Lactobacillus casei Low-Temperature, Dairy-Associated Proteome Promotes Persistence in the Mammalian Digestive Tract

Journal of Proteome Research

Volumn 14, Issue 8, 2015, Pages 3136-3147

  Lee, Bokyung ^a   Tachon, Sybille ^a   Eigenheer, Richard A ^a   Phinney, Brett S ^a   Marco, Maria L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

dairy; IBD; intestinal fitness; Lactobacillus casei; low temperature; mass spectrometry; microbiota; milk; probiotics; proteomics

Indexed keywords

3 OXOACYL ACP SYNTHASE; BACTERIAL PROTEIN; DEXTRO ALANINE TRANSFER PROTEIN; ION; PROBIOTIC AGENT; RECOMBINASE; RECOMBINASE A; SUPEROXIDE DISMUTASE; SYNTHETASE; UNCLASSIFIED DRUG; 3 OXOACYL ACYL CARRIER PROTEIN SYNTHASE; CULTURE MEDIUM; DLTD PROTEIN, BACTERIA; PROTEOME; RECA PROTEIN; THIOL ESTER HYDROLASE;

AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE TRANSPORT; CELL SURFACE; CONTROLLED STUDY; DIGESTIVE SYSTEM; ENERGY YIELD; ENZYME INACTIVATION; FATTY ACID METABOLISM; FEMALE; LACTOBACILLUS CASEI; LOW TEMPERATURE; MILK; MOUSE; NONHUMAN; NUCLEOTIDE METABOLISM; NUCLEOTIDE TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN SYNTHESIS; TANDEM MASS SPECTROMETRY; ADAPTATION; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; COLD; CULTURE MEDIUM; DRUG EFFECTS; GASTROINTESTINAL TRACT; GENETICS; LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; MUTATION; PHARMACOLOGY; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; PROTEOMICS;

LACTOBACILLUS CASEI; MAMMALIA;

3-OXOACYL-(ACYL-CARRIER-PROTEIN) SYNTHASE; ADAPTATION, PHYSIOLOGICAL; ANIMALS; BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; COLD TEMPERATURE; CULTURE MEDIA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; GASTROINTESTINAL TRACT; LACTOBACILLUS CASEI; MICE, INBRED BALB C; MILK; MUTATION; PROBIOTICS; PROTEOME; PROTEOMICS; REC A RECOMBINASES; SUPEROXIDE DISMUTASE; TANDEM MASS SPECTROMETRY; THIOLESTER HYDROLASES;

EID: 84938794096     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00387     Document Type: Article

References (109)

1. Sanders, M. E.; Guarner, F.; Guerrant, R.; Holt, P. R.; Quigley, E. M.; Sartor, R. B.; Sherman, P. M.; Mayer, E. A. An update on the use and investigation of probiotics in health and disease Gut 2013, 62, 787-96 10.1136/gutjnl-2012-302504
2. Bron, P. A.; van Baarlen, P.; Kleerebezem, M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa Nat. Rev. Microbiol. 2012, 10, 66-90 10.1038/nrmicro2690
3. Lebeer, S.; Vanderleyden, J.; De Keersmaecker, S. C. J. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens Nat. Rev. Microbiol. 2010, 8, 171-184 10.1038/nrmicro2297
4. Marco, M. L.; Tachon, S. Environmental factors influencing the efficacy of probiotic bacteria Curr. Opin. Biotechnol. 2013, 24, 207-213 10.1016/j.copbio.2012.10.002
5. Sanders, M. E.; Marco, M. L. Food formats for effective delivery of probiotics Annu. Rev. Food Sci. Technol. 2010, 1, 65-85 10.1146/annurev.food.080708.100743
6. Wang, J.; Guo, Z.; Zhang, Q.; Yan, L.; Chen, W.; Liu, X. M.; Zhang, H. P. Fermentation characteristics and transit tolerance of probiotic Lactobacillus casei Zhang in soymilk and bovine milk during storage J. Dairy Sci. 2009, 92, 2468-2476 10.3168/jds.2008-1849
7. da Conceicao, L. L.; Leandro, E. S.; Freitas, F. S.; de Oliveira, M. N.; Ferreira-Machado, A. B.; Borges, A. C.; de Moraes, C. A. Survival of Lactobacillus delbrueckii UFV H2b20 in fermented milk under simulated gastric and intestinal conditions Benefic. Microbes 2013, 4, 285-289 10.3920/BM2013.0003
