Carbohydrate, peptide and lipid metabolism of lactic acid bacteria in sourdough

Food Microbiology

Volumn 24, Issue 2, 2007, Pages 128-138

  Gänzle, Michael G ^a   Vermeulen, Nicoline ^b   Vogel, Rudi F ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Carbohydrate metabolism; Lipid metabolism; Peptide metabolism; Sourdough lactic acid bacteria

Indexed keywords

PROTEIN;

ARTICLE; BREAD; CARBOHYDRATE METABOLISM; ENZYME SPECIFICITY; ENZYMOLOGY; FERMENTATION; FOOD CONTROL; LACTOBACILLUS; LIPID METABOLISM; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; STANDARD; TASTE;

BREAD; CARBOHYDRATE METABOLISM; FERMENTATION; FOOD MICROBIOLOGY; LACTOBACILLUS; LIPID METABOLISM; OXIDATION-REDUCTION; PROTEINS; SUBSTRATE SPECIFICITY; TASTE;

BACTERIA (MICROORGANISMS); LACTOBACILLUS; LACTOBACILLUS PLANTARUM; LACTOBACILLUS PONTIS; LACTOBACILLUS SANFRANCISCENSIS;

EID: 33748917136     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2006.07.006     Document Type: Article

References (85)

1. Axelsson L. Lactic acid bacteria: classification and physiology. In: Salminen S., von Wright A., and Ouwehand A. (Eds). Lactic Acid Bacteria. Microbiological and Functional Aspects. third ed (2004), Marcel Dekker, New York 1-66
2. Berg R.W., Sandine W.E., and Anderson A.W. Identification of a growth stimulant for Lactobacillus sanfrancisco. Appl. Environ. Microbiol. 42 (1981) 786-788
3. Böcker, G., 1993. Ökologische und physiologische Charakterisierung der sauerteigtypischen Stämme Lactobacillus sanfrancisco und Lactobacillus pontis sp. nov. Dissertation, Universität Hohenheim, Fakultät für Allgemeine und Angewandte Naturwissenschaften.
4. Cocaign-Bousquet M., Garrigues C., Loubiere P., and Lindley N.D. Physiology of pyruvate metabolism in Lactococcus lactis. Antonie van Leeuwenhoek 70 (1996) 253-267
5. Cselovszky J., Wolf G., and Hammes W.P. Production of formate, acetate, and succinate by anaerobic fermentation of Lactobacillus pentosus in the presence of citrate. Appl. Microbiol. Biotechnol. 37 (1992) 94-97
6. Czerny M., and Schieberle P. Important aroma compounds in freshly ground wholemeal and white wheat flour-identification and quantitative changes during sourdough fermentation. J. Agric. Food Chem. 50 (2002) 6835-6840
7. Damiani P., Gobbetti M., Cossignani L., Corsetti A., Simonetti M.S., and Rossi J. The sourdough microflora. Characterization of hetero-and homofermentative lactic acid bacteria, yeasts and their interactions on the basis of the volatile compounds produced. Z. Lebensm. Wiss. Technol. 29 (1996) 63-70
8. De Angelis M., Mariotti L., Rossi J., Servili M., Fox P.F., Rollan G., and Gobbetti M. Arginine catabolism by sourdough lactic acid bacteria: purification and characterization of the arginine deiminase pathway enzymes from Lactobacillus sanfranciscensis CB1. Appl. Environ. Microbiol. 68 (2002) 6193-6201
9. De Angelis M., Curtin A.C., McSweeney P.L., Faccia M., and Gobbetti M. Lactobacillus reuteri DSM 20016: purification and characterization of a cystathionine gamma-lyase and use as adjunct starter in cheesemaking. J. Dairy Res. 69 (2002) 255-267
10. De Angelis M., Gallo G., Settanni L., Corbo M.R., McSweeney P.L.H., and Gobbetti M. Purification and characterization of an intracellular family 3 β-glucosidase from Lactobacillus sanfranciscensis CB1. Ital. J. Food Sci. 17 (2005) 131-142
11. de Vuyst L., and Neysens P. The sourdough microflora: biodiversity and metabolic interactions. Trends Food Sci. Technol. 16 (2005) 43-56
