Changes in Biochemical Properties during Ripening Process of Swiss-Type Cheeses Produced with Different Lactobacillus helveticus Strains

Document Type : Original Research

Authors
1 Department of Plant Food Technology and Gastronomy, Faculty of Food Science and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland.
2 Department of Biotechnology, Microbiology and Human Nutrition, Faculty of Food Science and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland.
3 Department of Epizootiology and Clinic of Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences in Lublin Akademicka 13, 20-950 Lublin, Poland.
Abstract
The presence of various biotypes of Lactobacillus helveticus seems to be related to the specificity of the ecosystem, which is one of the main determinants of the unique features of cheese produced in particular regions. So far, it has been proved that even biotypes isolated from the same niche differ significantly from each other and many features exhibited by these bacteria are strain-dependent. Therefore, the new strains of L. helveticus T104 and T105 (isolated from traditionally fermented Polish dairy product) were applied in the production of ripened cheeses due to their potential health-promoting properties. We determined changes in fat, fatty acids, protein, amino acids, and some physicochemical characteristics, e.g. antioxidant properties of the produced cheeses (in three stages of ripening). Tricine-SDS-PAGE and MALDI-TOF MS analysis showed some differences in protein and peptide profiles. Final products obtained using L. helveticus T105 exhibited the greatest amount of free amino acids, which are important precursor of cheese aroma and flavor. The research indicated that the tested strains could be applied in the manufacture of cheeses. Moreover, the cheese produced using the said strain exhibited the highest free radical scavenging capacity (88.89% after pre-ripening and 92.74% in the final products) even in comparison to the control cheese variant produced using the industrial L. helveticus strain. Obtained findings indicate that the tested strains exhibit technological and functional potential that provide a reference for further study and might contribute to the development of functional food products with novel, valuable characteristics.

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References
Adaszek, Ł., Banach T., Bartnicki, M., Winiarczyk, D., Łyp, P. and Winiarczyk, S. 2014. Application the mass spectrometry MALDI-TOF technique for detection of Babesia canis canis infection in dogs. Parasitol. Res., 113: 4293 – 4295.
Aminifar, M., Hamedi, M., Emam-Djomeh, Z. and Mehdinia, A. 2014. Investigation on proteolysis and formation of volatile compounds of Lighvan cheese during ripening J. Food Sci. Technol., 51: 2454 – 2462.
AOAC 1995. Official Methods of Analysis. 16th. Edn. AOAC. International. Gaithersburg. MD.
AOAC 2000. International Official Methods of Analysis. 17th. Edn. AOAC International. Gaithersburg. MD
Apostolidis, E., Kwon, Y. I. and Shetty, K. 2007. Inhibitory potential of herb fruit and fungal-enriched cheese against key enzymes linked to type 2 diabetes and hypertension. Innov. Food Sci. & Emerg. Technol., 8: 46 – 54.
Celik, O. F. and Tarakci, Z. 2017. The effects of starter cultures on chemical, biochemical and sensory properties of low‐fat Tulum cheeses during ripening. Int. J.
Chr. Hansen 2002. Emmental Cheese Types First revised edition. 1-23 Emmenthal-1rev_0302.doc/Apr 2002/1:23
Christiansen, J.K., Hughes, J.E., Welker, D.L., Rodríguez, B.T., Steele, J.L. and Broadbent, J.R. 2008. Phenotypic and genotypic analysis of amino acid auxotrophy in Lactobacillus helveticus CNRZ 32. Appl. Environ Microbiol., 74: 416 – 423.
Curioni, P. M. G. and Bosset, J. O. 2002. Key odorants in various cheese types as determined by gas chromatography-olfactometry. Int. Dairy J., 12: 959 – 984.
Domagała, J., Pluta-Kubica, A. and Pustkowiak, H. 2013. Changes in Conjugated Linoleic Acid Content in Emmental-Type Cheese during Manufacturing. Czech J. Food Sci., 31: 432 – 437.
EN 15505:2008 Foodstuffs. Determination of trace elements. Determination of sodium and magnesium by flame atomic absorption spectrometry (AAS) after microwave digestion
European Commission 2015. Prospects for Agricultural Markets and Income in the EU 2015–2025. Directorate-General for Agriculture and Rural Development. Brussels. Available from: <http://ec.europa.eu/agriculture/markets-and-prices/medium-term-outlook/index_en.htm#about>.
Fenelon, M. A., Beresford, T. P. and Guinee, T. P. 2002. Comparison of different bacterial culture systems for the production of reduced-fat Cheddar cheese. Int. J. Dairy Technol., 55:194 – 203.