8. Faye, T.; Tamburello, A.; Vegarud, G. E.; Skeie, S. Survival of lactic acid bacteria from fermented milks in an in vitro digestion model exploiting sequential incubation in human gastric and duodenum juice J. Dairy Sci. 2012, 95, 558-566 10.3168/jds.2011-4705
9. Martinez, R. C.; Aynaou, A. E.; Albrecht, S.; Schols, H. A.; De Martinis, E. C.; Zoetendal, E. G.; Venema, K.; Saad, S. M.; Smidt, H. In vitro evaluation of gastrointestinal survival of Lactobacillus amylovorus DSM 16698 alone and combined with galactooligosaccharides, milk and/or Bifidobacterium animalis subsp. lactis Bb-12 Int. J. Food Microbiol. 2011, 149, 152-158 10.1016/j.ijfoodmicro.2011.06.010
10. Haque, E.; Chand, R. Antihypertensive and antimicrobial bioactive peptides from milk proteins Eur. Food Res. Technol. 2008, 227, 7-15 10.1007/s00217-007-0689-6
11. Gonzalez, R.; Klaassens, E. S.; Malinen, E.; de Vos, W. M.; Vaughan, E. E. Differential transcriptional response of Bifidobacterium longum to human milk, formula milk, and galactooligosaccharide Appl. Environ. Microbiol. 2008, 74, 4686-4694 10.1128/AEM.00122-08
12. He, T.; Venema, K.; Priebe, M. G.; Welling, G. W.; Brummer, R. J. M.; Vonk, R. J. The role of colonic metabolism in lactose intolerance Eur. J. Clin. Invest. 2008, 38, 541-547 10.1111/j.1365-2362.2008.01966.x
13. Sela, D. A. Bifidobacterial utilization of human milk oligosaccharides Int. J. Food Microbiol. 2011, 149, 58-64 10.1016/j.ijfoodmicro.2011.01.025
14. Sela, D. A.; Chapman, J.; Adeuya, A.; Kim, J. H.; Chen, F.; Whitehead, T. R.; Lapidus, A.; Rokhsar, D. S.; Lebrilla, C. B.; German, J. B.; Price, N. P.; Richardson, P. M.; Mills, D. A. The genome sequence of Bifidobacterium longum subsp infantis reveals adaptations for milk utilization within the infant microbiome Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 18964-18969 10.1073/pnas.0809584105
15. Ward, R. E.; Ninonuevo, M.; Mills, D. A.; Lebrilla, C. B.; German, J. B. In vitro fermentation of breast milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri Appl. Environ. Microbiol. 2006, 72, 4497-4499 10.1128/AEM.02515-05
16. Azcarate-Peril, M. A.; Tallon, R.; Klaenhammer, T. R. Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk J. Dairy Sci. 2009, 92, 870-886 10.3168/jds.2008-1457
17. Turroni, F.; Foroni, E.; Serafini, F.; Viappiani, A.; Montanini, B.; Bottacini, F.; Ferrarini, A.; Bacchini, P. L.; Rota, C.; Delledonne, M.; Ottonello, S.; van Sinderen, D.; Ventura, M. Ability of Bifidobacterium breve to grow on different types of milk: exploring the metabolism of milk through genome analysis Appl. Environ. Microbiol. 2011, 77, 7408-7417 10.1128/AEM.05336-11
18. Wang, J. C.; Wu, R. N.; Zhang, W. Y.; Sun, Z. H.; Zhao, W. J.; Zhang, H. P. Proteomic comparison of the probiotic bacterium Lactobacillus casei Zhang cultivated in milk and soy milk J. Dairy Sci. 2013, 96, 5603-5624 10.3168/jds.2013-6927
19. Ashraf, R.; Shah, N. P. Immune system stimulation by probiotic microorganisms Crit. Rev. Food Sci. Nutr. 2014, 54, 938-956 10.1080/10408398.2011.619671
20. Saxelin, M.; Tynkkynen, S.; Mattila-Sandholm, T.; de Vos, W. M. Probiotic and other functional microbes: from markets to mechanisms Curr. Opin. Biotechnol. 2005, 16, 204-211 10.1016/j.copbio.2005.02.003
21. Guillemard, E.; Tondu, F.; Lacoin, F.; Schrezenmeir, J. Consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114001 reduces the duration of respiratory infections in the elderly in a randomised controlled trial Br. J. Nutr. 2010, 103, 58-68 10.1017/S0007114509991395
