Genotypic and phenotypic analysis of dairy lactococcus lactis biodiversity in milk: Volatile organic compounds as discriminating markers

Applied and Environmental Microbiology

Volumn 79, Issue 15, 2013, Pages 4643-4652

  Dhaisne, Amandine ^a,b,c   Guellerin, Maeva ^a,d   Laroute, Valérie ^a,b,c   Laguerre, Sandrine ^a,b,c   Cocaign Bousquet, Muriel ^a,b,c   Bourgeois, Pascal Le ^a,d   Loubiere, Pascal ^a,b,c  

^a INSA   (France)

^b UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^c CNRS   (France)

^d UPS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENOTYPIC DIVERSITY; MULTILOCUS SEQUENCE TYPING; PHENOTYPIC ANALYSIS; PHENOTYPIC CHARACTERS; PHENOTYPIC DIVERSITY; PHENOTYPIC VARIABLES; PULSED FIELD GEL ELECTROPHORESIS; VARIABLE SELECTION;

BIODIVERSITY; DAIRIES; ELECTROPHORESIS; METABOLISM; PRINCIPAL COMPONENT ANALYSIS; VOLATILE ORGANIC COMPOUNDS;

STRAIN;

BIOLOGICAL MARKER; VOLATILE ORGANIC COMPOUND;

BACTERIUM; DAIRY FARMING; ELECTROKINESIS; FERMENTATION; GENETIC DIFFERENTIATION; GENOTYPE; MILK; PHENOTYPE; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; VOLATILE ORGANIC COMPOUND;

ANIMAL; ARTICLE; CLASSIFICATION; FERMENTATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; LACTOCOCCUS LACTIS; METABOLISM; MICROBIOLOGY; MILK; MULTILOCUS SEQUENCE TYPING; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PULSED FIELD GEL ELECTROPHORESIS;

ANIMALS; BIOLOGICAL MARKERS; ELECTROPHORESIS, GEL, PULSED-FIELD; FERMENTATION; GENETIC VARIATION; GENOTYPE; LACTOCOCCUS LACTIS; MILK; MULTILOCUS SEQUENCE TYPING; PHENOTYPE; PHYLOGENY; POLYMERASE CHAIN REACTION; VOLATILE ORGANIC COMPOUNDS;

EID: 84880672123     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01018-13     Document Type: Article

References (50)