12. de Vuyst L., de Vin F., Vaningelgem F., and Degeest B. Recent developments in the biosynthesis and applications of heteropolysaccharides from lactic acid bacteria. Int. Dairy J. 11 (2001) 687-707
13. Decock P., and Capelle S. Bread technology and sourdough technology. Trends Food Sci. Technol. 16 (2005) 113-120
14. Di Cagno R., De Angelis M., Lavermicocca P., De Vincenzi M., Giovannini C., Faccia M., and Gobbetti M. Proteolysis by sourdough lactic acid bacteria: effects on wheat flour protein fractions and gliadin peptides involved in human cereal intolerance. Appl. Environ. Microbiol. 68 (2002) 623-633
15. Di Cagno R., De Angelis M., Auricchio S., Greco L., Clarke C., De Vincenzi M., Giovannini C., D'Archivio M., Landolfo F., Parrilli G., Minervini F., Arendt E., and Gobbetti M. Sourdough bread made from wheat and nontoxic flours and started with selected lactobacilli is tolerated in celiac sprue patients. Appl. Environ. Microbiol. 70 (2004) 1088-1096
16. Ehrmann M.A., and Vogel R.F. Maltose metabolism of Lactobacillus sanfranciscensis: cloning and heterologous expression of the key enzymes, maltose phosphorylase and phosphoglucomutase. FEMS Microbiol. Lett. 169 (1998) 81-86
17. Ehrmann M.A., and Vogel R.F. Molecular taxonomy and genetics of sourdough lactic acid bacteria. Trends Food Sci. Technol. 16 (2005) 31-42
18. 13C nuclear magnetic resonance analysis of glucose and citrate end products in an ldhL-ldhD double-knockout strain of Lactobacillus plantarum. J. Bacteriol. 178 (1996) 7311-7315
19. Gallo G., De Angelis M., McSweeney P.L.H., Corbo M.R., and Gobbetti M. Partial purification and characterization of an X-prolyl dipeptidyl aminopeptidase from Lactobacillus sanfranciscensis CB1. Food Chem. 9 (2005) 535-544
20. Gänzle M.G., Ehmann M., and Hammes W.P. Modelling of growth of Lactobacillus sanfranciscensis and Candida milleri in response to process parameters of the sourdough fermentation. Appl. Environ. Microbiol. 64 (1998) 2616-2623
21. Gänzle M.G., Thiele C., Vermeulen N., and Vogel R.F. Stoffwechsel von Laktobazillen und ihr Einfluss auf das Brotaroma. Getreidetechnology 59 (2005) 148-152
22. Gobbetti M., and Corsetti A. Co-metabolism of citrate and maltose by Lactobacillus brevis subsp. lindneri CB1 citrate-negative strain: effect on growth, end-products and sourdough fermentation. Z. Lebensm. Unters. Forsch. 203 (1996) 82-87
23. Gobbetti M., Smacchi E., and Corsetti A. The proteolytic system of Lactobacillus sanfrancisco CB1: purification and characterization of a proteinase, a dipeptidase, and an aminopeptidase. Appl. Environ. Microbiol. 62 (1996) 3220-3226
24. Gobbetti M., De Angelis M., Arnaut P., Tossut P., Corsetti A., and Lavermicocca A. Added pentosans in breadmaking: fermentations of derived pentoses by sourdough lactic acid bacteria. Food Microbiol. 16 (1999) 409-418
25. Gobbetti M., Lavermicocca P., Minervini F., De Angelis M., and Corsetti A. Arabinose fermentation by Lactobacillus plantarum in sourdough with added pentosans and α-l-arabinofuranosidase: a tool to increase the production of acetic acid. J. Appl. Microbiol. 88 (2000) 317-324
26. Gobbetti M., De Angelis M., Corsetti A., and Di Cagno R. Biochemistry and physiology of sourdough lactic acid bacteria. Trends Food Sci. Technol. 16 (2005) 57-69
27. Groot M.N.N., and de Bont J.A.M. Conversion of phenylalanine to benzaldehyde initiated by an aminotransferase in Lactobacillus plantarum. Appl. Environ. Microbiol. 64 (1998) 3009-3013
28. Grosch W., and Wieser H. Redox reactions in wheat dough as affected by ascorbic acid. J. Cereal Sci. 29 (1999) 1-16