22. Giralt, J.; Regadera, J. P.; Verges, R.; Romero, J.; de la Fuente, I.; Biete, A.; Villoria, J.; Cobo, J. M.; Guarner, F. Effects of probiotic Lactobacillus casei DN-114 001 in prevention of radiation-induced diarrhea: Results from multicenter, randomized, placebo-controlled nutritional trial Int. J. Radiat. Oncol., Biol., Phys. 2008, 71, 1213-1219 10.1016/j.ijrobp.2007.11.009
23. Pedone, C. A.; Bernabeu, A. O.; Postaire, E. R.; Bouley, C. F.; Reinert, P. The effect of supplementation with milk fermented by Lactobacillus casei (strain DN-114 001) on acute diarrhoea in children attending day care centres Int. J. Clin. Pract. 1999, 53, 179-184
24. Wong, S.; Jamous, A.; ODriscoll, J.; Sekhar, R.; Weldon, M.; Yau, C. Y.; Hirani, S. P.; Grimble, G.; Forbes, A. A Lactobacillus casei Shirota probiotic drink reduces antibiotic-associated diarrhoea in patients with spinal cord injuries: a randomised controlled trial Br. J. Nutr. 2014, 111, 672-678 10.1017/S0007114513002973
25. Vaghef-Mehrabany, E.; Alipour, B.; Homayouni-Rad, A.; Sharif, S. K.; Asghari-Jafarabadi, M.; Zavvari, S. Probiotic supplementation improves inflammatory status in patients with rheumatoid arthritis Nutrition 2014, 30, 430-435 10.1016/j.nut.2013.09.007
26. Cai, H.; Thompson, R.; Budinich, M. F.; Broadbent, J. R.; Steele, J. L. Genome sequence and comparative genome analysis of Lactobacillus casei: Insights into their niche-associated evolution Genome Biol. Evol. 2010, 1, 239-257 10.1093/gbe/evp019
27. Ai, L. Z.; Chen, C.; Zhou, F. F.; Wang, L.; Zhang, H.; Chen, W.; Guo, B. H. Complete genome sequence of the probiotic strain Lactobacillus casei BD-II J. Bacteriol. 2011, 193, 3160-3161 10.1128/JB.00421-11
28. Douillard, F. P.; Kant, R.; Ritari, J.; Paulin, L.; Palva, A.; de Vos, W. M. Comparative genome analysis of Lactobacillus casei strains isolated from Actimel and Yakult products reveals marked similarities and points to a common origin Microb. Biotechnol. 2013, 6, 576-587 10.1111/1751-7915.12062
29. Douillard, F. P.; Ribbera, A.; Jarvinen, H. M.; Kant, R.; Pietila, T. E.; Randazzo, C.; Paulin, L.; Laine, P. K.; Caggia, C.; von Ossowski, I.; Reunanen, J.; Satokari, R.; Salminen, S.; Palva, A.; de Vos, W. M. Comparative genomic and functional analysis of Lactobacillus casei and Lactobacillus rhamnosus strains marketed as probiotics Appl. Environ. Microbiol. 2013, 79, 1923-1933 10.1128/AEM.03467-12
30. Broadbent, J. R.; Neeno-Eckwall, E. C.; Stahl, B.; Tandee, K.; Cai, H.; Morovic, W.; Horvath, P.; Heidenreich, J.; Perna, N. T.; Barrangou, R.; Steele, J. L. Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation BMC Genomics 2012, 13, 533 10.1186/1471-2164-13-533
31. Maze, A.; Boel, G.; Zuniga, M.; Bourand, A.; Loux, V.; Yebra, M. J.; Monedero, V.; Correia, K.; Jacques, N.; Beaufils, S.; Poncet, S.; Joyet, P.; Milohanic, E.; Casaregola, S.; Auffray, Y.; Perez-Martinez, G.; Gibrat, J. F.; Zagorec, M.; Francke, C.; Hartke, A.; Deutscher, J. Complete genome sequence of the probiotic Lactobacillus casei strain BL23 J. Bacteriol. 2010, 192, 2647-2648 10.1128/JB.00076-10
32. Zhang, W. Y.; Yu, D. L.; Sun, Z. H.; Wu, R. N.; Chen, X.; Chen, W.; Meng, H.; Hu, S. N.; Zhang, H. P. Complete genome sequence of Lactobacillus casei Zhang, a new probiotic strain isolated from traditional homemade koumiss in Inner Mongolia, China J. Bacteriol. 2010, 192, 5268-5269 10.1128/JB.00802-10
33. Acedo-Felix, E.; Perez-Martinez, G. Significant differences between Lactobacillus casei subsp. casei ATCC 393T and a commonly used plasmid-cured derivative revealed by a polyphasic study Int. J. Syst. Evol. Microbiol. 2010, 53, 67-75 10.1099/ijs.0.02325-0
