Autolysis in Lactic Acid Bacteria and Its Importance in Cheese Technology

Year 2016, Volume: 14 Issue: 3, 293 - 301, 01.09.2016

Ömer Şimşek Oğuz Gürsoy Selime Hazır Dalca Yusuf Yılmaz

Abstract

Lactic acid bacteria LAB are critically important in cheese technology because of their role in biochemical reactions such as proteolysis, lipolysis and glycolysis during ripening. Like all bacteria, LAB have been also autolyzed by losing their cellular integrity by their own peptidoglycan hydrolase enzymes. As a result of autolysis, cellular enzymes of LAB are released into the cheese matrix. Intracellular microbial enzymes reach to their substrates in a shorter time period because of the early autolysis of cheese related microorganisms starter and non-starter microflora in the beginning stages of a ripening period. Autolysis may accelerate the formation of flavor compounds; therefore, it can shorten the ripening period of cheese production. In addition to accelerating cheese ripening, autolysis has a positive effect on cheese flavor. In this review, the mechanism and properties of autolysis in LAB, its importance in cheese making technology and the determination of starter autolysis in cheeses are presented

Keywords

Lactic acid bacteria, Autolysis, Cheese technology, Starter culture

Laktik Asit Bakterilerinde Otoliz ve Peynir Teknolojisindeki Önemi

Abstract

Laktik asit bakterileri LAB peynir teknolojisinde olgunlaşma için önemli olan proteoliz, lipoliz ve glikoliz gibi biyokimyasal reaksiyonların gerçekleşmesinde kritik bir öneme sahiptir. Tüm bakterilerde olduğu gibi LAB’ler de sahip oldukları peptidoglikan hidrolaz enzimleri ile çeşitli koşullarda hücresel bütünlüklerini kaybederek otolize uğramaktadır. Otoliz sonucunda LAB’lerin hücresel enzimleri açığa çıkmakta ve peynir matriksine salıverilmektedir. Peynir ile ilgili mikroorganizmaların starter ve starter olmayan mikroflora olgunlaşmanın ilk evrelerinde erken otolizi hücre içi mikrobiyal enzimleri substratlarıyla daha kısa sürede buluşturmakta ve bu olay peynirde lezzet bileşiklerinin oluşumunu hızlandırabilmektedir. Dolayısıyla, otoliz peynirlerin olgunlaşma süresini kısaltabilmektedir. Otoliz olgunlaşmayı hızlandırmasının yanı sıra peynir lezzeti üzerine olumlu etkilere de sahiptir. Bu derlemede, LAB’lerde otolizin mekanizması, özellikleri, peynir teknolojisindeki önemi ve peynirlerde starter otolizinin belirlenmesi ile ilgili bilgiler sunulmaktadır

