This review describes recent scientific research on the production of aroma compounds by lactic acid bacteria (LAB) in fermented food products. We discuss the various precursor molecules for the formation of aroma compounds in connection with the metabolic pathways involved. The roles of nonmetabolic properties such as cell lysis are also described in relation to aroma formation. Finally, we provide an overview of the literature on methods to steer and control aroma formation by LAB in mixed culture fermentations. We demonstrate that the technological progress made recently in high-throughput analysis methods has been driving the development of new approaches to understand, control, and steer aroma formation in (dairy) fermentation processes. This currently entails proposing new rules for designing stable, high-performance mixed cultures constituting a selection of strains, which in concert and on the basis of their individual predicted gene contents deliver the required functionalities.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Alting AC, Engels WJM, Van Schalkwijk S, Exterkate FA. 1995. Purification and characterization of cystathionine (beta)-lyase from Lactococcus lactis subsp. cremoris B78 and its possible role in flavor development in cheese. Appl. Environ. Microbiol. 61:4037–42 [Google Scholar]
  2. Anderson M, Heeschen W, Jellema A, Kuzdzal-Savoie S, Needs EC. et al. 1991. Determination of free fatty acids in milk and milk products. Int. Dairy Fed. Bull. 265:3–52 [Google Scholar]
  3. Ardö Y. 2006. Flavour formation by amino acid catabolism. Biotechnol. Adv. 24:238–42 [Google Scholar]
  4. Ayad EH, Verheul A, Engels WJ, Wouters JT, 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 [Google Scholar]
  5. Baankreis R, van Schalkwijk S, Alting AC, Exterkate FA. 1995. The occurrence of two intracellular oligoendopeptidases in Lactococcus lactis and their significance for peptide conversion in cheese. Appl. Microbiol. Biotechnol. 44:386–92 [Google Scholar]
  6. Bachmann H. 2009. Regulatory and adaptive responses of Lactococcus lactis in situ. PhD thesis, Wagening. Univ., Wageningen, Neth. [Google Scholar]
  7. Bachmann H, de Wilt L, Kleerebezem M, van Hylckama Vlieg JE. 2010. Time-resolved genetic responses of Lactococcus lactis to a dairy environment. Environ. Microbiol. 12:1260–70 [Google Scholar]
  8. Bachmann H, Kleerebezem M, van Hylckama Vlieg JE. 2008. High-throughput identification and validation of in situ-expressed genes of Lactococcus lactis. Appl. Environ. Microbiol. 74:4727–36 [Google Scholar]
  9. Bachmann H, Kruijswijk Z, Molenaar D, Kleerebezem M, van Hylckama Vlieg JET. 2009a. A high-throughput cheese manufacturing model for effective cheese starter culture screening. J. Dairy Sci. 92:5868–82 [Google Scholar]
  10. Bachmann H, Molenaar D, Kleerebezem M, van Hylckama Vlieg JE. 2011. High local substrate availability stabilizes a cooperative trait. ISME J. 5:929–32 [Google Scholar]
  11. Bachmann H, Santos F, Kleerebezem M, van Hylckama Vlieg JE. 2007. Luciferase detection during stationary phase in Lactococcus lactis. Appl. Environ. Microbiol. 73:4704–6 [Google Scholar]
  12. Bachmann H, Starrenburg MJ, Dijkstra A, Molenaar D, Kleerebezem M. et al. 2009b. Regulatory phenotyping reveals important diversity within the species Lactococcus lactis. Appl. Environ. Microbiol. 75:5687–94 [Google Scholar]
  13. Bachmann H, Starrenburg MJ, Molenaar D, Kleerebezem M, van Hylckama Vlieg JE. 2012. Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution. Genome Res. 22:115–24 [Google Scholar]
  14. Bandell M, Lhotte ME, Marty-Teysset C, Veyrat A, Prévost H. et al. 1998. Mechanism of the citrate transporters in carbohydrate and citrate cometabolism in Lactococcus and Leuconostoc species. Appl. Environ. Microbiol. 64:1594–600 [Google Scholar]
  15. Bayjanov JR, Siezen RJ, van Hijum SA. 2010. PanCGHweb: a web tool for genotype calling in pangenome CGH data. Bioinformatics 26:1256–57 [Google Scholar]
