Emmental cheese environment enhances Propionibacterium freudenreichii stress tolerance

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Gagnaire, Valérie ^a   Jardin, Julien ^a   Rabah, Houem ^a   Briard Bion, Valérie ^a   Jan, Gwénaël ^a  

^a UMR1253   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARAGINE; ASPARTIC ACID; BACTERIAL PROTEIN; CYPB PROTEIN; CYSTEINE; CYTOCHROME P450; DNAK1 PROTEIN; GLUTAMINE; GLYCINE; GROES1 PROTEIN; ISOLEUCINE; LACTIC ACID; LEUCINE; OXIDOREDUCTASE; PROPIONIC ACID; PYRUVIC ACID; SERINE; THIOREDOXIN; UNCLASSIFIED DRUG; VALINE; PROBIOTIC AGENT;

ADAPTATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CATABOLISM; CHEESE; CITRIC ACID CYCLE; GROWTH RATE; NONHUMAN; OSMOADAPTATION; OSMOLARITY; OXIDATION REDUCTION REACTION; PROPIONIBACTERIUM FREUDENREICHII; PROPIONIBACTERIUM FREUDENREICHII SHERMANII; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; STRESS; FOOD CONTROL; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROPIONIBACTERIUM;

CHEESE; FOOD MICROBIOLOGY; PROBIOTICS; PROPIONIBACTERIUM; STRESS, PHYSIOLOGICAL;

EID: 84943196032     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135780     Document Type: Article

References (48)