34. Oozeer, R.; Goupil-Feuillerat, N.; Alpert, C. A.; van de Guchte, M.; Anba, J.; Mengaud, J.; Corthier, G. Lactobacillus casei is able to survive and initiate protein synthesis during its transit in the digestive tract of human flora-associated mice Appl. Environ. Microbiol. 2002, 68, 3570-3574 10.1128/AEM.68.7.3570-3574.2002
35. Oozeer, R.; Mater, D. D. G.; Goupil-Feuillerat, N.; Corthier, G. Initiation of protein synthesis by a labeled derivative of the Lactobacillus casei DN-114 001 strain during transit from the stomach to the cecum in mice harboring human microbiota Appl. Environ. Microbiol. 2004, 70, 6992-6997 10.1128/AEM.70.12.6992-6997.2004
36. Foligne, B.; Nutten, S.; Grangette, C.; Dennin, V.; Goudercourt, D.; Poiret, S.; Dewulf, J.; Brassart, D.; Mercenier, A.; Pot, B. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria World J. Gastroenterol. 2007, 13, 236-243
37. Rochat, T.; Bermudez-Humaran, L.; Gratadoux, J. J.; Fourage, C.; Hoebler, C.; Corthier, G.; Langella, P. Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice Microb. Cell Fact. 2007, 6, 22 10.1186/1475-2859-6-22
38. Watterlot, L.; Rochat, T.; Sokol, H.; Cherbuy, C.; Bouloufa, I.; Lefevre, F.; Gratadoux, J. J.; Honvo-Hueto, E.; Chilmonczyk, S.; Blugeon, S.; Corthier, G.; Langella, P.; Bermudez-Humaran, L. G. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice Int. J. Food Microbiol. 2010, 144, 35-41 10.1016/j.ijfoodmicro.2010.03.037
39. Archambaud, C.; Nahori, M. A.; Soubigou, G.; Becavin, C.; Laval, L.; Lechat, P.; Smokvina, T.; Langella, P.; Lecuit, M.; Cossart, P. Impact of lactobacilli on orally acquired listeriosis Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 16684-16689 10.1073/pnas.1212809109
40. Revilla-Guarinos, A.; Alcantara, C.; Rozes, N.; Voigt, B.; Zuniga, M. Characterization of the response to low pH of Lactobacillus casei Delta RR12, a mutant strain with low D-alanylation activity and sensitivity to low pH J. Appl. Microbiol. 2014, 116, 1250-1261 10.1111/jam.12442
41. Yebra, M. J.; Zuniga, M.; Beaufils, S.; Perez-Martinez, G.; Deutscher, J.; Monedero, V. Identification of a gene cluster enabling Lactobacillus casei BL23 to utilize myo-inositol Appl. Environ. Microbiol. 2007, 73, 3850-3858 10.1128/AEM.00243-07
42. Munoz-Provencio, D.; Llopis, M.; Antolin, M.; de Torres, I.; Guarner, F.; Perez-Martinez, G.; Monedero, V. Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix Arch. Microbiol. 2009, 191, 153-61 10.1007/s00203-008-0436-9
43. Munoz-Provencio, D.; Perez-Martinez, G.; Monedero, V. Characterization of a fibronectin-binding protein from Lactobacillus casei BL23 J. Appl. Microbiol. 2010, 108, 1050-1059 10.1111/j.1365-2672.2009.04508.x
44. Alcantara, C.; Zuniga, M. Proteomic and transcriptomic analysis of the response to bile stress of Lactobacillus casei BL23 Microbiology 2012, 158, 1206-1218 10.1099/mic.0.055657-0
45. Broadbent, J. R.; Larsen, R. L.; Deibel, V.; Steele, J. L. Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress J. Bacteriol. 2010, 192, 2445-2458 10.1128/JB.01618-09
46. Wang, J. C.; Zhang, W. Y.; Zhong, Z.; Wei, A. B.; Bao, Q. H.; Zhang, Y.; Sun, T. S.; Postnikoff, A.; Meng, H.; Zhang, H. P. Transcriptome analysis of probiotic Lactobacillus casei Zhang during fermentation in soymilk J. Ind. Microbiol. Biotechnol. 2012, 39, 191-206 10.1007/s10295-011-1015-7
47. Wu, R.; Zhang, W.; Sun, T.; Wu, J.; Yue, X.; Meng, H.; Zhang, H. Proteomic analysis of responses of a new probiotic bacterium Lactobacillus casei Zhang to low acid stress Int. J. Food Microbiol. 2011, 147, 181-7 10.1016/j.ijfoodmicro.2011.04.003
48. Sambrook, J.; Maniatis, T.; Fritsch, E. F. Molecular Cloning: A Laboratory Manual, 2 nd ed.; Cold Spring Harbor Laboratory: Cold Spring Harbor, NY, 1989.
