Extracellular phytase activites of lactic acid bacteria in sourdough mix prepared from traditionally produced boza as starter culture

Fermentation using Lactic Acid Bacteria (LAB) and LAB species can exhibit extracellular activities such as decreasing of antinutritional factors, in particular phytic acid (PA) or phytate. The objective of this study was to assess extracellular phytase activities of LAB in sourdough mix prepared from traditionally produced boza as starter culture. To do this, thirthy-five boza samples were collected from Central Anatolia, Marmara and Eastern Anatolia regions in Turkey to be used as starter culture for preparing sourdough mix. In each mixture, LAB strains and phytase (+) ones were screened by culture-based examination, characterized by VITEK® MS, and extracellular phytase activity of each LAB strain was determined by spectrophotometry. Overall, 29 presumptive strains of LAB were isolated. Of them, 21 were found to be phytase (+). The average extracellular phytase activity was 656.8±188.1 U//mL, and a Pediococcus pentosaceus EK1 isolate showed the highest activity as 1285.5 U/mL. In conclusion, the traditionally produced bozas have been found as potential starter culture reservoirs for sourdough fermentation with significantly higher extracellular phytase activities, thus challenging opportunitites to lower antinutritional factors, in particular phytic acid (PA) or phytate in the foods for the consumers.

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Anastasio, M., Pepe, O., Cirillo, T., Palomba, S., Blaiotta, G., Villani, F. (2010). Selection and use of phytate-degrading LAB to improve cereal-based products by mineral solubilization during dough fermentation. Journal of Food Science, 75, M28-35. https://doi.org/10.1111/j.1750-3841.2009.01402.x

Bae, H. D., Yanke, L. J., Cheng, K. J., Selinger, L. B. (1999). A novel staining method for detecting phytase activity. Journal of Microbiological Methods, 39(1), 17-22. https://doi.org/10.1016/S0167-7012(99)00096-2

Borcaklı, M., Öztürk, T., Yeşilada, E. (2018). Cereal source and microbial consortia of the starter culture influence the chemical composition and physicochemical characteristics of boza. Turkish Journal of Agriculture and Forestry, 42, 412-422. https://doi.org/10.3906/tar-1802-3

Catzeddu, P. (2019). Sourdough breads. In Flour and breads and their fortification in health and disease prevention (pp. 177-188). Academic Press. https://doi.org/10.1016/B978-0-12-814639-2.00014-9

Cizeikiene, D., Juodeikiene, G., Bartkiene, E., Damasius, J., Paskevicius, A. (2015). Phytase activity of lactic acid bacteria and their impact on the solubility of minerals from wholemeal wheat bread. International Journal of Food Sciences and Nutrition, 66(7), 736-742. https://doi.org/10.3109/09637486.2015.1088939

Damayanti, E., Ratisiwi, F., Istiqomah, L., Sembiring, L., Febrisiantosa, A. (2017). Phytate degrading activities of lactic acid bacteria isolated from traditional fermented food. AIP Conference Proceedings 1823, 020053. https://doi.org/10.1063/1.4978126

De Angelis, M., Gallo, G., Corbo, M. R., McSweeney, P. L., Faccia, M., Giovine, M., Gobbetti, M. (2003). Phytase activity in sourdough lactic acid bacteria: purification and characterization of a phytase from Lactobacillus sanfranciscensis CB1. International Journal of Food Microbiology, 87(3), 259-270. https://doi.org/10.1016/S0168-1605(03)00072-2

De Vuyst, L., Van Kerrebroeck, S., Harth, H., Huys, G., Daniel, H. M., Weckx, S. (2014). Microbial ecology of sourdough fermentations: diverse or uniform?. Food Microbiology, 37, 11-29. https://doi.org/10.1016/j.fm.2013.06.002

De Vuyst, L., Van Kerrebroeck, S., Leroy, F. (2017). Microbial ecology and process technology of sourdough fermentation. Advances in Applied Microbiology, 100, 49-160. https://doi.org/10.1016/bs.aambs.2017.02.003