1. Schleifer KH, Kraus J, Dvorak C, Kilpper-Bälz R, Collins MD, Fischer W. 1985. Transfer of Streptococcus lactis and related streptococci to the genus Lactococcus gen. nov. Syst. Appl. Microbiol. 6:183-195.
2. Klijn N, Weerkamp AH, de Vos WM. 1995. Detection and characterization of lactose-utilizing Lactococcus spp. in natural ecosystems. Appl. Environ. Microbiol. 61:788-792.
3. Kelly W, Ward L. 2002. Genotypic vs. phenotypic biodiversity in Lactococcus lactis. Microbiology 148:3332-3333.
4. Salama MS, Sandine WE, Giovannoni SJ. 1993. Isolation of Lactococcus lactis subsp. cremoris from nature by colony hybridization with rRNA probes. Appl. Environ. Microbiol. 59:3941-3945.
5. Rademaker JL, Herbet H, Starrenburg MJ, Naser SM, Gevers D, Kelly WJ, Hugenholtz J, Swings J, van Hylckama Vlieg JE. 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. 73:7128-7137.
6. Passerini D, Beltramo C, Coddeville M, Quentin Y, Ritzenthaler P, Daveran-Mingot ML, Le Bourgeois P. 2010. Genes but not genomes reveal bacterial domestication of Lactococcus lactis. PLoS One 5:e15306. doi:10.1371/journal.pone.0015306.
7. Fernández E, Alegría A, Delgado S, Martín MC, Mayo B. 2011. Comparative phenotypic and molecular genetic profiling of wild Lactococcus lactis subsp. lactis strains of the L. lactis subsp. lactis and L. lactis subsp. cremoris genotypes, isolated from starter-free cheeses made of raw milk. Appl. Environ. Microbiol. 77:5324-5335.
8. Siezen RJ, Bayjanov JR, Felis GE, van der Sijde MR, Starrenburg M, Molenaar D, Wels M, van Hijum SA, van Hylckama Vlieg JE. 2011. Genome-scale diversity and niche adaptation analysis of Lactococcus lactis by comparative genome hybridization using multi-strain arrays. Microb. Biotechnol. 4:383-402.
9. Taïbi A, Dabour N, Lamoureux M, Roy D, LaPointe G. 2010. Evaluation of the genetic polymorphism among Lactococcus lactis subsp. cremoris strains using comparative genomic hybridization and multilocus sequence analysis. Int. J. Food Microbiol. 144:20-28.
10. Cachon R, Jeanson S, Aldarf M, Divies C. 2002. Characterisation of lactic starters based on acidification and reduction activities. Lait 82:281-288.
11. Brasca M, Morandi S, Lodi R, Tamburini A. 2007. Redox potential to discriminate among species of lactic acid bacteria. J. Appl. Microbiol. 103: 1516-1524.
12. Kristo E, Biliaderis CG, Tzanetakis N. 2003. Modelling of the acidification process and rheological properties of milk fermented with a yogurt starter culture using response surface methodology. Food Chem. 83:437-446.
13. Cheng H. 2010. Volatile flavor compounds in yogurt: a review. Crit. Rev. Food Sci. Nutr. 50:938-950.
14. Smit G, Smit BA, Engels WJ. 2005. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol. Rev. 29:591-610.
15. Aly S, Floury J, Piot M, Lortal S, Jeanson S. 2012. The efficacy of nisin can drastically vary when produced in situ in model cheeses. Food Microbiol. 32:185-190.
16. Hickey RM, Ross RP, Hill C. 2004. Controlled autolysis and enzyme release in a recombinant lactococcal strain expressing the metalloendopeptidase enterolysin A. Appl. Environ. Microbiol. 70:1744-1748.
17. Valence F, Deutsch SM, Richoux R, Gagnaire V, Lortal S. 2000. Autolysis and related proteolysis in Swiss cheese for two Lactobacillus helveticus strains. J. Dairy Res. 67:261-271.
18. Bachmann H, Starrenburg MJ, Dijkstra A, Molenaar D, Kleerebezem M, Rademaker JL, van Hylckama Vlieg JE. 2009. Regulatory phenotyping reveals important diversity within the species Lactococcus lactis. Appl. Environ. Microbiol. 75:5687-5694.
19. Bayjanov JR, Molenaar D, Tzeneva V, Siezen RJ, van Hijum SA. 2012. PhenoLink-a web-tool for linking phenotype to ~omics data for bacteria: application to gene-trait matching for Lactobacillus plantarum strains. BMC Genomics 13:170. doi:10.1186/1471-2164-13-170.
20. Bayjanov JR, Starrenburg MJ, van der Sijde MR, Siezen RJ, van Hijum SA. 2013. Genotype-phenotype matching analysis of 38 Lactococcus lactis strains using random forest methods. BMC Microbiol. 13:68. doi:10.1186/1471-2180-13-68.
21. Tan-a-ram P, Cardoso T, Daveran-Mingot ML, Kanchanatawee S, Loubière P, Girbal L, Cocaign-Bousquet M. 2011. Assessment of the diversity of dairy Lactococcus lactis subsp. lactis isolates by an integrated approach combining phenotypic, genomic, and transcriptomic analyses. Appl. Environ. Microbiol. 77:739-748.
22. Kütahya OE, Starrenburg MJ, Rademaker JL, Klaassen CH, van Hylckama Vlieg JE, Smid EJ, Kleerebezem M. 2011. High-resolution ampli-fied fragment length polymorphism typing of Lactococcus lactis strains enables identification of genetic markers for subspecies-related phenotypes. Appl. Environ. Microbiol. 77:5192-5198.