49. Stephenson, D. P.; Moore, R. J.; Allison, G. E. Lactobacillus strain ecology and persistence within broiler chickens fed different diets: identification of persistent strains Appl. Environ. Microbiol. 2010, 76, 6494-6503 10.1128/AEM.01137-10
50. Tachon, S.; Lee, B.; Marco, M. L. Diet alters probiotic Lactobacillus persistence and function in the intestine Environ. Microbiol. 2014, 16, 2915-2926 10.1111/1462-2920.12297
51. Moyne, A. L.; Harris, L. J.; Marco, M. L. Assessments of total and viable Escherichia coli O157:H7 on field and laboratory grown lettuce PLoS One 2013, 8, e70643 10.1371/journal.pone.0070643
52. Derzelle, S.; Bolotin, A.; Mistou, M. Y.; Rul, F. Proteome analysis of Streptococcus thermophilus grown in milk reveals pyruvate formate-lyase as the major upregulated protein Appl. Environ. Microbiol. 2005, 71, 8597-8605 10.1128/AEM.71.12.8597-8605.2005
53. Luckhart, S.; Giulivi, C.; Drexler, A. L.; Antonova-Koch, Y.; Sakaguchi, D.; Napoli, E.; Wong, S.; Price, M. S.; Eigenheer, R.; Phinney, B. S.; Pakpour, N.; Pietri, J. E.; Cheung, K.; Georgis, M.; Riehle, M. Sustained activation of Akt elicits mitochondrial dysfunction to block Plasmodium falciparum infection in the mosquito host PLoS Pathog. 2013, 9, e1003180 10.1371/journal.ppat.1003180
54. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74, 5383-5392 10.1021/ac025747h
55. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75, 4646-58 10.1021/ac0341261
56. Kall, L.; Storey, J. D.; MacCoss, M. J.; Noble, W. S. Assigning significance to peptides identified by tandem mass spectrometry using decoy databases J. Proteome Res. 2008, 7, 29-34 10.1021/pr700600n
57. Takeda, K.; Okumura, K. Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the human NK-cell activity Biosci., Biotechnol., Biochem. 2007, 137, 791S-793S 10.1271/bbb.64.2706
58. Leloup, L.; Ehrlich, S. D.; Zagorec, M.; MorelDeville, F. Single-crossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsI and lacL genes Appl. Environ. Microbiol. 1997, 63, 2117-2123
59. Marco, M. L.; Bongers, R. S.; de Vos, W. M.; Kleerebezem, M. Spatial and temporal expression of Lactobacillus plantarum genes in the gastrointestinal tracts of mice Appl. Environ. Microbiol. 2007, 73, 124-132 10.1128/AEM.01475-06
60. Daniel, C.; Poiret, S.; Dennin, V.; Boutillier, D.; Pot, B. Bioluminescence imaging study of spatial and temporal persistence of Lactobacillus plantarum and Lactococcus lactis in living mice Appl. Environ. Microbiol. 2013, 79, 1086-1094 10.1128/AEM.03221-12
61. Barria, C.; Malecki, M.; Arraiano, C. M. Bacterial adaptation to cold Microbiology 2013, 159, 2437-2443 10.1099/mic.0.052209-0
62. Kiriukhin, M. Y.; Neuhaus, F. C. D-alanylation of lipoteichoic acid: Role of the D-alanyl carrier protein in acylation J. Bacteriol. 2001, 183, 2051-2058 10.1128/JB.183.6.2051-2058.2001
63. Chavarri, M.; Maranon, I.; Ares, R.; Ibanez, F. C.; Marzo, F.; Villaran Mdel, C. Microencapsulation of a probiotic and prebiotic in alginate-chitosan capsules improves survival in simulated gastro-intestinal conditions Int. J. Food Microbiol. 2010, 142, 185-189 10.1016/j.ijfoodmicro.2010.06.022
64. Saxelin, M.; Lassig, A.; Karjalainen, H.; Tynkkynen, S.; Surakka, A.; Vapaatalo, H.; Jarvenpaa, S.; Korpela, R.; Mutanen, M.; Hatakka, K. Persistence of probiotic strains in the gastrointestinal tract when administered as capsules, yoghurt, or cheese Int. J. Food Microbiol. 2010, 144, 293-300 10.1016/j.ijfoodmicro.2010.10.009
65. Chandan, R. C. Enhancing market value of milk by adding cultures J. Dairy Sci. 1999, 82, 2245-2256 10.3168/jds.S0022-0302(99)75472-X