Keywords

Laktik asit bakterileri, Otoliz, Peynir teknolojisi, Starter kültür

References

• De Vuyst, L., Leroy, F., 2007. Bacteriocins from lactic acid bacteria: Production, purification, and food Biotechnol. 13: 194–199. Molecular Microbiol.
• Leroy, F., Verluyten, J., De Vuyst, L., 2006.Functional meat starter cultures for improved sausage fermentation. Int. J. Food Microbiol. 106: 270–285.
• Hannon, J.A., Wilkinson, M.G., Delahunty, C.M., Wallace, J.M., Morrissey, P.A., Beresford, T.P., 2003. Use of autolytic starter systems to accelerate the ripening of Cheddar cheese. Int. Dairy J. 13: 313–323.
• McSweeney, P.L.H., 2004.Biochemistry of cheese ripening. Int. J. Dairy Technol. 57: 127-144.
• Valence, F., Deutsch, S.M., Richoux, R., Gagnaire, V., Lortal, L., 2000. Autolysis and related proteolysis in Swiss cheese for two Lactobacillus helveticus strains. J. Dairy Res. 67: 261–271.
• Beresford, T.P., Fitzsimons, N.A., Brennan, N.L., Cogan, T.M., 2001. Recent advances in cheese microbiology. Int. Dairy J. 11: 259-274.
• Shockman, G. D., Daneo-Moore, L., Kariyama, R., Massidda, O., 1996. Bacterial walls, peptidoglycan hydrolases, autolysins and autolysis. Microb. Drug Resist. 2: 95-98.
• Crouigneau, A.A., Feuillat, M., Guilloux-Benatier, M., 2000. Influence of some factors on autolysis of Oenococcus oeni. Vitis 39:167-171.
• Rolain, T., Bernard, E., Courtin, P., Bron, P.A., Kleerebezem, M., Chapot-Chartier, M.P., Hols, P., 2012. hydrolases for morphogenesis, autolysis, and peptidoglycan plantarum WCFS1. Microbiol. Cell Fact. 11: 137.
• Chapot-Chartier, M., Kulakauskas, S., 2014. Cell Lactobacillus wall structure and functions in lactic acid bacteria. Microbial Cell Factories 13: 1-23.
• Madigan, M.T., Martinko, J.M., 2010. Brock Mikroorganizmaların Biyolojisi, Çökmüş, C., (ed.), 11, Palme Yayıncılık.
• Buist, G., Kok, J., Leenhouts, K.I., Dabrowska, M., Venema, G., Haandrikman, A.l., 1995. Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation. J. Bacteriol. 177: 1554-1563.
• Steen, A., Buist, G., Leenhouts, K.J., El Khattabi, M., Grijpstra, F., Zomer, A.L., Venema, G., Kuipers, O.P., Kok, J., 2003. Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J. Biol. Chem. 278: 23874–23881.
• Steen, A., Buist, G., Horsburgh, G.J., Venema, G., Kuipers, O.P., Foster, S.J., Kok, J., 2005. AcmA of Lactococcus lactis is an N-acetylglucosaminidase with an optimal number of LysM domains for proper functioning”. FEBS J. 272: 2854–2868.
• Claes, I.J., Schoofs, G., Regulski, K., Courtin, P., Chapot-Chartier, M.P., Rolain, T., 2012. Genetic and biochemical characterization of the cell wall hydrolase activity of the major secreted protein of Lactobacillus rhamnosus GG. PLoS One 7: 31588.
• Regulski, K., Courtin, P., Meyrand, M., Claes, I.J., Lebeer, S., Vanderleyden, J., 2012. Analysis of the peptidoglycan Lactobacillus casei and characterization of the major gamma-D-Glutamyl-L-Lysylendopeptidase. PLoS One 7: 32301. complement of
• Layec, S., Decaris, B., Leblond-Bourget, N., 2008. Diversity of Firmicutes peptidoglycan hydrolases and specificities of those involved in daughter cell separation. Res. Microbiol. 159: 507–515.
• Redko, Y., Courtin, P., Mezange, C., Huard, C., Chapot-Chartier, M.P., 2007. Lactococcus lactis gene yjgB encodes a gamma-D-glutaminyl-L- lysylendopeptidase peptidoglycan. Appl. Environ. Microbiol. 73: 5825– 5831. which hydrolyzes
• El-Kholy, W., El-Soda, M., Ezzat, N., El Shafei, H., 1998. Autolysis and intracellular enzyme release from cheese related dairy lactobacilli. Lait 78: 439- 452.
