ACE- Inhibitory and metal-binding activity produced during milk fermentation by three probiotic potential LAB strains isolated from Chiapas double cream cheese

Keywords: Lactic acid bacteria, ACE-inhibitory activity, metal-binding activity, double cream cheese, halotolerant probiotics

Abstract

Some probiotic lactic acid bacteria could generate bioactive peptides during milk fermentation. The aim of this work was to evaluate the ACE inhibitory and mineral-binding (calcium and iron) activity during milk fermentation by three probiotic LAB strains (Lactobacillus plantarum, Lb. pentosus and Lb. acidipiscis) as well as mixed fermentation.  These strains were previously isolated from Chiapas double cream cheese. The fermentation that showed the highest microbial growth was performed by Lb. plantarum, followed by mixed fermentation and Lb. acidipiscis. However, the mixed fermentation had higher proteolysis. Milk fermentations performed with Lb. acidispiscis, Lb. pentosus and mixed showed high ACE-inhibitory activity (97%). The Lb. plantarum and mixed fermentations showed the higher iron-binding activity, 99 % and 97, respectively, whereas the Lb. acidipiscis and mixed fermentations had the highest calcium-binding activity. These results showed that probiotic microorganisms isolated from double cream cheese have great potential to be used in the production of functional foods.

References

Abdel-Hamid, M., Otte, J., De Gobba, C., Osman, A., and Hamad, E. (2017). Angiotensin I-converting enzyme inhibitory activity and antioxidant capacity of bioactive peptides derived from enzymatic hydrolysis of buffalo milk proteins. International Dairy Journal 66, 91–98.
Abubakr, M.A.S., Hassan, Z., Muftah, M., Imdakim, A., and Sharifah, N.R.S.A. (2012). Antioxidant activity of lactic acid bacteria (LAB) fermented skim milk as determined by 1,1-diphenyl-2-picrylhydrazyl (DPPH) and ferrous chelating activity (FCA). African Journal of Microbiology Research 6, 6358–6364.
Adler-Nissen, J. (1979). Determination of the degree of hydrolysis of food protein hydrolysates by trinitrobenzenesulfonic acid. Journal of Agricultural and Food Chemistry 27, 1256–1262.
Agyei, D., Ongkudon, C.M., Wei, C.Y., Chan, A.S., and Danquah, M.K. (2016). Bioprocess challenges to the isolation and purification of bioactive peptides. Food and Bioproducts Processing 98, 244–256.
Antonios, T.F.T. and MacGregor, G.A. (1995). Angiotensin-converting enzyme inhibitors in hypertension: potential problems. Journal of Hypertension 13, S11–S16.
Argyri, A.A., Zoumpopoulou, G., Karatzas, K.A.G., Tsakalidou, E., Nychas, G.J.E., Panagou, E.Z., and Tassou, C.C. (2013). Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiology 33, 282–29.
Ayyash, M., Al-Dhaheri, A.S., Al Mahadin, S., Kizhakkayil, J., and Abushelaibi, A. (2018). In vitro investigation of anticancer, antihypertensive, antidiabetic, and antioxidant activities of camel milk fermented with camel milk probiotic: A comparative study with fermented bovine milk. Journal of Dairy Science 101, 900–911.
Behera, S.S., Ray, R.C., and Zdolec, N. (2018). Lactobacillus plantarum with functional properties: an approach to increase safety and shelf-life of fermented foods. Biomed Research International 2018- 9361614, 1–18.
Buttriss, J. (1997). Nutritional properties of fermented milk products. International Journal of Dairy Technology 50, 21–27.
