Biosynthesis and role of 3-methylbutanal in cheese by lactic acid bacteria: Major metabolic pathways, enzymes involved, and strategies for control

References

• Afzal, M. I., Boulahya, K. A., Paris, C., Delaunay, S. and Cailliez-Grimal, C. (2013a). Effect of oxygen on the biosynthesis of flavor compound 3-methylbutanal from leucine catabolism during batch culture in Carnobacterium maltaromaticum LMA 28. J. Dairy Sci. 96:352–359.
   PubMed Web of Science ®Google Scholar
• Afzal, M. I., Delaunay, S., Paris, C., Borges, F., Revol-Junelles, A. M. and Cailliez-Grimal, C. (2012). Identification of metabolic pathways involved in the biosynthesis of flavor compound 3-methylbutanal from leucine catabolism by Carnobacterium maltaromaticum LMA 28. Int. J. Food Microbiol. 157:332–339.
   PubMed Web of Science ®Google Scholar
• Afzal, M. I., Gonzalez, C. C., Lhomme, E., Ali, N. K., Payot, S., Burgain, J., Gaiani, C., Borges, F., Revol-Junelles, A. M., Delaunay, S. and Cailliez-Grimal, C. (2013b). Characterization of Carnobacterium maltaromaticum LMA 28 for its positive technological role in soft cheese making. Food Microbiol. 36:223–230.
   PubMed Web of Science ®Google Scholar
• Afzal, M. I., Jacquet, T., Delaunay, S., Borges, F., Milliere, J. B., Revol-Junelles, A. M. and Cailliez-Grimal, C. (2010). Carnobacterium maltaromaticum: Identification, isolation tools, ecology and technological aspects in dairy products. Food Microbiol. 27:573–579.
   PubMed Web of Science ®Google Scholar
• Amárita, F., de la Plaza, M., Fernández de Palencia, P., Requena, T. and Peláez, C. (2006). Cooperation between wild lactococcal strains for cheese aroma formation. Food Chem. 94:240–246.
   Web of Science ®Google Scholar
• Ardo, Y. (2006). Flavour formation by amino acid catabolism. Biotechnol. Adv. 24:238–242.
   PubMed Web of Science ®Google Scholar
• Avsar, Y. K., Karagul-Yuceer, Y., Drake, M. A., Singh, T. K., Yoon, Y. and Cadwallader, K. R. (2004). Characterization of nutty flavor in cheddar cheese. J. Dairy Sci. 87:1999–2010.
   PubMed Web of Science ®Google Scholar
• Ayad, E. H. E., Awad, S., El Attar, A., de Jong, C. and El-Soda, M. (2004a). Characterisation of Egyptian Ras cheese. 2. Flavour formation. Food Chem. 86:553–561.
   Web of Science ®Google Scholar
• Ayad, E. H. E., Nashat, S., El-Sadek, N., Metwaly, H. and El-Soda, M. (2004b). Selection of wild lactic acid bacteria isolated from traditional Egyptian dairy products according to production and technological criteria. Food Microbiol. 21:715–725.
   Web of Science ®Google Scholar
• Ayad, E. H. E., Verheul, A., Bruinenberg, P., Wouters, J. T. M. and Smit, G. (2003). Starter culture development for improving the flavour of Proosdij-type cheese. Int. Dairy J. 13:159–168.
   Web of Science ®Google Scholar
• Ayad, E. H. E., Verheul, A., De Jong, C., Wouters, J. T. M. and Smit, G. (1999). Flavour forming abilities and amino acid requirements of Lactococcus lactis strains isolated from artisanal and non-dairy origin. Int. Dairy J. 9:725–735.
   Web of Science ®Google Scholar
• Ayad, E. H. E., Verheul, A., Engels, W. J., Wouters, J. T. and Smit, G. (2001). Enhanced flavour formation by combination of selected lactococci from industrial and artisanal origin with focus on completion of a metabolic pathway. J. Appl. Microbiol. 90:59–67.
