Use of non-growing Lactococcus lactis cell suspensions for production of volatile metabolites with direct relevance for flavour formation during dairy fermentations

Microbial Cell Factories

Volumn 13, Issue 1, 2014, Pages

  Van De Bunt, Bert ^a,b   Bron, Peter A ^a,b,c   Sijtsma, Lolke ^a,c,d   De Vos, Willem M ^d,e   Hugenholtz, Jeroen ^f  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b NIZO FOOD RESEARCH   (Netherlands)

^c The Kluyver Centre for Genomics of Industrial Fermentations/NCSB   (Netherlands)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e UNIVERSITY OF HELSINKI   (Finland)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Amino acid metabolism; Cheese; Flavour; Lactic acid bacteria; Lactococcus lactis; Non growing; Screening method

Indexed keywords

2 OXOGLUTARIC ACID; AMINO ACID; FLAVORING AGENT; GLUCOSE; LEUCINE; PYRIDOXAL 5 PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; VOLATILE ORGANIC COMPOUND;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; CELL SUSPENSION; CHEESE RIPENING; CONTROLLED STUDY; FERMENTATION; FLAVOR; LACTIC ACID BACTERIUM; LACTOCOCCUS LACTIS; METABOLITE; NONHUMAN; PLASMID; PROTEIN DEGRADATION; ANIMAL; CHEESE; METABOLISM; MICROBIOLOGY;

ANIMALS; CHEESE; LACTOCOCCUS LACTIS; VOLATILE ORGANIC COMPOUNDS;

EID: 84924078487     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-014-0176-2     Document Type: Article

References (50)