  16. Broadbent JR, Neeno-Eckwall EC, Stahl B, Tandee K, Cai H. et al. 2012. Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation. BMC Genomics 13:533 [Google Scholar]
  17. Chaves AC, Fernandez M, Lerayer AL, Mierau I, Kleerebezem M, Hugenholtz J. 2002. Metabolic engineering of acetaldehyde production by Streptococcus thermophilus. Appl. Environ. Microbiol. 68:5656–62 [Google Scholar]
  18. Collins YF, McSweeney PL, Wilkinson MG. 2003a. Evidence of a relationship between autolysis of starter bacteria and lipolysis in cheddar cheese during ripening. J. Dairy Res. 70:105–13 [Google Scholar]
  19. Collins YF, McSweeney PL, Wilkinson MG. 2003b. Lipolysis and free fatty acid catabolism in cheese: a review of current knowledge. Int. Dairy J. 13:841–66 [Google Scholar]
  20. de Bok FA, Janssen PW, Bayjanov JR, Sieuwerts S, Lommen A. et al. 2011. Volatile compound fingerprinting of mixed-culture fermentations. Appl. Environ. Microbiol. 77:6233–39 [Google Scholar]
  21. de Ruyter PG, Kuipers OP, Meijer WC, de Vos WM. 1997. Food-grade controlled lysis of Lactococcus lactis for accelerated cheese ripening. Nat. Biotechnol. 15:976–79 [Google Scholar]
  22. Dias B, Weimer B. 1998. Conversion of methionine to thiols by lactococci, lactobacilli, and brevibacteria. Appl. Environ. Microbiol. 64:3320–26 [Google Scholar]
  23. Douglas GL, Klaenhammer TR. 2010. Genomic evolution of domesticated microorganisms. Annu. Rev. Food Sci. Technol. 1:397–414 [Google Scholar]
  24. Ehrlich F. 1907. Über die Bedingungen der Fuselölbindungen und über ihnen Zusammenhang mit dem Eiweissaufbau der Hefe. Ber. Deutsch Chem. Gesells. 40:1027–47 [Google Scholar]
  25. Engels WJM, Dekker R, de Jong C, Neeter R, Visser S. 1997. A comparative study of volatile compounds in the water-soluble fraction of various types of ripened cheese. Int. Dairy J. 7:255–63 [Google Scholar]
  26. Erkus O, de Jager VC, Spus M, van Alen-Boerrigter IJ, van Rijswijck IM. et al. 2013. Multifactorial diversity sustains microbial community stability. ISME J. 7:2126–36 [Google Scholar]
  27. Fernández M, Kleerebezem M, Kuipers OP, Siezen RJ, van Kranenburg R. 2002. Regulation of the metC-cysK operon, involved in sulfur metabolism in Lactococcus lactis. J. Bacteriol. 184:82–90 [Google Scholar]
  28. Fernández M, van Doesburg W, Rutten GA, Marugg JD, Alting AC. et al. 2000. Molecular and functional analyses of the metC gene of Lactococcus lactis, encoding cystathionine β-lyase. Appl. Environ. Microbiol. 66:42–48 [Google Scholar]
  29. Flahaut NAL, Wiersma A, van de Bunt B, Martens DE, Schaap PJ. et al. 2013. Genome-scale metabolic model for Lactococcus lactis MG1363 and its application to the analysis of flavor formation. Appl. Microbiol. Biotechnol. 97:8729–39 [Google Scholar]
  30. Golic N, Schliekelmann M, Fernández M, Kleerebezem M, van Kranenburg R. 2005. Molecular characterization of the CmbR activator-binding site in the metC-cysK promoter region in Lactococcus lactis. Microbiology 151:439–46 [Google Scholar]
  31. Griffiths MW, Tellez AM. 2013. Lactobacillus helveticus: the proteolytic system. Front. Microbiol. 4:30 [Google Scholar]
  32. Guldfeldt LU, Sorensen KI, Stroman P, Behrndt H, Williams D, Johansen E. 2001. Effect of starter cultures with a genetically modified peptidolytic or lytic system on cheddar cheese ripening. Int. Dairy J. 11:373–82 [Google Scholar]
  33. Guo T, Kong J, Zhang L, Zhang C, Hu S. 2012. Fine tuning of the lactate and diacetyl production through promoter engineering in Lactococcus lactis. PLoS One 7:e36296 [Google Scholar]
  34. Hao P, Zheng H, Yu Y, Ding G, Gu W. et al. 2011. Complete sequencing and pan-genomic analysis of Lactobacillus delbrueckii subsp. bulgaricus reveal its genetic basis for industrial yogurt production. PLoS One 6:e15964 [Google Scholar]
  35. Hugenholtz J. 1993. Citrate metabolism in lactic acid bacteria. FEMS Microbiol. Rev. 12:165–78 [Google Scholar]
  36. Hugenholtz J, Kleerebezem M, Starrenburg M, Delcour J, de Vos W, Hols P. 2000. Lactococcus lactis as a cell factory for high-level diacetyl production. Appl. Environ. Microbiol. 66:4112–14 [Google Scholar]