   PubMed Web of Science ®Google Scholar
• Banks, J. M., Yvon, M., Gripon, J. C., de la Fuente, M. A., Brechany, E. Y., Williams, A. G. and Muir, D. D. (2001). Enhancement of amino acid catabolism in Cheddar cheese using α-ketoglutarate: Amino acid degradation in relation to volatile compounds and aroma character. Int. Dairy J. 11:235–243.
   Web of Science ®Google Scholar
• Barbieri, G., Bolzoni, L., Careri, M., Mangia, A., Parolari, G., Spagnoli, S. and Virgili, R. (1994). Study of the volatile fraction of Parmesan cheese. J. Agric. Food Chem. 42:1170–1176.
   Web of Science ®Google Scholar
• Bergamini, C. V., Peralta, G. H., Milesi, M. M. and Hynes, E. R. (2013). Growth, survival, and peptidolytic activity of Lactobacillus plantarum I91 in a hard-cheese model. J. Dairy Sci. 96:5465–5476.
   PubMed Web of Science ®Google Scholar
• Bintsis, T. and Robinson, R. K. (2004). A study of the effects of adjunct cultures on the aroma compounds of Feta-type cheese. Food Chem. 88:435–441.
   Web of Science ®Google Scholar
• Bosset, J. O. and Gauch, R. (1993). Comparison of the volatile flavour compounds of six European ‘AOC’ cheeses by using a new dynamic headspace GC-MS method. Int. Dairy J. 3:359–377.
   Web of Science ®Google Scholar
• Boutrou, R. and Guéguen, M. (2005). Interests in Geotrichum candidum for cheese technology. Int. J. Food Microbiol. 102:1–20.
   PubMed Web of Science ®Google Scholar
• Brandsma, J. B., Floris, E., Dijkstra, A. R. D., Rijnen, L., Wouters, J. A. and Meijer, W. C. (2008). Natural diversity of aminotransferases and dehydrogenase activity in a large collection of Lactococcus lactis strains. Int. Dairy J. 18:1103–1108.
   Web of Science ®Google Scholar
• Broadbent, J. R., Brighton, C., McMahon, D. J., Farkye, N. Y., Johnson, M. E. and Steele, J. L. (2013). Microbiology of Cheddar cheese made with different fat contents using a Lactococcus lactis single-strain starter. J. Dairy Sci. 96:4212–4222.
   PubMed Web of Science ®Google Scholar
• Caldeo, V. and McSweeney, P. L. H. (2012). Changes in oxidation-reduction potential during the simulated manufacture of different cheese varieties. Int. Dairy J. 25:16–20.
   Web of Science ®Google Scholar
• Centeno, J. A., Tomillo, F. J., Fernández-García, E., Gaya, P. and Nuñez, M. (2002). Effect of wild strains of Lactococcus lactis on the volatile profile and the sensory characteristics of Ewes' raw milk cheese. J. Dairy Sci. 85:3164–3172.
   PubMed Web of Science ®Google Scholar
• De Cadinanos, L. P., Garcia-Cayuela, T., Yvon, M., Martinez-Cuesta, M. C., Pelaez, C. and Requena, T. (2013). Inactivation of the panE gene in Lactococcus lactis enhances formation of cheese aroma compounds. Appl. Environ. Microbiol. 79:3503–3506.
   PubMed Web of Science ®Google Scholar
• Deetae, P., Bonnarme, P., Spinnler, H. E. and Helinck, S. (2007). Production of volatile aroma compounds by bacterial strains isolated from different surface-ripened French cheeses. Appl. Microbiol. Biotechnol. 76:1161–1171.
   PubMed Web of Science ®Google Scholar
• Deetae, P., Saint-Eve, A., Spinnler, H. E. and Helinck, S. (2011). Critical effect of oxygen on aroma compound production by Proteus vulgaris. Food Chem. 126:134–139.
   Web of Science ®Google Scholar
• Deetae, P., Spinnler, H. E., Bonnarme, P. and Helinck, S. (2009). Growth and aroma contribution of Microbacterium foliorum, Proteus vulgaris and Psychrobacter sp. during ripening in a cheese model medium. Appl. Microbiol. Biotechnol. 82:169–177.