1. Visser S: Proteolytic enzymes and their relation to cheese ripening and flavor: an overview. J Dairy Sci 1993, 76:329-350.
2. Konings WN, Poolman B, Driessen AJM, Maloney PC: Bioenergetics and solute transport in lactococci. Crit Rev Microbiol 1989, 16:419-476.
3. Smid EJ, Poolman B, Konings WN: Casein utilization by lactococci. Appl Environ Microbiol 1991, 57:2447-2452.
4. Kunji ERS, Mierau I, Hagting A, Poolman B, Konings WN: The proteotytic systems of lactic acid bacteria. Antonie Van Leeuwenhoek 1996, 70:187-221.
5. Pritchard GG, Coolbear T: The physiology and biochemistry of the proteolytic system in lactic acid bacteria. FEMS Microbiol Rev 1993, 12:179-206.
6. Siezen RJ: Multi-domain, cell-envelope proteinases of lactic acid bacteria. Antonie Van Leeuwenhoek 1999, 76:139-155.
7. Savijoki K, Ingmer H, Varmanen P: Proteolytic systems of lactic acid bacteria. Appl Microbiol Biotechnol 2006, 71:394-406.
8. Bachmann H, Starrenburg MJC, Dijkstra A, Molenaar D, Kleerebezem M, Rademaker JLW, van Hylckama Vlieg JET: Regulatory phenotyping reveals important diversity within the species Lactococcus lactis. Appl Environ Microbiol 2009, 75:5687-5694.
9. Wouters JTM, Ayad EHE, Hugenholtz J, Smit G: Microbes from raw milk for fermented dairy products. Int Dairy J 2002, 12:91-109.
10. Ayad EHE, Verheul A, Wouters JTM, Smit G: Application of wild starter cultures for flavour development in pilot plant cheese making. Int Dairy J 2000, 10:169-179.
11. Brandsma JB, Floris E, Dijkstra ARD, Rijnen L, Wouters JA, Meijer WC: Natural diversity of aminotransferases and dehydrogenase activity in a large collection of Lactococcus lactis strains. Int Dairy J 2008, 18:1103-1108.
12. Ganesan B, Dobrowolski P, Weimer BC: Identification of the leucine-to-2-methylbutyric acid catabolic pathway of Lactococcus lactis. Appl Environ Microbiol 2006, 72:4264-4273.
13. García-Cayuela T, de Cadiñanos LP G, Peláez C, Requena T: 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 2012, 159:207-213.
14. Brandsma JB, van de Kraats I, Abee T, Zwietering MH, Meijer WC: Arginine metabolism in sugar deprived Lactococcus lactis enhances survival and cellular activity, while supporting flavour production. Food Microbiol 2012, 29:27-32.
15. Bachmann H, Kruijswijk Z, Molenaar D, Kleerebezem M, van Hylckama Vlieg JET: A high-throughput cheese manufacturing model for effective cheese starter culture screening. J Dairy Sci 2009, 92:5868-5882.
16. Wilkinson MG, Guinee TP, Fox PF: Factors which may influence the determination of autolysis of starter bacteria during cheddar cheese ripening. Int Dairy J 1994, 4:141-160.
17. Crow VL, Coolbear T, Gopal PK, Martley FG, McKay LL, Riepe H: The role of autolysis of lactic acid bacteria in the ripening of cheese. Int Dairy J 1995, 5:855-875.
18. Engels WJM, Dekker R, de Jong C, Neeter R, Visser S: A comparative study of volatile compounds in the water-soluble fraction of various types of ripened cheese. Int Dairy J 1997, 7:255-263.
19. Milo C, Reineccius GA: Identification and quantification of potent odorants in regular-Fat and Low-Fat mild cheddar cheese. J Agric Food Chem 1997, 45:3590-3594.
20. Varming C, Andersen LT, Petersen MA, Ardö Y: Flavour compounds and sensory characteristics of cheese powders made from matured cheeses. Int Dairy J 2013, 30:19-28.
21. Van Leuven I, Van Caelenberg T, Dirinck P: Aroma characterisation of Gouda-type cheeses. Int Dairy J 2008, 18:790-800.
22. Van Hoorde K, Van Leuven I, Dirinck P, Heyndrickx M, Coudijzer K, Vandamme P, Huys G: Selection, application and monitoring of Lactobacillus paracasei strains as adjunct cultures in the production of Gouda-type cheeses. Int J Food Microbiol 2010, 144:226-235.
23. Smit G, Braber A, Van Spronsen W, Van Den Berg G, Exterkate FA: Ch-Easy Model: a Cheese-Based Model to Study Cheese Ripening. In Bioflavour 95. Edited by Étiévant P, Schreier P. Dijon, Paris, France: INRA; :185-190.
24. González L, Sacristán N, Arenas R, Fresno JM, Eugenia Tornadijo M: Enzymatic activity of lactic acid bacteria (with antimicrobial properties) isolated from a traditional Spanish cheese. Food Microbiol 2010, 27:592-597.
25. Yvon M, Gitton C, Chambellon E, Bergot G, Monnet V: The initial efficiency of the proteolytic system of Lactococcus lactis strains determines their responses to a cheese environment. Int Dairy J 2011, 21:335-345.
26. Kaminogawa S, Ninomiya T, Yamauchi K: Aminopeptidase profiles of Lactic streptococci. J Dairy Sci 1984, 67:2483-2492.
