, 99(12), 6946-6953. https://doi.org/10.1016/j.psj.2020.09.043
Rosa, L., Santos, M., Abreu, J., Balthazar, C., Rocha, R., Silva, H., Esmerino, E., Duarte, M., Pimentel, T., Freitas, M., Silva, M., Cruz, A., & Teodoro, A. (2020). Antiproliferative and apoptotic effects of probiotic whey dairy beverages in human prostate cell lines. Food Research International, 137, 109450. https://doi.org/10.1016/j.foodres.2020.109450
Saadat, Y., Yari, A., Akbar, A., Talebi, M., & Pourghassem, B. (2020). Modulatory role of exopolysaccharides of Kluyveromyces marxianus and Pichia kudriavzevii as probiotic yeasts from dairy products in human colon cancer cells. Journal of Functional Foods, 64, 103675. https://doi.org/10.1016/j.jff.2019.103675
Sampaolesi, S., Gamba, R., De Antoni, G., & León, A. (2019). Potentiality of yeasts obtained as beer fermentation residue to be used as probiotics. LWT - Food Science and Technology, 113, 108251. https://doi.org/10.1016/j.lwt.2019.108251
Sanger, F., Nicklen, S., & Coulson, A. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academic of Sciences USA, 74(12), 5463-5467. https://doi.org/10.1073/pnas.74.12.5463
Sen, S., & Mansell, T. (2020). Yeasts as probiotics: Mechanisms, outcomes, and future potential. Fungal Genetics and Biology, 137, 103333. https://doi.org/10.1016/j.fgb.2020.103333
Shurson, G. (2018). Yeast and yeast derivatives in feed additives and ingredients: sources, characteristics, animal responses, and quantification methods. Animal Feed Science and Technology, 235, 60-76. https://doi.org/10.1016/j.anifeedsci.2017.11.010
St Pierre, M., Ruetz, S., Epstein, L., Gros, P., & Arias, I. (1994). ATP-dependent transport of organic anions in secretory vesicles of Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America PNAS, 91(20), 9476-9479. https://doi.org/10.1073/pnas.91.20.9476
Superintendencia de Industria y Comercio de Colombia. (2011). Denominación de Origen Queso PAIPA. Resolución 0070-802. https://www.sic.gov.co/sites/default/files/files/Denominacion%20de%20Origen/Agro%20-%20Alimenticios/Queso%20Paipa/queso_paipa.pdf
Tachibana, L., Telli, G., Dias, D., Gonçalves, G., Massatoshi, C., Bertoncello, R., Miyoko, M., Hamed, S., & Ranzani-Paiva, M. (2020). Effect of feeding strategy of probiotic Enterococcus faecium on growth performance, hematologic, biochemical parameters and non-specific immune response of Nile tilapia. Aquaculture Reports, 16, 100277. https://doi.org/10.1016/j.aqrep.2020.100277
Vanden, N., Díaz-Vergara, L., Rossi, Y., Aminahuel, C., Mauri, A., Cavaglieri, L., & Montenegro, M. (2020). Effect of microencapsulation in whey protein and water-soluble chitosan derivative on the viability of the probiotic Kluyveromyces marxianus VM004 during storage and in simulated gastrointestinal conditions. LWT - Food Science and Technology, 118, 108844. https://doi.org/10.1016/j.lwt.2019.108844
Vohra, A., Syal, P., & Madan, A. (2016). Probiotic yeasts in livestock sector. Animal Feed Science and Technology, 219, 31-47. https://doi.org/10.1016/j.anifeedsci.2016.05.019
Yadav, J., Bezawada, J., Yan, S., Tyagi, R., & Surampalli, R. (2012). Candida krusei: biotechnological potentials and concerns about its safety. Canadian Journal of Microbiology, 58(8), 937-952. https://doi.org/10.1139/w2012-077
Zouari, A., Briard-Bion, V., Gaucheron, F., Schuck, P., Gaiani, C., Triki, M., Hamadi Attia, H., & Ayadi, M. (2020). Effect of pH on the physicochemical characteristics and the surface chemical composition of camel and bovine whey protein’s powders. Food Chemistry, 333, 127514. https://doi.org/10.1016/j.foodchem.2020.127514
Zullo, B., & Ciafardini, G. (2019). Evaluation of physiological properties of yeast strains isolated from olive oil and their in vitro probiotic trait. Food Microbiology, 78, 179-187. https://doi.org/10.1016/j.fm.2018.10.016