   PubMed Web of Science ®Google Scholar
• De la Plaza, M., Fernández de Palencia, P., Peláez, C. and Requena, T. (2004). Biochemical and molecular characterization of α-ketoisovalerate decarboxylase, an enzyme involved in the formation of aldehydes from amino acids by Lactococcus lactis. FEMS Microbiol. Lett. 238:367–374.
   PubMed Web of Science ®Google Scholar
• Engels, W. J. M., Dekker, R., de Jong, C., Neeter, R. and Visser, S. (1997). A comparative study of volatile compounds in the water-soluble fraction of various types of ripened cheese. Int. Dairy J. 7:255–263.
   Web of Science ®Google Scholar
• Fernández de Palencia, P., De la Plaza, M., Amárita, F., Requena, T. and Peláez, C. (2006). Diversity of amino acid converting enzymes in wild lactic acid bacteria. Enzyme Microb. Technol. 38:88–93.
   Web of Science ®Google Scholar
• Fernández de Palencia, P., De la Plaza, M., Mohedano, M. L., Martínez-Cuesta, M. C., Requena, T., López, P. and Peláez, C. (2004). Enhancement of 2-methylbutanal formation in cheese by using a fluorescently tagged Lacticin 3147 producing Lactococcus lactis strain. Int. J. Food Microbiol. 93:335–347.
   PubMed Web of Science ®Google Scholar
• Freiding, S., Ehrmann, M. A. and Vogel, R. F. (2012). Comparison of different IlvE aminotransferases in Lactobacillus sakei and investigation of their contribution to aroma formation from branched chain amino acids. Food Microbiol. 29:205–214.
   PubMed Web of Science ®Google Scholar
• García-Cayuela, T., Gómez de Cadiñanos, L. P., Peláez, C. and Requena, T. (2012). Expression in Lactococcus lactis of functional genes related to amino acid catabolism and cheese aroma formation is influenced by branched chain amino acids. Int. J. Food Microbiol. 159:207–213.
   PubMed Web of Science ®Google Scholar
• Garde, S., Ávila, M., Fernández-García, E., Medina, M. and Nuñez, M. (2007). Volatile compounds and aroma of Hispánico cheese manufactured using lacticin 481-producing Lactococcus lactis subsp. lactis INIA 639 as an adjunct culture. Int. Dairy J. 17:717–726.
   Web of Science ®Google Scholar
• Gkatzionis, K., Hewson, L., Hollowood, T., Hort, J., Dodd, C. E. R. and Linforth, R. S. T. (2013). Effect of Yarrowia lipolytica on blue cheese odour development: Flash profile sensory evaluation of microbiological models and cheeses. Int. Dairy J. 30:8–13.
   Web of Science ®Google Scholar
• Hannon, J. A., Kilcawley, K. N., Wilkinson, M. G., Delahunty, C. M. and Beresford, T. P. (2006). Production of ingredient-type cheddar cheese with accelerated flavor development by addition of enzyme-modified cheese powder. J. Dairy Sci. 89:3749–3762.
   PubMed Web of Science ®Google Scholar
• Helinck, S., Le Bars, D., Moreau, D. and Yvon, M. (2004). Ability of thermophilic lactic acid bacteria to produce aroma compounds from amino acids. Appl. Environ. Microbiol. 70:3855–3861.
   PubMed Web of Science ®Google Scholar
• Hou, J., Hannon, J. A., McSweeney, P. L. H., Beresford, T. P. and Guinee, T. P. (2014). Effect of curd washing on cheese proteolysis, texture, volatile compounds, and sensory grading in full fat Cheddar cheese. Int. Dairy J. 34:190–198.
   Web of Science ®Google Scholar
• Irigoyen, A., Ortigosa, M., Juansaras, I., Oneca, M. and Torre, P. (2007). Influence of an adjunct culture of Lactobacillus on the free amino acids and volatile compounds in a Roncal-type ewe's-milk cheese. Food Chem. 100:71–80.
