Early adaptation to oxygen is key to the industrially important traits of lactococcus lactis ssp. cremoris during milk fermentation

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Cretenet, Marina ^b,c,d   Le Gall, Gwenaëlle ^a   Wegmann, Udo ^a   Even, Sergine ^b,c   Shearman, Claire ^e   Stentz, Régis ^a   Jeanson, Sophie ^a,b,c,e  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UMR1253   (France)

^c AGROCAMPUS OUEST   (France)

^d UNIVERSITÉ DE CAEN   (France)

^e NONE   (France)

Author keywords

Acidification; Growth; Lactococcus lactis; Metabolomics; Oxidative stress; Redox potential; Stress response; Transcriptomics

Indexed keywords

2,3 BUTANEDIOL; ACETIC ACID; FERRICHROME; OXYGEN; PYRUVIC ACID; RIBONUCLEOTIDE REDUCTASE; TRANSCRIPTOME;

ACIDIFICATION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOLOGICAL TRAIT; CARBON METABOLISM; CONTROLLED STUDY; CULTURE MEDIUM; DAIRY INDUSTRY; EVOLUTIONARY ADAPTATION; FERMENTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; LACTOCOCCUS LACTIS SUBSP. CREMORIS; MILK; NONHUMAN; OPERON; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; OXYGEN CONSUMPTION; OXYGENATION; REDUCTION; TRANSCRIPTOMICS; ADAPTATION; ANIMAL; BOVINE; FOOD CONTROL; GENETICS; GROWTH, DEVELOPMENT AND AGING; LACTOCOCCUS LACTIS; METABOLISM; METABOLOMICS; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHENOTYPE;

LACTOCOCCUS LACTIS; LACTOCOCCUS LACTIS SUBSP. CREMORIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CATTLE; FERMENTATION; FOOD MICROBIOLOGY; LACTOCOCCUS LACTIS; METABOLOMICS; MILK; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN; PHENOTYPE; TRANSCRIPTOME;

EID: 84924284722     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1054     Document Type: Article

References (54)