Dubois, D., Grare, M., Prere, M. F., Segonds, C., Marty, N., Oswald, E. (2012). Performances of the Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry system for rapid identification of bacteria in routine clinical microbiology. Journal of Clinical Microbiology, 50(8), 2568-2576. https://doi.org/10.1128/JCM.00343-12

Erkmen, O., Bozoğlu, T. F. (2016). Food Microbiology: Principles into Practice. New Jersey: Wiley, p. 366, ISBN 9781119237761 https://doi.org/10.1002/9781119237860

Gänzle, M. G. (2014). Enzymatic and bacterial conversions during sourdough fermentation. Food Microbiology, 37, 2- 10. https://doi.org/10.1016/j.fm.2013.04.007

Gänzle, M., Ripari, V. (2016). Composition and function of sourdough microbiota: From ecological theory to bread quality. International Journal of Food Microbiology, 239, 19-25. https://doi.org/10.1016/j.ijfoodmicro.2016.05.004

Goswami, G., Bora, S. S., Parveen, A., Boro, R. C., Barooah, M. (2017). Identification and functional properties of dominant lactic acid bacteria isolated from Kahudi, a traditional rapeseed fermented food product of Assam, India. Journal of Ethnic Foods, 4(3), 187-197. https://doi.org/10.1016/j.jef.2017.08.008

Gotcheva, V., Pendiella, S.S., Angelov, A., Roshkova, Z., Webb, C. (2001). Monitoring the fermentation of the traditional Bulgarian beverage boza. International Journal of Food Science and Technology, 36, 129-134. https://doi.org/10.1046/j.1365-2621.2001.00429.x

Grases, F., Prieto, R. M., Costa-Bauza, A. (2017). Dietary phytate and interactions with mineral nutrients. In Clinical Aspects of Natural and Added Phosphorus in Foods (pp. 175- 183). Springer, New York. https://doi.org/10.1007/978-1-4939-6566-3_12

Hancioglu, O., Karapinar, M. (1997). Microflora of Boza, a traditional fermented Turkish beverage. International Journal of Food Microbiology, 35, 271-274. https://doi.org/10.1016/S0168-1605(96)01230-5

Hurrell, R. F., Reddy, M. B., Juillerat, M. A., Cook, J. D. (2003). Degradation of phytic acid in cereal porridges improves iron absorption by human subjects. The American Journal of Clinical Nutrition, 77(5), 1213-1219. https://doi.org/10.1093/ajcn/77.5.1213

Irkin, R. (2019). Natural Fermented Beverages. In A. M. Grumezescu & A. M. Holban (Eds.), Natural Beverages (p. 399-425). Cambridge MA: Woodhead Publishing Elsevier. ISBN: 9780128166895 https://doi.org/10.1016/B978-0-12-816689-5.00014-6

ISO 6887-6. (2013). Microbiology of food and animal feed - - Preparation of test samples, initial suspension and decimal dilutions for microbiological examination - Part 6: Specific rules for the preparation of samples taken at the primary production stage. ISO, E. 11133: 2014. Microbiology of food, animal feed and water− Preparation, production, storage and performance testing of culture media.

Karaman, K., Sagdic, O., Durak, M. Z. (2018). Use of phytase active yeasts and lactic acid bacteria isolated from sourdough in the production of whole wheat bread. LWT - Food Science and Technology, 91, 557-567. https://doi.org/10.1016/j.lwt.2018.01.055

Khodaii, Z., Natanzi, M., Naseri, M., Goudarzvand, M., Dodson, H., Snelling, A. (2013). Phytase activity of lactic acid bacteria isolated from dairy and pharmaceutical probiotic products. International Journal of Enteric Pathogens, 1, 12-16. https://doi.org/10.17795/ijep9359

Kivanc, M., Yilmaz, M., Cakir, E. (2011). Isolation and identifi cation of lactic acid bacteria from boza, and their microbial activity against several reporter strains. Turkish Journal of Biology, 35, 313-324.