   Web of Science ®Google Scholar
• Irlinger, F., Yung, S. A., Sarthou, A. S., Delbes-Paus, C., Montel, M. C., Coton, E., Coton, M. and Helinck, S. (2012). Ecological and aromatic impact of two Gram-negative bacteria (Psychrobacter celer and Hafnia alvei) inoculated as part of the whole microbial community of an experimental smear soft cheese. Int. J. Food Microbiol. 153:332–338.
   PubMed Web of Science ®Google Scholar
• Jackson, H. W. and Morgan, M. E. (1954). Identity and origin of the malty aroma substance from milk cultures of Streptococcus lactis var. maltigenes. J. Dairy Sci. 37:1316–1324.
   Web of Science ®Google Scholar
• Kaminarides, S., Nestoratos, K. and Massouras, T. (2013). Effect of added milk and cream on the physicochemical, rheological and volatile compounds of Greek whey cheeses. Small Rumin. Res. 113:446–453.
   Web of Science ®Google Scholar
• Kieronczyk, A., Cachon, R., Feron, G. and Yvon, M. (2006). Addition of oxidizing or reducing agents to the reaction medium influences amino acid conversion to aroma compounds by Lactococcus lactis. J. Appl. Microbiol. 101:1114–1122.
   PubMed Web of Science ®Google Scholar
• Kieronczyk, A., Skeie, S., Langsrud, T., Le Bars, D. and Yvon, M. (2004). The nature of aroma compounds produced in a cheese model by glutamate dehydrogenase positive Lactobacillus INF15D depends on its relative aminotransferase activities towards the different amino acids. Int. Dairy J. 14:227–235.
   Web of Science ®Google Scholar
• Larrouture-Thiveyrat, C. and Montel, M. C. (2003). Effects of environmental factors on leucine catabolism by Carnobacterium piscicola. Int. J. Food Microbiol. 81:177–184.
   PubMed Web of Science ®Google Scholar
• Liu, M., Nauta, A., Francke, C. and Siezen, R. J. (2008). Comparative genomics of enzymes in flavor-forming pathways from amino acids in lactic acid bacteria. Appl. Environ. Microbiol. 74:4590–4600.
   PubMed Web of Science ®Google Scholar
• MacLeod, P. and Morgan, M. E. (1955). Leucine metabolism of Streptococcus lactis var. maltigenes. I. Conversion of alpha-ketoisocaproic acid to leucine and 3-methylbutanal. J. Dairy Sci. 38:1208–1214.
   Web of Science ®Google Scholar
• Martínez-Cuesta, C., Requena, T. and Peláez, C. (2002). Effect of bacteriocin-induced cell damage on the branched-chain amino acid transamination by Lactococcus lactis. FEMS Microbiol. Lett. 217:109–113.
   PubMed Web of Science ®Google Scholar
• Martínez-Cuesta, M. C., Requena, T. and Peláez, C. (2006). Cell membrane damage induced by lacticin 3147 enhances aldehyde formation in Lactococcus lactis IFPL730. Int. J. Food Microbiol. 109:198–204.
   PubMed Web of Science ®Google Scholar
• Massouras, T., Pappa, E. C. and Mallatou, H. (2006). Headspace analysis of volatile flavour compounds of teleme cheese made from sheep and goat milk. Int. J. Dairy Technol. 59:250–256.
   Web of Science ®Google Scholar
• Miller, A., Morgan, M. E. and Libbey, L. M. (1974). Lactobacillus maltaromicus, a new species producing a malty aroma. Int. J. Syst. Bacteriol. 24:346–354.
   Google Scholar
• Møller, K. K., Rattray, F. P., Bredie, W. L. P., Høier, E. and Ardö, Y. (2013). Physicochemical and sensory characterization of Cheddar cheese with variable NaCl levels and equal moisture content. J. Dairy Sci. 96:1953–1971.
   PubMed Web of Science ®Google Scholar
• Morales, P., Fernández-García, E., Gaya, P. and Nuñez, M. (2003). Formation of volatile compounds by wild Lactococcus lactis strains isolated from raw ewes' milk cheese. Int. Dairy J. 13:201–209.