1. Klaenhammer T, Altermann E, Arigoni F, Bolotin A, Breidt F, Broadbent JR, Cano R, Chaillou S, Deutscher J, Gasson MJ, Van de Guchte M, Guzzo J, Hartke A, Hawkins T, Hols P, Hutkins RW, Kleerebezem M, Kok J, Kuipers OP, Lubbers M, Maguin E, McKay L, Mills D, Nauta A, Overbeek R, Pel H, Pridmore D, Saier M, Van Sinderen D, Sorokin A, et al.: Discovering lactic acid bacteria by genomics. Antonie Van Leeuwenhoek 2002, 82:29-58.
2. Cocaign-Bousquet M, Even S, Lindley N, Loubière P: Anaerobic sugar catabolism in Lactococcus lactis: genetic regulation and enzyme control over pathway flux. Appl Microbiol Biotechnol 2002, 60:24-32. 10.1007/s00253-002-1065-x
3. Flahaut N, Wiersma A, Bunt B, Martens D, Schaap P, Sijtsma L, Santos V, 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. 10.1007/s00253-013-5140-2
4. Schleifer KH, Kraus J, Dvorak C, Kilpper-Balz R, Collins MD, Fischer W: Transfer of Streptococcus lactis and related Streptococci to the Genus Lactoccoccus gen. nov. Syst Appl Microbiol 1985, 6:183-195. 10.1016/S0723-2020(85)80052-7
5. Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A: The complete genome sequence of the lactioc acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 2001, 11:731-753. 10.1101/gr.GR-1697R
6. Wegmann U, O'Connell-Motherway M, Zomer A, Buist G, Shearman C, Canchaya C, Ventura M, Goesmann A, Gasson MJ, Kuipers OP, van Sinderen D, Kok J: Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 2007, 189:3256-3270. 10.1128/JB.01768-06
7. Linares DM, Kok J, Poolman B: Genome sequences of Lactococcus lactis MG1363 (revised) and NZ9000 and comparative physiological studies. J Bacteriol 2010, 192:5806-5812. 10.1128/JB.00533-10
8. Duwat P, Sourice S, Cesselin B, Lamberet G, Vido K, Gaudu P, Le Loir Y, Violet F, Loubière P, Gruss A: Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J Bacteriol 2001, 183:4509-4516. 10.1128/JB.183.15.4509-4516.2001
9. Gaudu P, Vido K, Cesselin B, Kulakauskas S, Tremblay J, Rezaïki L, Lamberet G, Sourice S, Duwat P, Gruss A: Respiration capacity and consequences in Lactococcus lactis . Antonie Van Leeuwenhoek 2002, 82:263-269. 10.1023/A:1020635600343
10. Rezaiki L, Cesselin B, Yamamoto Y, Vido K, Van West E, Gaudu P, Gruss A: Respiration metabolism reduces oxidative and acid stress to improve long-term survival of Lactococcus lactis. Mol Microbiol 2004, 53:1331-1342. 10.1111/j.1365-2958.2004.04217.x
11. Neves AR, Ramos A, Costa H, van Swam II, Hugenholtz J, Kleerebezem M, de Vos W, Santos H: Effect of different NADH oxidase levels on glucose metabolism by Lactococcus lactis: Kinetics of intracellular metabolite pools determined by In Vivo nuclear magnetic resonance. Appl Environ Microbiol 2002, 68:6332-6342. 10.1128/AEM.68.12.6332-6342.2002
12. Zomer AL, Buist G, Larsen R, Kok J, Kuipers OP: Time-resolved determination of the CcpA Regulon of Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 2007, 189:1366-1381. 10.1128/JB.01013-06
13. Carvalho AL, Turner DL, Fonseca LL, Solopova A, Catarino T, Kuipers OP, Eberhard OV, Neves AR, Santos H: Metabolic and transcriptional analysis of acid stress in Lactococcus lactis , with a focus on the kinetics of lactic acid pools. PLoS ONE 2013, 8:e68470. 10.1371/journal.pone.0068470
14. de Jong A, Hansen ME, Kuipers OP, Kilstrup M, Kok J: The transcriptional and gene regulatory network of Lactococcus lactis MG1363 during growth in milk. PLoS ONE 2013, 8:e53085. 10.1371/journal.pone.0053085
15. Cretenet M, Laroute V, Ulve V, Jeanson S, Nouaille S, Even S, Piot M, Girbal L, Le Loir Y, Loubiere P, Lortal S, Cocaign-Bousquet M: Dynamic analysis of the Lactococcus lactis transcriptome in cheeses made from milk concentrated by ultrafiltration reveals multiple strategies of adaptation to stresses. Appl Environ Microbiol 2011, 77:247-257. 10.1128/AEM.01174-10
16. Dressaire C, Redon E, Milhem H, Besse P, Loubiere P, Cocaign-Bousquet M: Growth rate regulated genes and their wide involvement in the Lactococcus lactis stress responses. BMC Genomics 2008, 9:343. 10.1186/1471-2164-9-343