Konietzny, U., Greiner, R. (2004). Bacterial phytase: potential application, in vivo function and regulation of its synthesis. Brazilian Journal of Microbiology, 35(1), 11-18. https://doi.org/10.1590/S1517-83822004000100002

Kourkouta, L., Koukourikos, K., Iliadis, C., Ouzounakis, P., Monios, A., Tsaloglidou, A. (2017). Bread and health. Journal of Pharmacy and Pharmacology, 5, 821-826. https://doi.org/10.17265/2328-2150/2017.11.005

Leenhardt, F., Levrat-Verny, M.A., Chanliaud, E., Rémésy, C. (2005). Moderate decrease of pH by sourdough fermentation is sufficient to reduce phytate content of whole wheat flour through endogenous phytase activity. Journal of Agricultural and Food Chemistry, 53(1), 98-102. https://doi.org/10.1021/jf049193q

Lokumcu Altay, F., Karbancioglu-Guler, F., Daskaya Dikmen, C., Heperkan, Z.D. (2013). A review on traditional Turkish fermented non-alcoholic beverages: Microbiota, fermentation process and quality characteristics. International Journal of Food Microbiology, 167, 44-56. https://doi.org/10.1016/j.ijfoodmicro.2013.06.016

Lopez, H. W., Ouvry, A., Bervas, E., Guy, C., Messager, A., Demigne, C., Remesy, C. (2000). Strains of lactic acid bacteria isolated from sour doughs degrade phytic acid and improve calcium and magnesium solubility from wholewheat flour. Journal of Agricultural and Food Chemistry, 48(6), 2281-2285. https://doi.org/10.1021/jf000061g

Lott, J. N., Ockenden, I., Raboy, V., Batten, G.D. (2000). Phytic acid and phosphorus in crop seeds and fruits: a global estimate. Seed Science Research, 10(1), 11-33. https://doi.org/10.1017/S0960258500000039

Menteş, Ö., Ercan, R., Akçelik, M. (2007). Inhibitor activities of two Lactobacillus strains, isolated from sourdough, against rope-forming Bacillus strains. Food Control, 18(4), 359-363. https://doi.org/10.1016/j.foodcont.2005.10.020

Moll, R., Davis, B. (2017). Iron, vitamin B12 and folate. Medicine, 45(4), 198-203. https://doi.org/10.1016/j.mpmed.2017.01.007

Nuobariene, L., Cizeikiene, D., Gradzeviciute, E., Hansen, Å.S., Rasmussen, S.K., Juodeikiene, G., Vogensen, F. K. (2015). Phytase-active lactic acid bacteria from sourdoughs: Isolation and identification. LWT-Food Science and Technology, 63(1), 766-772. https://doi.org/10.1016/j.lwt.2015.03.018

Osimani, A., Garofalo, C., Aquilanti, L., Milanović, V., Clementi, F. (2015). Unpasteurised commercial boza as a source of microbial diversity. International Journal of Food Microbiology, 194, 62-70. https://doi.org/10.1016/j.ijfoodmicro.2014.11.011

Papadimitriou, K., Alegría, Á., Bron, P.A., de Angelis, M., Gobbetti, M., Kleerebezem, M., Lemos, J.A., Linares, D.M., Ross, P., Stanton, C., Turroni, F., van Sinderen, D., Varmanen, P., Ventura, M., Zúñiga, M., Tsakalidou, E., Kok, J. (2016). Stress physiology of lactic acid bacteria. Microbiology and Molecular Biology Reviews: MMBR, 80(3), 837-890. https://doi.org/10.1128/MMBR.00076-15