   Web of Science ®Google Scholar
• Morgan, M. E. (1970). Microbial flavor defects in dairy products and methods for their simulation. I. Malty flavor. J. Dairy Sci. 53:270–272.
   Web of Science ®Google Scholar
• Morgan, M. E., Lindsay, R. C., Libbey, L. M. and Pereira, R. L. (1966). Identity of additional aroma constituents in milk cultures of Streptococcus lactis var. maltigenes. J. Dairy Sci. 49:15–18.
   PubMed Web of Science ®Google Scholar
• Pappa, E. C., Massouras, T., Sotirakoglou, K. and Kandarakis, L. (2013). Formation of volatile compounds in Teleme cheese manufactured with mesophilic and thermophilic dairy starters. Small Rumin. Res. 111:110–119.
   Web of Science ®Google Scholar
• Pedersen, T. B., Ristagno, D., McSweeney, P. L. H., Vogensen, F. K. and Ardö, Y. (2013). Potential impact on cheese flavour of heterofermentative bacteria from starter cultures. Int. Dairy J. 33:112–119.
   Web of Science ®Google Scholar
• Rijnen, L., Yvon, M., van Kranenburg, R., Courtin, P., Verheul, A., Chambellon, E. and Smit, G. (2003). Lactococcal aminotransferases AraT and BcaT are key enzymes for the formation of aroma compounds from amino acids in cheese. Int. Dairy J. 13:805–812.
   Web of Science ®Google Scholar
• Ruyssen, T., Janssens, M., Van Gasse, B., Van Laere, D., Van der Eecken, N., De Meerleer, M., Vermeiren, L., Van Hoorde, K., Martins, J. C., Uyttendaele, M. and De Vuyst, L. (2013). Characterisation of Gouda cheeses based on sensory, analytical and high-field 1H nuclear magnetic resonance spectroscopy determinations: Effect of adjunct cultures and brine composition on sodium-reduced Gouda cheese. Int. Dairy J. 33:142–152.
   Web of Science ®Google Scholar
• Sable, S. and Cottenceau, G. (1999). Current knowledge of soft cheeses flavor and related compounds. J. Agric. Food Chem. 47:4825–4836.
   PubMed Web of Science ®Google Scholar
• Salmerón, I., Thomas, K. and Pandiella, S. S. (2014). Effect of substrate composition and inoculum on the fermentation kinetics and flavour compound profiles of potentially non-dairy probiotic formulations. LWT - Food Sci. Technol. 55:240–247.
   Web of Science ®Google Scholar
• Sgarbi, E., Lazzi, C., Tabanelli, G., Gatti, M., Neviani, E. and Gardini, F. (2013). Nonstarter lactic acid bacteria volatilomes produced using cheese components. J. Dairy Sci. 96:4223–4234.
   PubMed Web of Science ®Google Scholar
• Sheldon, R. M., Lindsay, R. C., Libbey, L. M. and Morgan, M. E. (1971). Chemical nature of malty flavor and aroma produced by Streptococcus lactis var. maltigenes. Appl. Microbiol. 22:263–266.
   PubMedGoogle Scholar
• Sinz, Q. and Schwab, W. (2012). Metabolism of amino acids, dipeptides and tetrapeptides by Lactobacillus sakei. Food Microbiol. 29:215–223.
   PubMed Web of Science ®Google Scholar
• Smit, B. A., Engels, W. J. and Smit, G. (2009). Branched chain aldehydes: production and breakdown pathways and relevance for flavour in foods. Appl. Microbiol. Biotechnol. 81:987–999.
   PubMed Web of Science ®Google Scholar
• Smit, B. A., Engels, W. J., Wouters, J. T. and Smit, G. (2004). Diversity of L-leucine catabolism in various microorganisms involved in dairy fermentations, and identification of the rate-controlling step in the formation of the potent flavour component 3-methylbutanal. Appl. Microbiol. Biotechnol. 64:396–402.