66. Laakso, K.; Koskenniemi, K.; Koponen, J.; Kankainen, M.; Surakka, A.; Salusjarvi, T.; Auvinen, P.; Savijoki, K.; Nyman, T. A.; Kalkkinen, N.; Tynkkynen, S.; Varmanen, P. Growth phase-associated changes in the proteome and transcriptome of Lactobacillus rhamnosus GG in industrial-type whey medium Microb. Biotechnol. 2011, 4, 746-766 10.1111/j.1751-7915.2011.00275.x
67. Waldbauer, J. R.; Rodrigue, S.; Coleman, M. L.; Chisholm, S. W. Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle PLoS One 2012, 7, e43432 10.1371/journal.pone.0043432
68. Cohen, D. P. A.; Renes, J.; Bouwman, F. G.; Zoetendal, E. G.; Mariman, E.; de Vos, W. M.; Vaughan, E. E. Proteomic analysis of log to stationary growth phase Lactobacillus plantarum cells and a 2-DE database Proteomics 2006, 6, 6485-6493 10.1002/pmic.200600361
69. Al-Naseri, A.; Bowman, J. P.; Wilson, R.; Nilsson, R. E.; Britz, M. L. Impact of lactose starvation on the physiology of Lactobacillus casei GCRL163 in the presence or absence of tween 80 J. Proteome Res. 2013, 12, 5313-5322 10.1021/pr400661g
70. Hamon, E.; Horvatovich, P.; Bisch, M.; Bringel, F.; Marchioni, E.; Aoude-Werner, D.; Ennahar, S. Investigation of biomarkers of bile tolerance in Lactobacillus casei using comparative proteomics J. Proteome Res. 2012, 11, 109-118 10.1021/pr200828t
71. Rivas-Sendra, A.; Landete, J. M.; Alcantara, C.; Zuniga, M. Response of Lactobacillus casei BL23 to phenolic compounds J. Appl. Microbiol. 2011, 111, 1473-1481 10.1111/j.1365-2672.2011.05160.x
72. Wu, C.; He, G.; Zhang, J. Physiological and proteomic analysis of Lactobacillus casei in response to acid adaptation J. Ind. Microbiol. Biotechnol. 2014, 41, 1533-1540 10.1007/s10295-014-1487-3
73. Wu, C.; Zhang, J.; Chen, W.; Wang, M.; Du, G.; Chen, J. A combined physiological and proteomic approach to reveal lactic-acid-induced alterations in Lactobacillus casei Zhang and its mutant with enhanced lactic acid tolerance Appl. Microbiol. Biotechnol. 2012, 93, 707-722 10.1007/s00253-011-3757-6
74. Wu, R.; Wang, W.; Yu, D.; Zhang, W.; Li, Y.; Sun, Z.; Wu, J.; Meng, H.; Zhang, H. Proteomics analysis of Lactobacillus casei Zhang, a new probiotic bacterium isolated from traditional home-made koumiss in Inner Mongolia of China Mol. Cell. Proteomics 2009, 8, 2321-2338 10.1074/mcp.M800483-MCP200
75. Wu, R.; Sun, Z.; Wu, J.; Meng, H.; Zhang, H. Effect of bile salts stress on protein synthesis of Lactobacillus casei Zhang revealed by 2-dimensional gel electrophoresis J. Dairy Sci. 2010, 93, 3858-3868 10.3168/jds.2009-2967
76. Hussain, M. A.; Knight, M. I.; Britz, M. L. Proteomic analysis of lactose-starved Lactobacillus casei during stationary growth phase J. Appl. Microbiol. 2009, 106, 764-773 10.1111/j.1365-2672.2008.03961.x
77. Abdallah, C.; Dumas-Gaudot, E.; Renaut, J.; Sergeant, K. Gel-based and gel-free quantitative proteomics approaches at a glance Int. J. Plant Genomics 2012, 2012, 1-17 10.1155/2012/494572
78. He, J. T.; Liu, Y. S.; He, S. Z.; Wang, Q. S.; Pu, H.; Tong, Y. P.; Ji, J. G. Comparison of two-dimensional gel electrophoresis based and shotgun strategies in the study of plasma membrane proteome Proteomics: Clin. Appl. 2007, 1, 231-241 10.1002/prca.200600004
79. Link, A. J.; Eng, J.; Schieltz, D. M.; Carmack, E.; Mize, G. J.; Morris, D. R.; Garvik, B. M.; Yates, J. R. Direct analysis of protein complexes using mass spectrometry Nat. Biotechnol. 1999, 17, 676-682 10.1038/10890