  37. Hugenholtz J, Splint R, Konings WN, Veldkamp H. 1987. Selection of protease-positive and protease-negative variants of Streptococcus cremoris. Appl. Environ. Microbiol. 53:309–14 [Google Scholar]
  38. Imhof R, Glättli H, Bosset JO. 1995. Volatile organic compounds produced by thermophilic and mesophilic single strain dairy starter cultures. Lebensm. Wiss. Technol. 28:78–86 [Google Scholar]
  39. Kieronczyk A, Skeie S, Langsrud T, Yvon M. 2003. Cooperation between Lactococcus lactis and nonstarter lactobacilli in the formation of cheese aroma from amino acids. Appl. Environ. Microbiol. 69:734–39 [Google Scholar]
  40. Kovaleva GY, Gelfand MS. 2007. Transcriptional regulation of the methionine and cysteine transport and metabolism in streptococci. FEMS Microbiol. Lett. 276:207–15 [Google Scholar]
  41. Kunji ER, Mierau I, Hagting A, Poolman B, Konings WN. 1996. The proteolytic systems of lactic acid bacteria. Antonie Leeuwenhoek 70:187–221 [Google Scholar]
  42. Lees GJ, Jago GR. 1976. Formation of acetaldehyde from threonine by lactic acid bacteria. J. Dairy Res. 43:75–83 [Google Scholar]
  43. Leroy F, de Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15:67–78 [Google Scholar]
  44. Liu M, Prakash C, Nauta A, Siezen RJ, Francke C. 2012. Computational analysis of cysteine and methionine metabolism and its regulation in dairy starter and related bacteria. J. Bacteriol. 194:3522–33 [Google Scholar]
  45. Lortal S, Chapot-Chartier M-P. 2005. Role, mechanisms and control of lactic acid bacteria lysis in cheese. Int. Dairy J. 15:857–71 [Google Scholar]
  46. Molimard P, Spinnler HE. 1996. Review: Compounds involved in the flavor of surface mold-ripened cheeses: origins and properties. J. Dairy Sci. 79:169–84 [Google Scholar]
  47. Nauta A, van den Burg B, Karsens H, Venema G, Kok J. 1997. Design of thermolabile bacteriophage repressor mutants by comparative molecular modeling. Nat. Biotechnol. 15:980–83 [Google Scholar]
  48. Nierop Groot MN, de Bont JA. 1999. Involvement of manganese in conversion of phenylalanine to benzaldehyde by lactic acid bacteria. Appl. Environ. Microbiol. 65:5590–93 [Google Scholar]
  49. Nierop Groot MN, de Bont JAM. 1998. Conversion of phenylalanine to benzaldehyde initiated by an aminotransferase in Lactobacillus plantarum. Appl. Environ. Microbiol. 64:3009–13 [Google Scholar]
  50. O'Flaherty S, Klaenhammer TR. 2011. The impact of omic technologies on the study of food microbes. Annu. Rev. Food Sci. Technol. 2:353–71 [Google Scholar]
  51. Ott A, Fay LB, Chaintreau A. 1997. Determination and origin of the aroma impact compounds of yogurt flavor. J. Agric. Food Chem. 45:850–58 [Google Scholar]
  52. Ott A, Germond JE, Chaintreau A. 2000. Vicinal diketone formation in yogurt: 13C precursors and effect of branched-chain amino acids. J. Agric. Food Chem. 48:724–31 [Google Scholar]
  53. Park EJ, Chun J, Cha CJ, Park WS, Jeon CO, Bae JW. 2012. Bacterial community analysis during fermentation of ten representative kinds of kimchi with barcoded pyrosequencing. Food Microbiol. 30:197–204 [Google Scholar]
  54. Prins WA, Botha M, Botes M, de Kwaadsteniet M, Endo A, Dicks LMT. 2010. Lactobacillus plantarum 24, isolated from the Marula fruit (Sclerocarya birrea), has probiotic properties and harbors genes encoding the production of three bacteriocins. Curr. Microbiol. 61:584–89 [Google Scholar]
  55. Pudlik AM, Lolkema JS. 2012a. Rerouting citrate metabolism in Lactococcus lactis to citrate-driven transamination. Appl. Environ. Microbiol. 78:6665–73 [Google Scholar]
  56. Pudlik AM, Lolkema JS. 2012b. Substrate specificity of the citrate transporter CitP of Lactococcus lactis. J. Bacteriol. 194:3627–35 [Google Scholar]
  57. Pudlik AM, Lolkema JS. 2013. Uptake of α-ketoglutarate by citrate transporter CitP drives transamination in Lactococcus lactis. Appl. Environ. Microbiol. 79:1095–101 [Google Scholar]