Fortina, M.G., Nicastro, G., Carminati, D., Neviani, E. and Manachini, P.L. 1998. Lactobacillus helveticus heterogeneity in natural cheese starters: The diversity in phenotypic characteristics. J. Appl. Microbiol,. 84: 72 – 80.
Gagnaire, V., Piot, M., Camier, B., C. Vissers J. P., Jan, G. and Léonil, J. 2004. Survey of bacterial proteins released in cheese: A proteomic approach. Int. J. Food Microbiol., 94: 185 – 201.
Ganesan, B., Weimer, B. C., Qian, M.C. and Burbank, H. M. 2007. Compounds associated with cheese flavor. In: Improving the flavour of cheese. (Ed): Weimer, B.C. CRC Press, Boca Raton, pp. 26 – 51.
Gatti, M., Bottari, B., Lazzi, C., Neviani, E. and Mucchetti, G. 2014. Microbial evolution in raw- milk, long-ripened cheeses produced using undefined natural whey starters. J. Dairy Sci., 97: 573 – 591.
Griffiths, M. W. and Tellez, A. M. 2013. Lactobacillus helveticus: the proteolytic system. Front. Microbiol., 30: 1-9. doi: 10.3389/fmicb.2013.00030.
Gupta, A., Mann, B., Kumar, R. and Sangwan, R. B. 2009. Antioxidant activity of Cheddar cheeses at different stages of ripening. Int. J. Dairy Technol. 62: 339 – 347.
Hannon, J. A., Kilcawley, K. N., Wilkinson, M. G., Delahunty, C. M. and Beresford, T. P. 2007. Flavor precursor development in Cheddar cheese due to lactococcal starters and the presence and lysis of Lactobacillus helveticus. Int. Dairy J., 17: 316 – 327.
Hébert, E. M., Mamone, Picariello, G., Raya, G.R. R., De Giori, G. S., Ferranti, P. and Addeo, F. 2008. Characterization of the pattern of αs1– and β- casein breakdown and release of a bioactive peptide by a cell envelope proteinase from Lactobacillus delbrueckii subsp. lactis CRL 581. Appl. Environ Microbiol.,74: 3682 – 3689.
Helinck, S., Bars, D. L., Moreau, D. and Yvon, M. 2004. Ability of thermophilic lactic acid bacteria to produce aroma compounds from amino acids. App. Environ. Microbiol., 70: 3855 – 3681.
Hernandez, L. B., Miralles, B., Amigo, L., Ramos, M. and Recio, I. 2005. Identification of antioxidant and ACE-inhibitory peptides in fermented milk. J. Sci. Food Agric., 85: 1041 – 1048.
Hill, A. R. 2007. Physical factors affecting flavour of cheese. In: Improving the flavour of cheese. (Ed.): Weimer, B.C. CRC Press, Boca Raton, pp. 252 – 283.
ISO 12966-4: 2015 Animal and vegetable fats and oils - Gas chromatography of fatty acid methyl esters - Part 4: Determination by capillary gas chromatography.
Klein, N., Maillard, M. B., Thierry, A. and Lortal, S. 2001. Conversion of amino acids into aroma compounds by cell-free extracts of Lactobacillus helveticus. J. Appl. Microbiol., 91: 404 – 411.
Lopez, C., Maillard M. B., Briard-Bion, V., Camier, B. and Hannon, J.A. 2006. Lipolysis during ripening of Emmental cheese considering organization of fat and preferential localization of bacteria, J. Agric. Food Chem., 54: 5855 – 5867.
Mangia, N. P., Murgia, M. A., Garau, G. and Deiana, P. 2011. Microbiological and Physicochemical Properties of Pecorino Romano Cheese Produced Using a Selected Starter Culture. J. Agr. Sci. Tech., 13: 585 – 600.
Mcsweeney, P. L. H. 2004. Biochemistry of cheese ripening. Int. J. Dairy Technol., 57: 127 – 144.
Nielsen, M. S., Martinussen, T., Flambard, B., Sørensen, K. I. and Otte, J. 2009. Peptide profiles and angiotensin-I-converting enzyme inhibitory activity of fermented milk products: effect of bacterial strain, fermentation PH, and storage time. Int. Dairy J., 19: 155 – 165.
Perna, I., Intaglietta, A., Simonetti, E. and Gambacort, A. 2015. Short communication: effect of genetic type on antioxidant activity of Caciocavallo cheese during ripening J. Dairy Sci. 98: 3690 – 3694.