80. Wolff, S.; Otto, A.; Albrecht, D.; Zeng, J. S.; Buttner, K.; Gluckmann, M.; Hecker, M.; Becher, D. Gel-free and gel-based proteomics in Bacillus subtilis: a comparative study Mol. Cell. Proteomics 2006, 5, 1183-1192 10.1074/mcp.M600069-MCP200
81. Duwat, P.; Ehrlich, S. D.; Gruss, A. The recA gene of Lactococcus lactis: characterization and involvement in oxidative and thermal stress Mol. Microbiol. 1995, 17, 1121-1131 10.1111/j.1365-2958.1995.mmi-17061121.x
82. Budde, I.; Steil, L.; Scharf, C.; Volker, U.; Bremer, E. Adaptation of Bacillus subtilis to growth at low temperature: a combined transcriptomic and proteomic appraisal Microbiology 2006, 152, 831-853 10.1099/mic.0.28530-0
83. Borezee, E.; Pellegrini, E.; Berche, P. OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survival Infect. Immun. 2000, 68, 7069-7077 10.1128/IAI.68.12.7069-7077.2000
84. Gitton, C.; Meyrand, M.; Wang, J. H.; Caron, C.; Trubuil, A.; Guillot, A.; Mistou, M. Y. Proteomic signature of Lactococcus lactis NCDO763 cultivated in milk Appl. Environ. Microbiol. 2005, 71, 7152-7163 10.1128/AEM.71.11.7152-7163.2005
85. Herve-Jimenez, L.; Guillouard, I.; Guedon, E.; Gautier, C.; Boudebbouze, S.; Hols, P.; Monnet, V.; Rul, F.; Maguin, E. Physiology of Streptococcus thermophilus during the late stage of milk fermentation with special regard to sulfur amino-acid metabolism Proteomics 2008, 8, 4273-4286 10.1002/pmic.200700489
86. Smeianov, V. V.; Wechter, P.; Broadbent, J. R.; Hughes, J. E.; Rodriguez, B. T.; Christensen, T. K.; Ardo, Y.; Steele, J. L. Comparative high-density microarray analysis of gene expression during growth of Lactobacillus helveticus in milk versus rich culture medium Appl. Environ. Microbiol. 2007, 73, 2661-2672 10.1128/AEM.00005-07
87. Mansilla, M. C.; Cybulski, L. E.; Albanesi, D.; de Mendoza, D. Control of membrane lipid fluidity by molecular thermosensors J. Bacteriol. 2004, 186, 6681-6688 10.1128/JB.186.20.6681-6688.2004
88. Tsuzuki, M.; Moskvin, O. V.; Kuribayashi, M.; Sato, K.; Retamal, S.; Abo, M.; Zeilstra-Ryalls, J.; Gomelsky, M. Salt stress-induced changes in the transcriptome, compatible solutes, and membrane lipids in the facultatively phototrophic bacterium Rhodobacter sphaeroides Appl. Environ. Microbiol. 2011, 77, 7551-7559 10.1128/AEM.05463-11
89. Lai, C. Y.; Cronan, J. E. beta-ketoacyl-acyl carrier protein synthase III (FabH) is essential for bacterial fatty acid synthesis J. Biol. Chem. 2003, 278, 51494-51503 10.1074/jbc.M308638200
90. Choi, K. H.; Heath, R. J.; Rock, C. O. beta-ketoacyl-acyl carrier protein synthase III (FabH) is a determining factor in branched-chain fatty acid biosynthesis J. Bacteriol. 2000, 182, 365-370 10.1128/JB.182.2.365-370.2000
91. Call, E. K.; Klaenhammer, T. R. Relevance and application of sortase and sortase-dependent proteins in lactic acid bacteria Front. Microbiol. 2013, 4, 73 10.3389/fmicb.2013.00073
92. Wall, T.; Bath, M.; Britton, R. A.; Jonsson, H.; Versalovic, J.; Roos, S. The early response to acid shock in Lactobacillus reuteri involves the ClpL chaperone and a putative cell wall-altering esterase Appl. Environ. Microbiol. 2007, 73, 3924-3935 10.1128/AEM.01502-06
93. Palumbo, E.; Deghorain, M.; Cocconcelli, P. S.; Kleerebezem, M.; Geyer, A.; Hartung, T.; Morath, S.; Hols, P. D-Alanyl ester depletion of teichoic acids in Lactobacillus plantarum results in a major modification of lipoteichoic acid composition and cell wall perforations at the septum mediated by the Acm2 autolysin J. Bacteriol. 2006, 188, 3709-3715 10.1128/JB.188.10.3709-3715.2006