• Kenny, O., FitzGerald, R.J., O’Cuinn, G., Beresford, T., Jordan, K., 2006. Autolysis of selected Lactobacillus helveticus adjunct strains during cheddar cheese ripening. Int. Dairy J. 16: 797-804.
• Lortal, S., Chapot-Chartier, M.P., 2005. Role, mechanisms and control of lactic acid bacteria lysis in cheese. Int. Dairy. J. 15: 857–871.
• Poquet, I., Saint, V., Seznec, E., Simoes, N., Bolotin, A., Gruss, A., 2000. HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing. Mol. Microbiol. 35: 1042–1051.
• Smith, T.J., Blackman, S.A., Foster, S.J., 2000. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiol. 146: 249–262.
• Bie, R., Sjöström, G., 1975. Autolytic properties of some lactic acid bacteria used in cheese production. Part II- Experiments with fluid substrates and cheese. Milchwissenschaft 30: 739- 747.
• Dako, E., El-Soda, M., Vuillemard, J.C., Simard, Autolytic R.E., aminopeptidase activities of lactic acid bacteria. Food Res. Int. 28: 503-509. properties and
• Boutrou, R., Sepulchre, A., Pitel, G., Durier, C., Vassal, L., Gripon, J.C., Monnet, V., 1998. Lactococcal lysis and curd proteolysis: two predictable events important for the development of cheese flavour. Int. Dairy J. 8: 609-616. [27] Çıbık, R.
• Chapot-Chartier, P., 2004. Characterisation
• Lactobacillus pentosus. Lett. Appl. Microbiol. 38: 459-463. enzymes in
• Kozáková, D., Solich, K., Ondrácková I., Sviráková, E., Plocková, M., 2010. Effect of some environmental factors on autolysis of lactococci used for cheese production. J. Food Nut. Res. 49: 1-9.
• Nunez, J.R., Medrano, R.R., Moorillon, G.V.N., Mendez, N.G., 2011. Effect of pH and salt gradient on the autolysis of Lactococcus lactis strains. Brazil. J. Microbiol. 42: 1495-1499.
• Lortal, S., Rousseau, M., Boyaval, P., van Heijenoort, J., 1991. Cell wall and autoIytic system of Lactobacillus helveticus ATCC 12046. J. Gen Microbiol. 137:549-559.
• Ostlie, H.M., Vegarud, G., Langsrud, T., 1995. Autolysis of lactococci: detection of lytic enzymes by polyacrylamide gel electrophoresis and characterization in buffer systems. Appl. Environ. Microbiol. 10: 3598-3603.
• Higgins, M.L., Coyette, J., Shockman, G.D., 1973. Sites of cellular autolysis in Lactobacillus acidophilus. J. Bacteriol. 116: 1375-1382.
• Terzaghi, B.E., Sandine, W.E., 1975. Improved medium for lactic streptococci and their bacteriophages. Appl. Microbiol. 29: 807-813.
• Oumer, A., Gaya, P., Fernandez-Garsia, E., Mariaca, R., Gadre, S., Medina, M., Nunez, M., 2001. Proteolysis and formation of volatile compounds in cheese manufactured with a bacteriocin-producing adjunct culture. J. Dairy Res. 68: 1117-1219.
• Crow, V.L., Martley, F.G., Coolbear, T., Roundhill, S.J., 1995. The influence of phage assisted lysis of Lactococcus lactis subsp. lactis ML8 on Cheddar cheese ripening. Int. Dairy J. 5: 451-472.
• Lepeuple, A.S., Van Gemert, E., Chapot-Chartier, M.-P., 1998. Analysis of the bacteriolytic enzymes of the autolytic Lactococcus lactis subsp. cremoris strain AM2 by renaturing polyacrylamide gel electrophoresis: identification of a prophage encoded enzyme. Appl. and Environ. Microbiol. 65: 4142–4148.
• Meijer, W., Dobbelaar, C., Hugenholtz, J., 1998. Thermo inducible lysis in Lactococcus lactis subsp. cremoris SK110: Implications for cheese ripening. Int. Dairy J. 8: 275–280.
• Law, B.A., 2001. Controlled and accelerated cheese ripening: the research base for new technologies. Int. Dairy J. 11: 383-398.
• El Soda, M., 1993. The role of lactic acid bacteria in accelerated cheese ripening. FEMS Microbiol. Rev. 12: 239-252.
• Deutsch, S.M., Neveu, A., Guezenec, S., Ritzenthaler, P., Lortal, S., 2003. Early lysis of Lactobacillus helveticus CNRZ 303 in Swiss cheese is not prophage-related. Int. J. Food Microbiol. 81: 147-157.