29. Hammes P.P., Brandt M.J., Francis K.L., Rosenheim J., Seitter M.F.H., and Vogelmann A. Microbial ecology of cereal fermentations. Trends Food Sci. Technol. 16 (2005) 4-11
30. Hammes W.P., and Hertel C. The genera Lactobacillus and Carnobacterium. In: Dworkin M. (Ed). The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, third ed (2003), Springer, Berlin. http://link.springer-ny.com/link/service/books/10125/ 〈http://link.springer-ny.com/link/service/books/10125/〉
31. Hammes W.P., Stolz P., and Gänzle M.G. Metabolism of lactobacilli in traditional sourdoughs. Adv. Food Sci. 18 (1996) 176-184
32. Hansen A., and Schieberle P. Generation of aroma compounds during sourdough fermentation: applied and fundamental aspects. Trends Food Sci. Technol. 16 (2005) 85-94
33. Hugenholtz J., Sysbesma W., Nierop Groot M., Wisselink W., Ladero V., Burgess K., van Sinderen D., Piard J.-C., Egignk G., Smid E.J., Savoy G., Sesma F., Jansen T., Hos P., and Kleerebezem M. Metabolic engineering of lactic acid bacteria for the production of nutraceuticals. Antonie van Leeuwenhoek 82 (2002) 217-235
34. Kang Y. Molekularbiologische Untersuchung aromarelevanter Stoffwechselleistungen von Laktobazillen im Sauerteig (2005), Verlag Grauer, Beuren
35. Knorr R., Ehrmann M.A., and Vogel R.F. Cloning, expression, and characterization of acetate kinase from Lactobacillus sanfranciscensis. Microbiol. Res. 156 (2001) 267-277
36. Knorr R., Ehrmann M.A., and Vogel R.F. Cloning of the phosphotransacetylase gene from Lactobacillus sanfranciscensis and characterization of its gene product. J. Basic Microbiol. 41 (2001) 339-349
37. Konings W.N. The cell membrane and the struggle for life of lactic acid bacteria. Antonie van Leeuwenhoek 82 (2002) 3-27
38. Korakli M., and Vogel R.F. Purification and characterisation of mannitol dehydrogenase from Lactobacillus sanfranciscensis. FEMS Microbiol. Lett. 220 (2003) 281-286
39. Korakli M., Gänzle M.G., Knorr R., Frank M., Rossmann A., and Vogel R.F. Metabolism of Lactobacillus sanfraniscensis under high pressure: investigations using stable carbon isotopes. In: Hayashi R. (Ed). Trends in High Pressure Bioscience and Biotechnology (2002), Elsevier, Amsterdam 287-294
40. Kunji E.R., Mierau I., Hagting A., Poolman B., and Konings W.N. The proteolytic systems of lactic acid bacteria. Antonie van Leeuwenhoek 70 (1996) 187-221
41. Laignelet B., and Dumas C. Oxydation des lipides et distribution des lipides oxydés au cours du pétrissage de la pate de farine de blé tendre. Lebensm. Wiss. Technol. 17 (1984) 226-230
42. Larrouture C., Ardaillon V., Pépin M., and Montel M.C. Ability of meat starter cultures to catabolize leucine and evaluation of the degradation products by using an HPLC method. Food Microbiol. 17 (2000) 563-570
43. Lavermicocca P., Valerio F., Evidente A., Lazzaroni S., Corsetti A., and Gobbetti M. Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl. Environ. Microbiol. 66 (2000) 4084-4090
44. Lavermicocca P., Valerio F., and Visconti A. Antifungal activity of phenyllactic acid against molds isolated from bakery products. Appl. Environ. Microbiol. 69 (2003) 634-640
45. Lokman B.C., Heerikhuisen M., Leer R.J., van den Broek A., Borsboom Y., Chaillou S., Postma P.W., and Pouwels P.H. Regulation of expression of the Lactobacillus pentosus xylAB operon. J. Bacteriol. 179 (1997) 5391-5397
46. Loponen J., Mikola M., Katina K., Sontag-Strohm F., and Salovaara H. Degradation of HMW glutenins during wheat sourdough fermentations. Cereal Chem. 81 (2004) 87-93