94. Velez, M. P.; Verhoeven, T. L. A.; Draing, C.; Von Aulock, S.; Pfitzenmaier, M.; Geyer, A.; Lambrichts, I.; Grangette, C.; Pot, B.; Vanderleyden, J.; De Keersmaecker, S. C. J. Functional analysis of D-alanylation of lipoteichoic acid in the probiotic strain Lactobacillus rhamnosus GG Appl. Environ. Microbiol. 2007, 73, 3595-3604 10.1128/AEM.02083-06
95. Saar-Dover, R.; Bitler, A.; Nezer, R.; Shmuel-Galia, L.; Firon, A.; Shimoni, E.; Trieu-Cuot, P.; Shai, Y. D-alanylation of lipoteichoic acids confers resistance to cationic peptides in group B Streptococcus by increasing the cell wall density PLoS Pathog. 2012, 8, e1002891 10.1371/journal.ppat.1002891
96. Walter, J.; Loach, D. M.; Alqumber, M.; Rockel, C.; Hermann, C.; Pfitzenmaier, M.; Tannock, G. W. D-alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract Environ. Microbiol. 2007, 9, 1750-1760 10.1111/j.1462-2920.2007.01292.x
97. Palomino, M. M.; Allievi, M. C.; Grundling, A.; Sanchez-Rivas, C.; Ruzal, S. M. Osmotic stress adaptation in Lactobacillus casei BL23 leads to structural changes in the cell wall polymer lipoteichoic acid Microbiology 2013, 159, 2416-2426 10.1099/mic.0.070607-0
98. de Jong, A.; Hansen, M. E.; Kuipers, O. P.; 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
99. Mccord, J. M.; Fridovic, I. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein) Science 1969, 244, 6049-6055 10.1126/science.1586-a
100. Nakano, M. M.; Hajarizadeh, F.; Zhu, Y.; Zuber, P. Loss-of-function mutations in yjbD result in ClpX- and ClpP-independent competence development of Bacillus subtilis Mol. Microbiol. 2001, 42, 383-394 10.1046/j.1365-2958.2001.02639.x
101. Nakano, S.; Kuster-Schock, E.; Grossman, A. D.; 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
102. Tachon, S.; Brandsma, J. B.; 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
103. Jayamanne, V. S.; Adams, M. R. Modelling the effects of pH, storage temperature and redox potential (E-h) on the survival of bifidobacteria in fermented milk Int. J. Food Sci. Technol. 2009, 44, 1131-1138 10.1111/j.1365-2621.2009.01931.x
104. Bolduc, M. P.; Raymond, Y.; Fustier, P.; Champagne, C. P.; Vuillemard, J. C. Sensitivity of bifidobacteria to oxygen and redox potential in non-fermented pasteurized milk Int. Dairy J. 2006, 16, 1038-1048 10.1016/j.idairyj.2005.10.030
105. Mohammadi, R.; Mortazavian, A. M. Review Article: Technological aspects of prebiotics in probiotic fermented milks Food Rev. Int. 2011, 27, 192-212 10.1080/87559129.2010.535235
106. Bruno-Barcena, J. M.; Andrus, J. M.; Libby, S. L.; Klaenhammer, T. R.; Hassan, H. M. Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity Appl. Environ. Microbiol. 2004, 70, 4702-4710 10.1128/AEM.70.8.4702-4710.2004
107. LeBlanc, J. G.; del Carmen, S.; Miyoshi, A.; Azevedo, V.; Sesma, F.; Langella, P.; Bermudez-Humaran, L. G.; Watterlot, L.; Perdigon, G.; de Moreno de LeBlanc, A. Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohns disease in mice J. Biotechnol. 2011, 151, 287-293 10.1016/j.jbiotec.2010.11.008
108. Isolauri, E.; Juntunen, M.; Rautanen, T.; Sillanaukee, P.; Koivula, T. A Human Lactobacillus strain (Lactobacillus-casei sp Strain GG) promotes recovery from acute diarrhea in children Pediatrics 1991, 88, 90-97
109. Sanders, M. E.; Klaenhammer, T. R.; Ouwehand, A. C.; Pot, B.; Johansen, E.; Heimbach, J. T.; Marco, M. L.; Tennila, J.; Ross, R. P.; Franz, C.; Page, N.; Pridmore, R. D.; Leyer, G.; Salminen, S.; Charbonneau, D.; Call, E.; Lenoir-Wijnkoop, I. Effects of genetic, processing, or product formulation changes on efficacy and safety of probiotics Ann. N. Y. Acad. Sci. 2014, 1309, 1-18 10.1111/nyas.12363