23. Taïbi A, Dabour N, Lamoureux M, Roy D, LaPointe G. 2011. Comparative transcriptome analysis of Lactococcus lactis subsp. cremoris strains under conditions simulating cheddar cheese manufacture. Int. J. Food Microbiol. 146:263-275.
24. Cocaign-Bousquet M, Lindley ND. 1995. Pyruvate overflow and carbon flux within the central metabolic pathways of Corynebacterium glutamicum during growth on lactate. Enzyme Microb. Technol. 17:260-267.
25. Nouaille S, Even S, Charlier C, Le Loir Y, Cocaign-Bousquet M, Loubière P. 2009. Transcriptomic response of Lactococcus lactis in mixed culture with Staphylococcus aureus. Appl. Environ. Microbiol. 75:4473-4482.
26. Tanigawa K, Kawabata H, Watanabe K. 2010. Identification and typing of Lactococcus lactis by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl. Environ. Microbiol. 76:4055-4062.
27. Le Bourgeois P, Lautier M, van den Berghe L, Gasson MJ, Ritzenthaler P. 1995. Physical and genetic map of the Lactococcus lactis subsp. cremoris MG1363 chromosome: comparison with that of Lactococcus lactis subsp. lactis IL 1403 reveals a large genome inversion. J. Bacteriol. 177:2840-2850.
28. Nelson RJ. 1994. Relationship between phylogeny and pathotype for the bacterial blight pathogen of rice. Appl. Environ. Microbiol. 60:3275-3283.
29. Felsenstein J. 1989. PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164-166.
30. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Stat. Methodol. 57:289-300.
31. Lê Cao K-A, González I, Déjean S. 2009. integrOmics: an R package to unravel relationships between two omics datasets. Bioinformatics 25: 2855-2856.
32. Ward JH. 1963. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58:236-244.
33. Shen H, Huang JZ. 2008. Sparse principal component analysis via regularized low rank matrix approximation. J. Multivariate Anal. 99:1015-1034.
34. David S, van der Rest ME, Driessen AJ, Simons G, de Vos WM. 1990. Nucleotide sequence and expression in Escherichia coli of the Lactococcus lactis citrate permease gene. J. Bacteriol. 172:5789-5794.
35. Le Bourgeois P, Daveran-Mingot ML, Ritzenthaler P. 2000. Genome plasticity among related Lactococcus strains: identification of genetic events associated with macrorestriction polymorphisms. J. Bacteriol. 182: 2481-2491.
36. Collins YF, McSweeney PL, Wilkinson MG. 2003. Lipolysis and free fatty acid catabolism in cheese: a review of current knowledge. Int. Dairy J. 13:841-866.
37. Fox PF, Wallace JM. 1997. Formation of flavor compounds in cheese. Adv. Appl. Microbiol. 45:17-85.
38. McSweeney PL, Sousa MJ. 2000. Biochemical pathways for the production of flavour compounds in cheeses during ripening: a review. Lait 80:32.
39. Bemiller J, Huber K. 2007. Carbohydrates, p 83-155. In Damodaran S, Parkin KL, Fennema OR (ed), Fennema's food chemistry, 4th ed. CRC Press, New York, NY.
40. Gutiérrez-Méndez N, Vallejo-Cordoba B, González-Córdova AF, Nevárez-Moorillón GV, Rivera-Chavira B. 2008. Evaluation of aroma generation of Lactococcus lactis with an electronic nose and sensory analysis. J. Dairy Sci. 91:49-57.
41. Bayjanov JR, Wels M, Starrenburg M, van Hylckama Vlieg JE, Siezen RJ, Molenaar D. 2009. PanCGH: a genotype-calling algorithm for pangenome CGH data. Bioinformatics 25:309-314.
42. 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. 17:183-190.
43. Kelly WJ, Ward LJ, Leahy SC. 2010. Chromosomal diversity in Lactococcus lactis and the origin of dairy starter cultures. Genome Biol. Evol. 2:729-744.
44. Salama MS, Musafija-Jeknic T, Sandine WE, Giovannoni SJ. 1995. An ecological study of lactic acid bacteria: isolation of new strains of Lactococcus including Lactococcus lactis subspecies cremoris. J. Dairy Sci. 78:1004-1017.
45. Hansen EB. 2002. Commercial bacterial starter cultures for fermented foods of the future. Int. J. Food Microbiol. 78:119-131.
46. de Bok FA, Janssen PW, Bayjanov JR, Sieuwerts S, Lommen A, van Hylckama Vlieg JE, Molenaar D. 2011. Volatile compound fingerprinting of mixed-culture fermentations. Appl. Environ. Microbiol. 77:6233-6239.
47. 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. 97:306-313.
48. Chipman D, Barak Z, Schloss JV. 1998. Biosynthesis of 2-aceto-2-hydroxy acids: acetolactate synthases and acetohydroxyacid synthases. Biochim. Biophys. Acta 1385:401-419.
49. Smit BA, Engels WJ, Smit G. 2009. Branched chain aldehydes: production and breakdown pathways and relevance for flavour in foods. Appl. Microbiol. Biotechnol. 81:987-999.
50. Passerini D, Laroute V, Coddeville M, Le Bourgeois P, Loubière P, Ritzenthaler P, Cocaign-Bousquet M, Daveran-Mingot ML. 2013. New insights into Lactococcus lactis diacetyl-and acetoin-producing strains isolated from diverse origins. Int. J. Food Microbiol. 160:329-336.