Carballo-Sánchez, M.P., Ramírez-Ramírez, J.C., Gimeno, M., Hall, G.M., Ríos-Durán, M.G. and Shirai, K. (2016). Papaya (Carica papaya) and tuna (Thunnus albacares) by-products fermentation as biomanufacturing approach towards antioxidant protein hydrolysates. Revista Mexicana de Ingeniería Química 15, 91–100.
Chalamaiah, M., Yu, W., and Wu, J. (2018). Immunomodulatory and anticancer protein hydrolysates (peptides) from food proteins: a review. Food Chemistry 245, 205–222.
Chaves-López, C., Serio, A., Paparella, A., Martuscelli, M., Corsetti, A., Tofalo, R. and Suzzi, G. (2014). Impact of microbial cultures on proteolysis and release of bioactive peptides in fermented milk. Food Microbiology 42, 117–121.
Dimitrov, Z. (2009). Characterization of bioactive peptides with calcium-binding activity released by specially designed cheese starter. Biotechnology & Biotechnological Equipment 23, 927–930.
dos Santos, K.M.O., Vieira, A.D.S., Buriti, F.C.A., do Nascimento, J.C.F., de Melo, M.E.S., Bruno, L.M., de Fátima Borges, M., Rocha, C.R.C., de Souza Lopes, A.C., de Melo Franco, B.D.G. and Todorov, S.D. (2015). Artisanal Coalho cheeses as source of beneficial Lactobacillus plantarum and Lactobacillus rhamnosus strains. Dairy Science and Technology 95, 209–230.
Fajardo-Espinoza, F.S., Romero-Rojas, A. and Hernández-Sánchez, H. (2020). Production of bioactive peptides from bovine colostrum whey using enzymatic hydrolysis. Revista Mexicana de Ingeniería Química 19, 1–9.
Fernández-Tomé, S., Martínez-Maqueda, D., Girón, R., Goicoechea, C., Miralles, B., and Recio, I. (2016). Novel peptides derived from αs1-casein with opioid activity and mucin stimulatory effect on HT29-MTX cells. Journal of Functional Foods 25, 466–476.
Figueroa-Hernández, C., Cruz-Guerrero, A., Rodríguez-Serrano, G., Gómez-Ruiz, L., García-Garibay, M., and Jiménez-Guzmán, J. (2012). Producción de péptidos fijadores de calcio y hierro por Lactococcus lactis subsp. cremoris NCFB 712. Revista Mexicana de Ingieniería Química 11, 259–267.
Figueroa-Hernández, C., Mota-Gutierrez, J., Ferrocino, I., Hernández-Estrada, Z.J., González-Ríos, O., Cocolin, L. and Suárez-Quiroz, M.L. (2019). The challenges and perspectives of the selection of starter cultures for fermented cocoa beans. International Journal of Food Microbiology 301, 41–50.
Gobbetti, M., Stepaniak, L., De Angelis, M., Corsetti, A. and Di Cagno, R. (2002). Latent bioactive peptides in milk proteins: proteolytic activation and significance in dairy processing. Critical Reviews in Food Science and Nutrition 42, 223–39.
González-Córdova, A.F., Yescas, C., Ortiz-Estrada, Á.M., De la Rosa-Alcaraz, M. de los Á., Hernández-Mendoza, A. and Vallejo-Cordoba, B. (2016). Invited review: Artisanal Mexican cheeses. Journal of Dairy Science 99, 3250–3262.
Gonzalez-Gonzalez, C.R., Machado, J., Correia, S., McCartney, A.L., Stephen Elmore, J. and Jauregi, P. (2019). Highly proteolytic bacteria from semi-ripened Chiapas cheese elicit angiotensin-I converting enzyme inhibition and antioxidant activity. LWT-Food Science and Technology 111, 449–456.
Gonzalez-Gonzalez, C.R., Tuohy, K.M. and Jauregi, P. (2011). Production of angiotensin-I-converting enzyme (ACE) inhibitory activity in milk fermented with probiotic strains: Effects of calcium, pH and peptides on the ACE-inhibitory activity. International Dairy Journal 21, 615–622.