27. Kenny O, FitzGerald RJ, O'Cuinn G, Beresford T, Jordan K: Growth phase and growth medium effects on the peptidase activities of Lactobacillus helveticus. Int Dairy J 2003, 13:509-516.
28. Christensen JE, Dudley EG, Pederson JA, Steele JL: Peptidases and amino acid catabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 1999, 76:217-246.
29. Gao S, Mooberry ES, Steele JL: Use of 13C nuclear magnetic resonance and Gas chromatography to examine methionine catabolism by Lactococci. Appl Environ Microbiol 1998, 64:4670-4675.
30. Ziadi M, Bergot G, Courtin P, Chambellon E, Hamdi M, Yvon M: Amino acid catabolism by Lactococcus lactis during milk fermentation. Int Dairy J 2010, 20:25-31.
31. Rijnen L, Bonneau S, Yvon M: Genetic characterization of the major Lactococcal aromatic aminotransferase and its involvement in conversion of amino acids to aroma compounds. Appl Environ Microbiol 1999, 65:4873-4880.
32. Yvon M, Thirouin S, Rijnen L, Fromentier D, Gripon J: An aminotransferase from Lactococcus lactis initiates conversion of amino acids to cheese flavor compounds. Appl Environ Microbiol 1997, 63:414-419.
33. Klein N, Maillard MB, Thierry A, Lortal S: Conversion of amino acids into aroma compounds by cell-free extracts of Lactobacillus helveticus. J Appl Microbiol 2001, 91:404-411.
34. Exterkate FA, Alting AC: The role of starter peptidases in the initial proteolytic events leading to amino acids in Gouda cheese. Int Dairy J 1995, 5:15-28.
35. Le Boucher C, Courant F, Jeanson S, Chereau S, Maillard MB, Royer AL, Thierry A, Dervilly-Pinel G, Le Bizec B, Lortal S: First mass spectrometry metabolic fingerprinting of bacterial metabolism in a model cheese. Food Chem 2013, 141:1032-1040.
36. Banks JM, Yvon M, Gripon JC, de la Fuente MA, Brechany EY, Williams AG, Muir DD: Enhancement of amino acid catabolism in Cheddar cheese using alpha-ketoglutarate: amino acid degradation in relation to volatile compounds and aroma character. Int Dairy J 2001, 11:235-243.
37. Yvon M, Berthelot S, Gripon JC: Adding α-ketoglutarate to semi-hard cheese curd highly enhances the conversion of amino acids to aroma compounds. Int Dairy J 1998, 8:889-898.
38. Helinck S, Le Bars D, Moreau D, Yvon M: Ability of thermophilic lactic acid bacteria to produce aroma compounds from amino acids. Appl Environ Microbiol 2004, 70:3855-3861.
39. Thierry A, Maillard M-B, Yvon M: Conversion of l-Leucine to Isovaleric Acid by Propionibacterium freudenreichii TL 34 and ITGP23. Appl Environ Microbiol 2002, 68:608-615.
40. Kieronczyk A, Skeie S, Olsen K, Langsrud T: Metabolism of amino acids by resting cells of non-starter lactobacilli in relation to flavour development in cheese. Int Dairy J 2001, 11:217-224.
41. Yvon M, Rijnen L: Cheese flavour formation by amino acid catabolism. Int Dairy J 2001, 11:185-201.
42. Nierop Groot MN, de Bont JAM: Conversion of Phenylalanine to Benzaldehyde Initiated by an Aminotransferase in Lactobacillus plantarum. Appl Environ Microbiol 1998, 64:3009-3013.
43. Smit BA, Engels WJM, Wouters JTM, Smit G: 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 2004, 64:396-402.
44. Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A: The complete genome sequence of the Lactic Acid Bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 2001, 11:731-753.
45. Gasson MJ: Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol 1983, 154:1-9.
46. Ayad EHE, Verheul A, de Jong C, Wouters JTM, Smit G: Flavour forming abilities and amino acid requirements of Lactococcus lactis strains isolated from artisanal and non-dairy origin. Int Dairy J 1999, 9:725-735.
47. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Huges J, Goh Y, Benson A, Baldwin K, Lee J-H, Díaz-Muñiz I, Dosti B, Smeianov V, Wechter W, Barabote R, et al: Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci 2006, 103:15611-15616.
48. Siezen RJ, Bayjanov J, Renckens B, Wels M, van Hijum SAFT, Molenaar D, van Hylckama Vlieg JET: Complete Genome Sequence of Lactococcus lactis subsp. lactis KF147, a Plant-Associated Lactic Acid Bacterium. J Bacteriol 2010, 192:2649-2650.
49. Poolman B, Konings WN: Relation of growth of Streptococcus lactis and Streptococcus cremoris to amino acid transport. J Bacteriol 1988, 170:700-707.
50. Flahaut NL, Wiersma A, Bunt B, Martens D, Schaap P, Sijtsma L, Santos VM, Vos W: Genome-scale metabolic model for Lactococcus lactis MG1363 and its application to the analysis of flavor formation. Appl Microbiol Biotechnol 2013, 97:8729-8739.