• Hannon, J.A., Kilcawley, K.N., Wilkinson, M.G., Delahunty, C.M., Beresford, T.P., 2007. Flavour precursor development in Cheddar cheese due to lactococcal starters and the presence and lysis of Lactobacillus helveticus. Int. Dairy J. 17: 316-327.
• Crow, V.L., Coolbear, T., Gopal, P.K., Martley, F.G., McKay, L.L., Riepe, H., 1995. The role of autolysis of lactic acid bacteria in the ripening of cheese. Int. Dairy J. 5: 855-875.
• Lazzi, C., Povolo, M., Locci, F., Bernini, V., Neviani, E., Gatti, M., 2016. Can the development and autolysis of lactic acid bacteria influence the cheese volatile fraction? The case of Grana Padano. Int. J. Food. Microbiol. 233: 20-28.
• Bozoudi, D., Kotzamanidis, C., Hatzikamari, M., Tzanetakis, N., Menexes, G., Litopoulou-Tzanetaki, E., 2015. A comparison for acid production, proteolysis, autolysis and inhibitory properties of lactic acid bacteria from fresh and mature Feta PDO Greek cheese, made at three different mountainous areas. Int. J. Food Microbiol. 200: 87- 96.
• Collins, Y.F., McSweeney, P.L.H., Wilkinson, M.G., 2003. Evidence of a relationship between autolysis of starter bacteria and lipolysis in Cheddar cheese during ripening. J. Dairy Res. 70(1): 105-113.
• Bourdat-Deschamps, M., Le Bars, D., Yvon, M., Chapot-Chartier, M.-P., 2004. Autolysis of Lactobaccillus lactis AM2 stimulates the formation of certain aroma compounds from amino acids in a cheese model. Int. Dairy J. 14: 791-800.
• Wilkinson, M.G., Guinee, T.P., O’Callaghan, D.M., Fox, P.F., 1994. Autolysis and proteolysis in different strains of starter bacteria during Cheddar cheese ripening. J. Dairy Res. 61(2): 249-262.
• Sondergaard, L., Ryssel, M., Svendsen, C., Hoier, E., Andersen, U., Hammershoj, M., Moller, J.R., Arneborg, N., Jespersen, L., 2015. Impact of NaCl reduction in Danish semi-hard Samsoe cheeses on proliferation and autolysis of DL-starter cultures. Int. J. Food Microbiol. 213: 59-70.
• Rulikowska, A., Kilcawley, K.N., Doolan, I.A., Alonso-Gomez, M., Nongonierma, A.B., Hannon, J.A., Wilkinson, M.G., 2013. The impact of reduced sodium chloride content on Cheddar cheese quality. Int. Dairy J. 28: 45-55.
• Moller, K.K., Rattray, F.P., Bredie, W.L.P., Hoier, E., Ardö, Y., 2013. Physicochemical and sensory characterization of Cheddar cheese with variable NaCl levels and equal moisture content. J. Dairy Sci. 96: 1953-1971.
• Wilkinson, M.G., Guinee, T.P., Fox, P.F., 1994. Factors which may influence the determination of autolysis of starter bacteria during Cheddar cheese ripening. Int. Dairy J. 4: 141-160.
• Crow, V.L., Coolbear, T., Holland, R., Pritchard, G.G., Martley, F.G., 1993. Starters as finishers: starter properties relevant to cheese ripening. Int. Dairy J. 3: 423-460.
• Urbach, G., 1995. Contribution of lactic acid bacteria to flavour compound formation in dairy products. Int. Dairy J. 5: 877-903.
• O’Donovan, C.M., Wilkinson, M.G., Guinee, T.M., Fox, P.F., 1996. An investigation of the autolytic properties of three lactococcal strains during cheese ripening. Int. Dairy J. 6: 1149-1165.
• Krishna, B.M., Dutta, S.M., 1976. Studies on the autolytic changes in S. cremoris under starvation conditions. Milchwissenschaft 31: 741-744.
• El Soda, M., Farkye, N., Vuillemard, R.E., Simard, R.E., Olson, N.F., Kholy, W., Dako, E., Medrano, E., Gaber, M., Lim, L., 1995. Autolysis of lactic acid bacteria: impact on flavour development in cheese. In: Food Flavors: Generation, Analysis and Process Influence, G. Charalambous (Ed.), Elsevier Science B.V., Amsterdam, pp: 2205-2223.