Guzmán-Rodríguez, F., Gómez-Ruiz, L., Rodríguez-Serrano, G., Alatorre-Santamaría, S., García-Garibay, M., and Cruz-Guerrero, A. (2019). Iron binding and antithrombotic peptides released during the fermentation of milk by Lactobacillus casei Shirota. Revista Mexicana de Ingieniería Química 18, 1161-1166.
Hassan, T.H., Badr, M.A., Karam, N.A., Zkaria, M., El Saadany, H.F., Rahman, D.M.A., Shahbah, D.A., Al Morshedy, S.M., Fathy, M., Hosni Esh, A.M. and Selim, A.M. (2016). Impact of iron deficiency anemia on the function of the immune system in children. Medicine 95, (47), ec5395.
Huang, S.L., Zhao, L.N., Cai, X., Wang, S.Y., Huang, Y.F., Hong, J. and Rao, P.F. (2015). Purification and characterisation of a glutamic acid-containing peptide with calcium-binding capacity from whey protein hydrolysate. Journal of Dairy Research 82, 29–35.
Hwang, J.Y., Shue, Y.S. and Chang, H.M. (2001). Antioxidative activity of roasted and defatted peanut kernels. Food Research International 34, 639–647.
Ibrahim, H.R., Isono, H., and Miyata, T. (2018). Potential antioxidant bioactive peptides from camel milk proteins. Animal Nutrition 4, 273–280.
Jung, W.K. and Kim, S.K. (2007). Calcium-binding peptide derived from pepsinolytic hydrolysates of hoki (Johnius belengerii) frame. European Food Research and Technology 224, 763–767.
Kato, K., Takada, Y., Matsuyama, H., Kawasaki, Y., Aoe, S., Yano, H., and Toba, Y. (2002). Milk calcium taken with cheese increases bone mineral density and bone strength in growing rats. Bioscience Biotechnology & Biochemistry, 66, 2342–2346.
Kazou, M., Alexandraki, V., Pot, B., Tsakalidou, E. and Papadimitriou, K. (2017). Complete genome sequence of the dairy isolate Lactobacillus acidipiscis ACA-DC 1533. Genome Announcements 5, 1–2.
Korhonen, H. (2009). Milk-derived bioactive peptides: from science to applications. Journal of Functional Foods 1, 177–187.
Korhonen, H. and Pihlanto, A. (2006). Bioactive peptides production and functionality. International Dairy Journal 16, 945–960.
Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275.
Matejčeková, Z., Liptáková, D., Spodniaková, S. and Valík, Ľ. (2016). Characterization of the growth of Lactobacillus plantarum in milk in dependence on temperature. Acta Chimica Slovaca 9, 104–108.
Melgar-Lalanne, G., Rivera-Espinoza, Y., Reyes Méndez, A.I. and Hernández-Sánchez, H. (2013). In Vitro evaluation of the probiotic potential of halotolerant lactobacilli isolated from a ripened tropical Mexican cheese. Probiotics and Antimicrobial Proteins 5, 239–251.
Miles, A.A., Misra, S.S. and Irwin, J.O. (1938). The estimation of the bactericidal power of the blood. The Journal of Hygiene 38, 732–49.
Morales, F., Morales, J.I., Hernández, C.H. and Hernández-Sánchez, H. (2011). Isolation and partial characterization of halotolerant lactic acid bacteria from two Mexican cheeses. Applied Biochemistry and Biotechnology 164, 889–905.
Oguntoyinbo, F.A.and Narbad, A. (2015). Multifunctional properties of Lactobacillus plantarum strains isolated from fermented cereal foods. Journal of Functional Foods 17, 621–631.
Oh, Y.J. and Jung, D.S. (2015). Evaluation of probiotic properties of Lactobacillus and Pediococcus strains isolated from Omegisool, a traditionally fermented millet alcoholic beverage in Korea. LWT - Food Science and Technology 63, 437–444.
Pihlanto, A., Virtanen, T. and Korhonen, H. (2010). Angiotensin I converting enzyme (ACE) inhibitory activity and antihypertensive effect of fermented milk. International Dairy Journal 20, 3–10.