17. Raynaud S, Perrin R, Cocaign-Bousquet M, Loubiere P: Metabolic and transcriptomic adaptation of Lactococcus lactis subsp. lactis biovar diacetylactis in response to autoacidification and temperature downshift in skim milk. Appl Environ Microbiol 2005, 71:8016-8023. 10.1128/AEM.71.12.8016-8023.2005
18. Redon E, Loubiere P, Cocaign-Bousquet M: Transcriptome analysis of the progressive adaptation of Lactococcus lactis to carbon starvation. J Bacteriol 2005, 187:3589-3592. 10.1128/JB.187.10.3589-3592.2005
19. Xie Y, Chou L, Cutler A, Weimer B: DNA macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Appl Environ Microbiol 2004, 70:6738-6747. 10.1128/AEM.70.11.6738-6747.2004
20. Abraham S, Cachon R, Jeanson S, Ebel B, Michelon D, Aubert C, Rojas C, Feron G, Beuvier E, Gervais P, De Conink J: A procedure for reproducible measurement of redox potential (Eh) in dairy processes. Dairy Sci Technol 2013, 93:1-16. 10.1007/s13594-012-0091-4
21. Tengerdy R: Redox potential changes in 2-keto-L-gulonic acid fermentation. I-Correlation betweenredox potential and dissolved oxygen concentration. J Biotechnol Microbiol Technol Eng 1961, 3:241-253.
22. Aubert C, Capelle N, Jeanson S, Eckert H, Diviès C, Cachon R: Le potentiel d'oxydoréduction et sa prise en compte dans les procédés d'utilisation des bactéries lactiques. Sci Aliments 2002, 22:177-187. 10.3166/sda.22.177-187
23. Jeanson S, Hilgert N, Coquillard MO, Seukpanya C, Faiveley M, Neveu P, Abraham C, Georgescu V, Fourcassié P, Beuvier E: Milk acidification by Lactococcus lactis is improved by decreasing the level of dissolved oxygen rather than decreasing redox potential in the milk prior to inoculation. Int J Food Microbiol 2009, 131:75-81. 10.1016/j.ijfoodmicro.2008.09.020
24. Cachon R, Jeanson S, Aldarf M, Diviès C: Characterization of lactic starters based on acidification and reduction activities. Lait 2002, 82:281-288. 10.1051/lait:2002010
25. Cesselin B, Derré-Bobillot A, Fernanadez A, Lamberet G, Lechardeur D, Yamamoto Y, Pedersen MB, Garrigues C, Gruss A, Gaudu P: Responses of Lactic Acid Bacteria to Oxidative Stress. In Stress Responses of Lactic Acid Bacteria. Food Microbiology and Food Safety edition. Edited by: Tsakalidou E, Papadimitriou K. Springer Science; 2011:111-127.
26. Duwat P, Cesselin B, Sourice S, Gruss A: Lactococcus lactis , a bacterial model for stress responses and survival. Int J Food Microbiol 2000, 55:83-86. 10.1016/S0168-1605(00)00179-3
27. Miyoshi A, Rochat T, Gratadoux J-J, LeLoir Y, Costa Oliveira S, Langella P, Azevedo V: Oxidative stress in Lactococcus lactis . Genet Mol Res 2003, 2:348-359.
28. Neves AR, Pool WA, Kok J, Kuipers OP, Santos H: Overview on sugar metabolism and its control in Lactococcus lactis - the input from in vivo NMR. FEMS Microbiol Rev 2005, 29:531-554.
29. Oliveira A, Nielsen J, Forster J: Modeling Lactococcus lactis using a genome-scale flux model. BMC Microbiol 2005, 5:39. 10.1186/1471-2180-5-39
30. Gasson MJ, Godon JJ, Pillidge CJ, Eaton TJ, Jury K, Shearman CA: Characterization and exploitation of conjugation in Lactococcus lactis . Int Dairy J 1995, 5:757-762. 10.1016/0958-6946(95)00030-5
31. Pedersen MB, Garrigues C, Tuphile K, Brun C, Vido K, Bennedsen M, Møllgaard H, Gaudu P, Gruss A: Impact of Aeration and Heme-activated respiration on Lactococcus lactis gene expression: identification of a heme-responsive operon. J Bacteriol 2008, 190:4903-4911. 10.1128/JB.00447-08
32. Tachon S, Brandsma JB, Yvon M: NoxE NADH oxidase and the electron transport chain are responsible for the ability of Lactococcus lactis to decrease the redox potential of milk. Appl Environ Microbiol 2010, 76:1311-1319. 10.1128/AEM.02120-09
33. Jensen NBS, Melchiorsen CR, Jokumsen KV, Villadsen J: Metabolic behavior of Lactococcus lactis MG1363 in microaerobic continuous cultivation at a low dilution rate. Appl Environ Microbiol 2001, 67:2677-2682. 10.1128/AEM.67.6.2677-2682.2001