Petersen, M. A., Kristensen, H. T., Bakman, M., Varming, C., Jensen, M. E. P. and Ardö, Y.M. 2010. Aroma formation in a cheese model system by different Lactobacillus helveticus strains. In: Expression of multidisciplinary flavour science: proceedings of the 12th Weurman Symposium, Switzerland 2008, (Eds): Blank, I., Wüst, M. and Yeretzian, C., Zurich University of Applied Sciences, pp. 367 – 370.
Pihlanto, A. and Mäkinen, S. 2013. Antihypertensive properties of plant protein derived peptides. In: Bioactive Food Peptides in Health and Disease. (Eds.): Hernández-Ledesma, B. and Hsieh, C.C., InTech, Rijeka, pp. 144 – 182.
Pritchard, S.R., Phillips, M. and Kailasapathy, K. 2010. Identification of bioactive peptides in commercial Cheddar cheese. Food Res. Int., 43: 1545 – 1548.
Sadat-Mekmene, L., Jardin, J., Corre, C., Mollé, D., Richoux, R., Delage, M.M., Lortal, S. and Gagnaire, V. 2011. Simultaneous presence of PrtH and PrtH2 proteinases in Lactobacillus helveticus strains improves breakdown of the pure αs1-Casein. Appl. Environ Microbiol., 77: 179 – 186.
Saiga, A., Tanabe, S. and Nishimura, T. 2003. Antioxidant activity of peptides obtained from porcine myofibrillar proteins by protease treatment. J. Agric. Food Chem., 51: 3661 – 3667.
Schägger, H. and Von Jagow G. 1987. Tricine-sodium dodedyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368 – 379.
Sheenan, J. J., Fenelon, M. A., Wilkinson, M. G. and McSweeney, P. L. H. 2007. Effect of cook temperature on tarter and non-starter lactic acid bacteria viability. cheese composition and ripening indices of a semi-hard cheese manufactured using thermophilic cultures. Int. Dairy J., 17: 704 – 716.
Skrzypczak, K., Gustaw, W. and Waśko, A. 2015. Health-promoting properties exhibited by Lactobacillus helveticus strains. Acta Biochim. Pol., 64(4): 713–720.
Skrzypczak, K., Gustaw, W., Jabłońska-Ryś, E., Michalak-Majewska, M., Sławińska, A., Radzki, W., Gustaw, K. and Waśko, A. 2017a. Antioxidative properties of milk protein preparations fermented by Polish strains of Lactobacillus helveticus. Acta Sci. Pol. Technol. Aliment., 16(2):199 – 207.
Skrzypczak, K., Gustaw, W., Szwajgier, D., Fornal, E. and Waśko, A. 2017b. κ-Casein as a source of short-chain bioactive peptides generated by Lactobacillus helveticus JFST, 54(11): 3679 – 3688.
Skrzypczak, K.W., Gustaw, W.Z. and Waśko, A.D. 2018. Distribution of Cell Envelope Proteinases Genes among Polish Strains of Lactobacillus helveticus. Pol J Microbiol., 67(2): 203-21.
Tunick, M. H. 2000. Rheology of dairy foods that gel, stretch and fracture. J. Dairy Sci. 83: 1892 – 1898.
Türkoglu, H. 2011. Free Fatty Acid Composition and Sensory Characteristics of Orgu cheese. Sci. Res. Essays, 7: 1555 – 1560.
Virtanen, T., Pihlanto, A., Akkanen, S. and Korhonen, H. 2007. Development of antioxidant activity in milk whey during fermentation with lactic acid bacteria. J. Appl. Microbiol., 102: 106 – 115.
Waśko, A., Szwajgier, D. and Polak-Berecka, M. 2014. The role of ferulic acid esterase in the growth of Lactobacillus helveticus in the presence of phenolic acids and their derivatives. Euro. Food Res. Technol., 238: 299 – 236.
White, S. R., Broadbent, J. R., Oberg, C. J. and McMahon, D. J. 2003. Effect of Lactobacillus helveticus and Propionibacterium freudenrichii ssp. shermanii combinations on propensity for split defect in Swiss Cheese. J. Dairy Sci., 86: 719 – 727.
Widyastuti, Y., Lisdiyant, P. and Tisnadjaja D. 2014. Role of Lactobacillus helveticus on flavor formation in Cheese: Amino Acid Metabolism. Ann. Bogor., 18: 1 – 11.
Yvon, M. and Rijnen, L. 2001. Cheese ripening and technology: Cheese flavour formation by amino acid catabolism. Int. Dairy J., 11: 185 – 201.