Reyes-Mendez, A., Figueroa-Hernández, C., Melgar-Lalanne, G., Hernández-Sánchez, H., Dávila-Ortiz, G. and Jiménez-Martínez, C. (2015). Producción de péptidos fijadores de calcio y hierro por cepas probióticas de Bacillus subtilis, B. clausii y B. coagulans GBI-30. Revista Mexicana de Ingeniería Química 14, 1–9.
Rojas-Ronquillo, R., Cruz-Guerrero, A., Flores-Nájera, A., Rodríguez-Serrano, G., Gómez-Ruiz, L., Reyes-Grajeda, J.P., Jiménez-Guzmán, J. and García-Garibay, M. (2012). Antithrombotic and angiotensin-converting enzyme inhibitory properties of peptides released from bovine casein by Lactobacillus casei Shirota. International Dairy Journal 26, 147–154.
Saadi, S., Saari, N., Anwar, F., Abdul Hamid, A. and Ghazali, H.M. (2015). Recent advances in food biopeptides: production, biological functionalities and therapeutic applications. Biotechnology Advances 33, 80–116.
Shu, G., Shi, X., Chen, H., Ji, Z.and Meng, J. (2017). Optimization of goat milk with ACE inhibitory peptides fermented by Lactobacillus bulgaricus LB6 using response surface methodology. Molecules 22,(2001),1-9
Soleymanzadeh, N., Mirdamadi, S., Mirzaei, M.and Kianirad, M. (2019). Novel β-casein derived antioxidant and ACE-inhibitory active peptide from camel milk fermented by Leuconostoc lactis PTCC1899: Identification and molecular docking. International Dairy Journal 97, 201–208.
Sun, N., Wu, H., Du, M., Tang, Y., Liu, H., Fu, Y. and Zhu, B. (2016). Food protein-derived calcium chelating peptides: a review. Trends in Food Science and Technology 58, 140–148.
Tagliazucchi, D., Martini, S. and Solieri, L. (2019). Bioprospecting for bioactive peptide production by lactic acid bacteria isolated from fermented dairy food. Fermentation 5, 96,1-34.
Tanasupawat, S., Shida, O., Okada, S. and Komagata, K. (2000). Lactobacillus acidipiscis sp. nov. and Weissella thailandensis sp. nov., isolated from fermented fish in Thailand. International Journal of Systematic and Evolutionary Microbiology 50, 1479–1485. https://doi.org/10.1099/00207713-50-4-1479
Torres-Fuentes, C., Alaiz, M. and Vioque, J. (2012). Iron-chelating activity of chickpea protein hydrolysate peptides. Food Chemistry 134, 1585–1588.
Vasilev, D., Aleksic, B., Tarbuk, A., Dimitrijevic, M., Karabasil, N., Cobanovic, N. and Vasiljevic, N. (2015). Identification of lactic acid bacteria isolated from Serbian traditional fermented sausages Sremski and Lemeski Kulen. Procedia Food Science 5, 300–303.
Wong, P.Y.Y. and Kitts, D.D. (2003). Chemistry of buttermilk solid antioxidant activity. Journal of Dairy Science 86, 1541–1547.
Xiang, H., Sun-Waterhouse, D., Waterhouse, G.I.N., Cui, C. and Ruan, Z. (2019). Fermentation-enabled wellness foods: a fresh perspective. Food Science and Human Wellness, 8, 203–243.
Zotta, T., Piraino, P., Ricciardi, A., McSweeney, P.L.H.and Parente, E. (2006). Proteolysis in model sourdough fermentations. Journal of Agricultural and Food Chemistry 54, 2567–2574.
Published
2020-05-15
How to Cite
Hern´andez-SánchezH., Fajardo-Espinoza, F., Gutiérrez-López, G., Ávila-Reyes, S., Cano-Sarmiento, C., & Figueroa-Hernández, C. (2020). ACE- Inhibitory and metal-binding activity produced during milk fermentation by three probiotic potential LAB strains isolated from Chiapas double cream cheese. Revista Mexicana De Ingeniería Química, 20(1), 97-112. https://doi.org/10.24275/rmiq/Alim1395
Section
Food Engineering

Most read articles by the same author(s)

<< < 1 2 3 > >>