47. Martinez-Cuesta C., Requena T., and Pelaez C. Effect of bacteriocin-induced cell damage on the branched-chain amino acid transamination by Lactococcus lactis. FEMS Microbiol. Lett. 217 (2002) 109-113
48. Neubauer H., Glassker E., Hammes W.P., Poolman B., and Konings W.N. Mechanisms of maltose uptake and glucose excretion in Lactobacillus sanfrancisco. J. Bacteriol. 176 (1994) 3007-3012
49. Niefind K., Muller J., Riebel B., Hummel W., and Schomburg D. The crystal structure of R-specific alcohol dehydrogenase from Lactobacillus brevis suggests the structural basis of its metal dependency. J. Mol. Biol. 327 (2003) 317-328
50. Pepe O., Villani F., Oliviero D., Greco T., and Coppola S. Effect of proteolytic starter cultures as leavening agents of pizza dough. Int. J. Food Microbiol. 84 (2003) 319-326
51. Richter H., Vlad D., and Unden G. Significance of pantothenate for glucose fermentation by Oenococcus oeni and for suppression of the erythritol and acetate production. Arch. Microbiol. 175 (2001) 26-31
52. + from NADPH:NADH oxidase from Lactobacillus sanfrancisensis. Adv. Synth. Catal. 345 (2003) 707-712
53. Rijnen l., Courtin P., Gripon J.-C., and Yvon M. Expression of a heterologous glutamate dehydrogenase gene in Lactococcus lactis highly improves the conversion of amino acids to aroma compounds. Appl. Environ. Microbiol. 66 (2000) 1354-1359
54. Röcken W., Rick M., and Reinkemeier M. Controlled production of acetic acid in wheat sour doughs. Z. Lebensm. Unters. Forsch. 195 (1992) 259-263
55. Rollan G., Lorca G.L., and Font de Valdez G. Arginine catabolism and acid tolerance response in Lactobacillus reuteri isolated from sourdough. Food Microbiol. 20 (2003) 313-349
56. Sasaki Y., Laivenicks M., and Zeikus J.G. Lactobacillus reuteri ATCC53608 mdh gene cloning and recombinant mannitol dehydrogenase characterization. Appl. Microbiol. Biotechnol. 68 (2005) 36-41
57. Stolz P., Böcker G., Hammes W.P., and Vogel R.F. Utilization of electron acceptors by lactobacilli isolated from sourdough I. Lactobacillus sanfrancisco. Z. Lebensm. Unters. Forsch. 201 (1995) 91-96
58. Stolz P., Vogel R.F., and Hammes W.P. Utilization of electron acceptors by lactobacilli isolated from sourdough II. Lactobacillus pontis, L. reuteri, L. amylovorus, and L. fermentum. Z. Lebensm. Unters. Forsch. 201 (1995) 402-410
59. Stolz P., Hammes W.P., and Vogel R.F. Maltose-phosphorylase and hexokinaxse activity in lactobacilli from traditionally prepared sourdoughs. Adv. Food Sci. 18 (1996) 1-6
60. Sugihara F., and Kline L. Further studies on a growth medium for Lactobacillus sanfrancisco. J. Milk Food Technol. 38 (1975) 667-672
61. Tanous C., Kieronczyk A., Helinck S., Chambellon E., and Yvon M. Glutamate dehydrogenase activity: a major criterion for the selection of flavour-producing lactic acid bacteria strains. Antonie van Leeuwenhoek 82 (2002) 271-278
62. Tanous C., Gori A., Rijnen L., Chambellon E., and Yvon M. Pathways for α-ketoglutarate formation by Lactococcus lactis and their role in amino acid catabolism. Int. Dairy J. 15 (2005) 759-770
63. Thiele C., Gänzle M.G., and Vogel R.F. Contribution of sourdough lactobacilli, yeast, and cereal enzymes to the generation of amino acids in dough relevant for bread flavor. Cereal Chem. 79 (2002) 45-51
64. Thiele C., Gänzle M.G., and Vogel R.F. Fluorescence labeling of wheat proteins for determination of gluten hydrolysis and depolymerization during dough precessing and sourdough fermentation. J. Agric. Food Chem. 51 (2003) 2745-2752
65. Thiele C., Grassl S., and Gänzle M.G. Gluten hydrolysis and depolymerization during sourdough fermentation. J. Agric. Food Chem. 52 (2004) 1307-1314