Papadimitriou, K., Zoumpopoulou, G., Georgalaki, M., Alexandraki, V., Kazou, M., Anastasiou, R., Tsakalidou, E. (2019). Sourdough Bread. In Innovations in Traditional Foods (pp. 127-158). Woodhead Publishing. https://doi.org/10.1016/B978-0-12-814887-7.00006-X

Petrova, P., Petrov, K. (2017). Traditional Cereal Beverage Boza Fermentation Technology, Microbial Content and Healthy Effects. In Fermented Foods, Part II (pp. 284-305). CRC Press. ISBN: 978-1-1386-3784-9

Priyodip, P., Prakash, P. Y., Balaji, S. (2017). Phytases of probiotic bacteria: Characteristics and beneficial aspects. Indian Journal of Microbiology, 57(2), 148-154. https://doi.org/10.1007/s12088-017-0647-3

Raghavendra, P., Halami, P. M. (2009). Screening, selection and characterization of phytic acid degrading lactic acid bacteria from chicken intestine. International Journal of Food Microbiology, 133(1-2), 129-134. https://doi.org/10.1016/j.ijfoodmicro.2009.05.006

Reale, A., Mannina, L., Tremonte, P., Sobolev, A.P., Succi, M., Sorrentino, E., Coppola, R. (2004). Phytate degradation by lactic acid bacteria and yeasts during the wholemeal dough fermentation: a 31P NMR study. Journal of Agricultural and Food Chemistry, 52(20), 6300-6305. https://doi.org/10.1021/jf049551p

Reale, A., Konietzny, U., Coppola, R., Sorrentino, E., Greiner, R. (2007). The importance of lactic acid bacteria for phytate degradation during cereal dough fermentation. Journal of Agricultural and Food Chemistry, 55(8), 2993-7. https://doi.org/10.1021/jf063507n

Rollán, G.C., Gerez, C.L., LeBlanc, J.G. (2019). Lactic fermentation as a strategy to improve the nutritional and functional values of pseudocereals. Frontiers in Nutrition 6, 1-16.

Shi, J., Arunasalam, K., Yeung, D., Kakuda, Y., Mittal, G. (2004). Phytate from edible beans: chemistry, processing and health benefits. Journal of Food Agriculture and Enviroment, 2, 49-58. https://doi.org/10.3389/fnut.2019.00098

Songré-Ouattara, L.T., Mouquet-Rivier, C., Icard-Vernière, C., Humblot, C., Diawara, B., Guyot, J.P. (2008). Enzyme activities of lactic acid bacteria from a pearl millet fermented gruel (ben-saalga) of functional interest in nutrition. International Journal of Food Microbiology, 128(2), 395-400. https://doi.org/10.1016/j.ijfoodmicro.2008.09.004

Sumengen, M., Dincer, S., Kaya, A. (2013). Production and characterization of phytase from Lactobacillus plantarum. Food Biotechnology, 27(2), 105-118. https://doi.org/10.1080/08905436.2013.781507

Sümengen, M., Dinçer, S., Kaya, A. (2012). Phytase production from Lactobacillus brevis. Turkish Journal of Biology, 36, 533-541.

Tharmaraj, N., Shah, N.P. (2003). Selective enumeration of Lactobacillus delbrueckii ssp. bulgaricus, Streptococcus thermophilus, Lactobacillus acidophilus, bifidobacteria, Lactobacillus casei, Lactobacillus rhamnosus, and propionibacteria. Journal of Dairy Science, 86(7), 2288-2296. https://doi.org/10.3168/jds.S0022-0302(03)73821-1

Yildirim, R.M., Arici, M. (2019). Effect of the fermentation temperature on the degradation of phytic acid in whole-wheat sourdough bread. LWT - Food Science and Technology, 112, 108224. https://doi.org/10.1016/j.lwt.2019.05.122

Zamudio, M., González, A., Medina, J.A. (2001). Lactobacillus plantarum phytase activity is due to non-specific acid phosphatase. Letters in Applied Microbiology, 32, 181-184. https://doi.org/10.1046/j.1472-765x.2001.00890.x