34. Kimoto-Nira H, Moriya N, Ohmori H, Suzuki C: Altered superoxide dismutase activity by carbohydrate utilization in a Lactococcus lactis strain. J Food Protect 2014, 77:1161-1167. 10.4315/0362-028X.JFP-13-475
35. Jordan A, Pontis E, Aslund F, Hellman U, Gibert I, Reichard P: The ribonuclease reductase system of Lactococcus lactis . J Chem Biol 1996, 271:8779-8785. 10.1074/jbc.271.15.8779
36. Torrents E, Eliasson R, Wolpher H, Graslund A, Reichard P: The anaerobic ribonucleotide reductase from Lactococcus lactis . J Chem Biol 2001, 276:33488-33494. 10.1074/jbc.M103743200
37. Vido K, Diemer H, Van Dorsselaer A, Leize E, Juillard V, Gruss A, Gaudu P: Roles of thioredoxin reductase during the aerobic life of Lactococcus lactis . J Bacteriol 2005, 187:601-610. 10.1128/JB.187.2.601-610.2005
38. Nakano S, Küster-Schöck E, Grossman AD, Zuber P: Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis . Proc Natl Acad Sci U S A 2003, 100:13603-13608. 10.1073/pnas.2235180100
39. Li Y, Hugenholtz J, Abee T, Molenaar D: Glutathione protects Lactococcus lactis against oxidative stress. Appl Environ Microbiol 2003, 69:5739-5745. 10.1128/AEM.69.10.5739-5745.2003
40. Ravcheev DA, Li X, Latif H, Zengler K, Leyn SA, Korostelev YD, Kazakov AE, Novichkov PS, Osterman AL, Rodionov DA: Transcriptional regulation of central carbon and energy metabolism in bacteria by redox-responsive repressor rex. J Bacteriol 2012, 194:1145-1157. 10.1128/JB.06412-11
41. Turner MS, Tan YP, Giffard PM: Inactivation of an iron transporter in Lactococcus lactis results in resistance to tellurite and oxidative stress. Appl Environ Microbiol 2007, 73:6144-6149. 10.1128/AEM.00413-07
42. Frees D, Varmanen P, Ingmer H: Inactivation of a gene that is highly conserved in Gram-positive bacteria stimulates degradation of non-native proteins and concomitantly increases stress tolerance in Lactococcus lactis . Mol Microbiol 2001, 41:93-103. 10.1046/j.1365-2958.2001.02503.x
43. Smith WM, Dykes GA, Soomro AH, Turner MS: Molecular Mechanisms of Stress Resistance in Lactococcus Lactis . In Topics in Applied Microbiology and Microbial Biotechnology. Edited by: Mendez-Vilas A. Badajoz, Spain: Formatex Reasearch Center; 2010:1106-1118.
44. Rallu F, Gruss A, Maguin E: Lactococcus lactis and stress. Antonie Van Leeuwenhoek 1996, 70:243-251. 10.1007/BF00395935
45. Cocaign-Bousquet M, Garrigues C, Loubiere P, Lindley ND: Physiology of pyruvate metabolism in Lactococcus lactis . Antonie Van Leeuwenhoek 1996, 70:253-267. 10.1007/BF00395936
46. Ganesan B, Stuart MR, Weimer BC: Carbohydrate starvation causes a metabolically active but nonculturable state in Lactococcus lactis. Appl Environ Microbiol 2007, 73:2498-2512. 10.1128/AEM.01832-06
47. Stentz R, Wegmann U, Parker M, Bongaerts R, Lesaint L, Gasson M, Shearman C: CsiA is a bacterial cell wall synthesis inhibitor contributing to DNA translocation through the cell envelope. Mol Microbiol 2009, 72:779-794. 10.1111/j.1365-2958.2009.06683.x
48. Aminov RI: Horizontal gene exchange in environmental microbiota. Front Microbiol 2011, 2:158.
49. Gasson MJ: Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol 1983, 154:1-9.
50. Wegmann U, Overweg K, Jeanson S, Gasson M, Shearman C: Molecular characterisation and structural instability of the industrially important composite metabolic plasmid pLP712. Microbiology 2012, 158:2936-2945. 10.1099/mic.0.062554-0
51. 1 H NMR metabolomics data. Anal Chem 2006, 78:4430-4442. 10.1021/ac060209g
52. R Development Core Team: R: A Langage and Environment for Statistical Computing. Vienna, Austria: R Fondation for Statistical Computing; 2008.
53. Waters CM, Dunny GM: Analysis of functional domains of the Enterococcus faecalis pheromone-induced surface protein aggregation substance. J Bacteriol 2001, 183:5659-5667. 10.1128/JB.183.19.5659-5667.2001
54. Stentz R, Jury K, Eaton T, Parker M, Narbad A, Gasson M, Shearman C: Controlled expression of CluA in Lactococcus lactis and its role in conjugation. Microbiology 2004, 150:2503-2512. 10.1099/mic.0.27149-0