  58. Rademaker JL, Herbet H, Starrenburg MJ, Naser SM, Gevers D. et al. 2007. Diversity analysis of dairy and nondairy Lactococcus lactis isolates, using a novel multilocus sequence analysis scheme and (GTG)5-PCR fingerprinting. Appl. Environ. Microbiol. 73:7128–37 [Google Scholar]
  59. Samson JE, Moineau S. 2013. Bacteriophages in food fermentations: new frontiers in a continuous arms race. Annu. Rev. Food Sci. Technol. 4:347–68 [Google Scholar]
  60. Savijoki K, Ingmer H, Varmanen P. 2006. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 71:394–406 [Google Scholar]
  61. Schoustra SE, Kasase C, Toarta C, Kassen R, Poulain AJ. 2013. Microbial community structure of three traditional Zambian fermented products: mabisi, chibwantu and munkoyo. PLoS One 8:e63948 [Google Scholar]
  62. Sieuwerts S, Molenaar D, van Hijum SA, Beerthuyzen M, Stevens MJ. et al. 2010. Mixed-culture transcriptome analysis reveals the molecular basis of mixed-culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus. Appl. Environ. Microbiol. 76:7775–84 [Google Scholar]
  63. Siezen RJ, Bayjanov J, Renckens B, Wels M, van Hijum SA. et al. 2010. Complete genome sequence of Lactococcus lactis subsp. lactis KF147, a plant-associated lactic acid bacterium. J. Bacteriol. 192:2649–50 [Google Scholar]
  64. Siezen RJ, Bayjanov JR, Felis GE, van der Sijde MR, Starrenburg M. et al. 2011. Genome-scale diversity and niche adaptation analysis of Lactococcus lactis by comparative genome hybridization using multi-strain arrays. Microb. Biotechnol. 4:383–402 [Google Scholar]
  65. Smid EJ, Driessen AJM, Konings WN. 1989. Mechanism and energetics of dipeptide transport in membrane vesicles of Lactococcus lactis. J. Bacteriol. 171:292–98 [Google Scholar]
  66. Smid EJ, Poolman B, Konings WN. 1991. Casein utilization by lactococci. Appl. Environ. Microbiol. 57:2447–52 [Google Scholar]
  67. Smid EJ, Hugenholtz J. 2010. Functional genomics for food fermentation processes. Annu. Rev. Food Sci. Technol. 1:497–519 [Google Scholar]
  68. Smid EJ, Lacroix C. 2013. Microbe-microbe interactions in mixed culture food fermentations. Curr. Opin. Biotechnol. 24:148–54 [Google Scholar]
  69. Smit BA, Engels WJ, Bruinsma J, van Hylckama Vlieg JE, Wouters JT, Smit G. 2004. Development of a high throughput screening method to test flavour-forming capabilities of anaerobic micro-organisms. J. Appl. Microbiol. 97:306–13 [Google Scholar]
  70. Smit BA, van Hylckama Vlieg JE, Engels WJ, Meijer LJ, Wouters T, Smit G. 2005a. Identification, cloning, and characterization of a Lactococcus lactis branched-chain alpha-keto acid decarboxylase involved in flavor formation. Appl. Environ. Microbiol. 71:303–11 [Google Scholar]
  71. Smit G, Smit BA, Engels WJ. 2005b. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol. Rev. 29:591–610 [Google Scholar]
  72. Steele J, Broadbent J, Kok J. 2013. Perspectives on the contribution of lactic acid bacteria to cheese flavor development. Curr. Opin. Biotechnol. 24:135–41 [Google Scholar]
  73. Steen A, Buist G, Horsburgh GJ, Venema G, Kuipers OP. et al. 2005. AcmA of Lactococcus lactis is an N-acetylglucosaminidase with an optimal number of LysM domains for proper functioning. FEBS J. 272:2854–68 [Google Scholar]
  74. Sybesma W, Hugenholtz J, de Vos WM, Smid EJ. 2006. Safe use of genetically modified lactic acid bacteria in food. Bridging the gap between consumers, green groups, and industry. Elec. J. Biotechnol. 9:424–48 [Google Scholar]
  75. Tamime AY, Deeth HC. 1980. Yoghurt: technology and biochemistry. J. Food Prot. 43:939–77 [Google Scholar]
  76. van Hylckama Vlieg JE, Rademaker JL, Bachmann H, Molenaar D, Kelly WJ, Siezen RJ. 2006. Natural diversity and adaptive responses of Lactococcus lactis. Curr. Opin. Biotechnol. 17:183–90 [Google Scholar]
  77. Wegkamp A, Teusink B, de Vos WM, Smid EJ. 2010. Development of a minimal growth medium for Lactobacillus plantarum. Lett. Appl. Microbiol. 50:57–64 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error