   PubMed Web of Science ®Google Scholar
• Smit, B. A., van Hylckama Vlieg, J. E., Engels, W. J., Meijer, L., Wouters, J. T. and Smit, G. (2005). Identification, cloning, and characterization of a Lactococcus lactis branched-chain alpha-keto acid decarboxylase involved in flavor formation. Appl. Environ. Microbiol. 71:303–311.
   PubMed Web of Science ®Google Scholar
• Sørensen, L. M., Gori, K., Petersen, M. A., Jespersen, L. and Arneborg, N. (2011). Flavour compound production by Yarrowia lipolytica, Saccharomyces cerevisiae and Debaryomyces hansenii in a cheese-surface model. Int. Dairy J. 21:970–978.
   Web of Science ®Google Scholar
• Tanous, C., Gori, A., Rijnen, L., Chambellon, E. and Yvon, M. (2005). Pathways for α-ketoglutarate formation by Lactococcus lactis and their role in amino acid catabolism. Int. Dairy J. 15:759–770.
   Web of Science ®Google Scholar
• Tanous, C., Kieronczyk, A., Helinck, S., Chambellon, E. and Yvon, M. (2002). Glutamate dehydrogenase activity: A major criterion for the selection of flavour-producing lactic acid bacteria strains. Antonie Van Leeuwenhoek. 82:271–278.
   PubMed Web of Science ®Google Scholar
• Thage, B. V., Broe, M. L., Petersen, M. H., Petersen, M. A., Bennedsen, M. and Ardö, Y. (2005). Aroma development in semi-hard reduced-fat cheese inoculated with Lactobacillus paracasei strains with different aminotransferase profiles. Int. Dairy J. 15:795–805.
   Web of Science ®Google Scholar
• Thierry, A., Maillard, M. B. and Yvon, M. (2002). Conversion of L-Leucine to Isovaleric Acid by Propionibacterium freudenreichii TL 34 and ITGP23 Appl. Environ. Microbiol. 68:608–615.
   PubMed Web of Science ®Google Scholar
• Tucker, J. S. and Morgan, M. E. (1967). Decarboxylation of alpha-keto acids by Streptococcus lactis var. maltigenes. Appl. Microbiol. 15:694–700.
   PubMedGoogle Scholar
• Van Leuven, I., Van Caelenberg, T. and Dirinck, P. (2008). Aroma characterisation of Gouda-type cheeses. Int. Dairy J. 18:790–800.
   Web of Science ®Google Scholar
• Wallace, J. M. and Fox, P. F. (1997). Effect of adding free amino acids to Cheddar cheese curd on proteolysis, flavour and texture development. Int. Dairy J. 7:157–167.
   Web of Science ®Google Scholar
• Ward, D. E., Ross, R. P., van der Weijden, C. C., Snoep, J. L. and Claiborne, A. (1999). Catabolism of branched-chain alpha-keto acids in Enterococcus faecalis: the bkd gene cluster, enzymes, and metabolic route. J. Bacteriol. 181:5433–5442.
   PubMed Web of Science ®Google Scholar
• Whetstine, M. E., Drake, M. A., Broadbent, J. R. and McMahon, D. (2006). Enhanced nutty flavor formation in cheddar cheese made with a malty Lactococcus lactis adjunct culture. J. Dairy Sci. 89:3277–3284.
   PubMed Web of Science ®Google Scholar
• Williams, A. G., Noble, J. and Banks, J. M. (2001). Catabolism of amino acids by lactic acid bacteria isolated from Cheddar cheese. Int. Dairy J. 11:203–215.
   Web of Science ®Google Scholar
• Yvon, M. and Rijnen, L. (2001). Cheese flavour formation by amino acid catabolism. Int. Dairy J. 11:185–201.
   Web of Science ®Google Scholar
• Yvon, M., Thirouin, S., Rijnen, L., Fromentier, D. and Gripon, J. C. (1997). An aminotransferase from Lactococcus lactis initiates conversion of amino acids to cheese flavor compounds. Appl. Environ. Microbiol. 63:414–419.
   PubMed Web of Science ®Google Scholar