66. Tieking M., and Gänzle M.G. Exopolysaccharides from cereal-associated lactobacilli. Trends Food Sci. Technol. 16 (2005) 79-84
67. Tieking M., Korakli M., Ehrmann M.A., Gänzle M.G., and Vogel R.F. In situ production of exopolysaccharides during sourdough fermentation by cereal and intestinal isolates of lactic acid bacteria. Appl. Environ. Microbiol. 69 (2003) 945-952
68. Tieking M., Ehrmann M.A., Vogel R.F., and Gänzle M.G. Molecular and functional characterization of a levansucrase from Lactobacillus sanfranciscensis. Appl. Microbiol. Biotechnol. 66 (2005) 663-665
69. Tieking M., Kühnl W., and Gänzle M.G. Evidence for formation of heterooligosaccharides by Lactobacillus sanfranciscensis during growth in wheat sourdough. J. Agric. Food Chem. 53 (2005) 2456-2461
70. Titgemeyer F., and Hillen W. Global control of sugar metabolism: a Gram-positive solution. Antonie van Leeuwenhoek 82 (2002) 59-71
71. Turner M.S., Woodberry T., Hafner L.M., and Giffard P.M. The bspA locus of Lactobacillus fermentum BR11 encodes a l-cystine uptake system. J. Bacteriol. 181 (1999) 2191-2198
72. Valence F., Deutsch S.M., Richoux R., Gagnaire V., and Lortal S. Autolysis and related proteolysis in Swiss cheese for two Lactobacillus helveticus strains. J. Dairy Res. 67 (2000) 261-271
73. van Hijum S.A.F.T., Kralj S., Ozimek L.K., Dijkhuizen L., and van Geel-Schutten I.G.H. Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol. Mol. Biol. Rev. 70 (2006) 157-176
74. van Kranenburg R., Kleerebezem M., van Hylckama Vlieg J., Ursing B.M., Bockhost J., Smit B.A., Ayad E.H.E., Smit G., and Siezen R.J. Flavour formation from amino acids by lactic acid bacteria: predictions from genome sequence analysis. Int. Dairy J. 12 (2002) 111-121
75. Vermeulen, N., Czerny, M., Gänzle, M., Schieberle, P., Vogel, R.F. Reduction of (E)-2-nonenal and (E;E)-2,4-decadienal during sourdough fermentation. J. Cereal Sci., in press.
76. Vermeulen N., Thiele C., Gänzle M.G., and Vogel R.F. Cysteine metabolism by cereal-associated lactobacilli. In: de Vuyst L. (Ed). Sourdough, from Fundamentals to Applications (2003), Vrije Universiteit Brussel (VUB), IMDO, Brussels 58-59
77. T. Appl. Environ. Microbiol. 71 (2005) 6260-6266
78. Vermeulen N., Kretzer J., Machalitza H., Vogel R.F., and Gänzle M.G. Influence of redox-reactions catalysed by homo- and heterofermentative lactobacilli on gluten in wheat sourdoughs. J. Cereal Sci. 43 (2006) 137-143
79. T and Lactobacillus plantarum TMW1.468. J. Agric. Food Chem. 54 (2006) 3832-3839
80. Vogel R.F., Knorr R., Müller M.R.A., Steudel U., Gänzle M.G., and Ehrmann M.A. Non-dairy lactic fermentations: the cereal world. Antonie van Leeuwenhoek 76 (1999) 403-411
81. von Weymarn N., Hujanen M., and Leisola M. Production of d-mannitol by heterofermentative lactic acid bacteria. Process Biochem. 37 (2002) 1207-1213
82. Weimer B., Seefeldt K., and Dias B. Sulfur metabolism in bacteria associated with cheese. Antonie van Leeuwenhoek 76 (1999) 247-261
83. Weingand-Ziadé A., Gerber-Décombay C., and Affolter M. Functional characterization of a salt- and thermotolerant glutaminase from Lactobacillus rhamnosus. Enzyme Microb. Technol. 32 (2003) 862-867
84. Yvon M., Berthelot S., and Gripon J.C. Adding α-ketoglutarate to semi-hard cheese curd highly enhances the conversion of amino acids to aroma compounds. Int. Dairy J. 8 (1998) 889-898
85. Zotta T., Piraino P., Ricciardi A., McSweeney P.L.H., and Parente E. Proteolysis in model sourdough fermentations. J. Agric. Food Chem. 54 (2006) 2567-2574