1. Jan G, Lan A, Leverrier P Dairy propionibacteria as probiotics. In: Saarela M, editors. Functional dairy products. Cambridge CB21 6AH: Woodhead Publishing Limited, Abington Hall, Abington; 2007. pp. 165-194.
2. Thierry A, Falentin H, Deutsch SM, Jan G Propionibacterium spp. In: Fuquay JW, Fox PF, McSweeney PLH, editors. Encyclopedia of dairy sciences, Vol 1. San Diego, USA: Elsevier Academic Press, London, UK; 2011. pp. 403-411.
3. Leverrier P, Dimova D, Pichereau V, Auffray Y, Boyaval P, Jan G. Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: Physiological and proteomic analysis. Appl. Environ. Microbiol. 2003;69:3809-3818. PMID: 12839748
4. Gagnaire V, Lortal S, Léonil J. Free active peptidases are detected in Emmental juice extracted before ripening in the warm room. J. Dairy Res. 1998;65:119-128.
5. Cousin FJ, Mater D, Foligné B, Jan G. Dairy propionibacteria as human probiotics: A review of recent evidence. Dairy Sci. Technol. 2011;91:1-26.
6. Bouglé D, Roland N, Lebeurrier F, Arhan P. Effect of propionibacteria supplementation on fecal bifidobacteria and segmental colonic transit time in healthy human subjects. Scand. J. Gastroenterol. 1999;34:144-148. PMID: 10192191
7. Foligné B, Deutsch SM, Breton J, Cousin FJ, Dewulf J, Samson M et al. Promising immunomodulatory effects of selected strains of dairy propionibacteria as evidenced in vitro and in vivo. Appl. Environ. Microbiol. 2010;76:8259-8264. doi: 10.1128/AEM.01976-10 PMID: 20971874
8. Foligné B, Breton J, Mater D, Jan G. Tracking the microbiome functionality: Focus on Propionibacterium species. Gut 2013;62:1227-1228. doi: 10.1136/gutjnl-2012-304393 PMID: 23389969
9. Lan A, Bruneau A, Bensaada M, Philippe C, Bellaud P, Rabot S et al. Increased induction of apoptosis by Propionibacterium freudenreichii TL133 in colonic mucosal crypts of human microbiota-associated rats treated with 1, 2-dimethylhydrazine. Br. J. Nutr. 2008;100:1251-1259. doi: 10.1017/S0007114508978284 PMID: 18466653
10. Hugenholtz J, Hunik J, Santos H, Smid E. Nutraceutical production by propionibacteria. Lait 2002;82:103-112.
11. Havenaar R. Intestinal health functions of colonic microbial metabolites: A review. Benef. Microbes. 2011;2:103-114. doi: 10.3920/BM2011.0003 PMID: 21840809
12. Jan G, Belzacq AS, Haouzi D, Rouault A, Metivier D, Kroemer G et al. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ. 2002;9:179-188. PMID: 11840168
13. Lan A, Lagadic-Gossmann D, Lemaire C, Brenner C, Jan G. Acidic extracellular pH shifts colorectal cancer cell death from apoptosis to necrosis upon exposure to propionate and acetate, major end-products of the human probiotic propionibacteria. Apoptosis. 2007;12:573-591. PMID: 17195096
14. Isawa K, Hojo K, Yoda N, Kamiyama T, Makino S, Saito M et al. Isolation and identification of a new bifidogenic growth stimulator produced by Propionibacterium freudenreichii ET-3. Bioscience Biotechnology and Biochemistry 2002;66:679-681.
15. Okada Y, Tsuzuki Y, Miyazaki J, Matsuzaki K, Hokari R, Komoto S et al. Propionibacterium freudenreichii component 1.4-dihydroxy-2-naphthoic acid (DHNA) attenuates dextran sodium sulphate induced colitis by modulation of bacterial flora and lymphocyte homing. Gut 2006;55:681-688. PMID: 16299037
16. Okada Y, Hokari R, Kato S, Mataki N, Okudaira K, Takebayashi K et al. 1.4-dihydroxy-2-naphthoic acid (DHNA) shows anti-inflammatory effect on NSAID-induced colitis in IL-10-knockout mice through suppression of inflammatory cell infiltration and increased number of genus Bifidobacterium. Gastroenterology 2006;130:A313.
17. Le Marechal C, Peton V, Ple C, Vroland C, Jardin J, Briard-Bion V et al. Surface proteins of Propionibacterium freudenreichii are involved in its anti-inflammatory properties. J. Proteomics 2015;113:447-461. doi: 10.1016/j.jprot.2014.07.018 PMID: 25150945
18. Leverrier P, Fremont Y, Rouault A, Boyaval P, Jan G. In vitro tolerance to digestive stresses of propionibacteria: Influence of food matrices. Food Microbiol. 2005;22:11-18.
19. Hervé C, Fondrevez M, Cheron A, Barloy-Hubler F, Jan G. Transcarboxylase mRNA: A marker which evidences P.freudenreichii survival and metabolic activity during its transit in the human gut. Int. J. Food Microbiol. 2007;113:303-314. PMID: 17156879
20. Jan G, Leverrier P, Roland N. Survival and beneficial effects of propionibacteria in the human gut: In vivo and in vitro investigations. Lait 2002;82:131-144.
21. Jan G, Rouault A, Maubois JL. Acid stress susceptibility and acid adaptation of Propionibacterium freudenreichii subsp. shermanii. Lait 2000;80:325-336.
22. Jan G, Leverrier P, Pichereau V, Boyaval P. Changes in protein synthesis and morphology during acid adaptation of Propionibacterium freudenreichii. Appl. Environ. Microbiol. 2001;67:2029-2036. PMID: 11319077
23. Salvat-Brunaud D, Maubois JL, Maillard MB, Corre C, Thierry A. Extraction et analyse de la phase aqueuse de l'emmental à 4 stades d'affinage. Lait 1995;75:239-249.
24. Gagnaire V, Thierry A, Léonil J. Propionibacteria and facultatively heterofermentative lactobacilli weakly contribute to secondary proteolysis of Emmental cheese. Lait 2001;81:339-353.
25. T, a hardy actinobacterium with food and probiotic applications. Plos One 2010;5.
26. Cousin FJ, Louesdon S, Maillard MB, Parayre S, Falentin H, Deutsch SM et al. The first dairy product exclusively fermented by Propionibacterium freudenreichii: A new vector to study probiotic potentialities in vivo. Food Microbiol. 2012;32:135-146. doi: 10.1016/j.fm.2012.05.003 PMID: 22850385
27. Spackman DH, Stein WH, Moore S. Automatic recording apparatus for use in the chromatography of amino-acids. Anal. Chem. 1958;30:1190-1206.
28. R Core Team. A language and environment for statistical computing. R Foundation for Statistical Computing 2014; http://www.R-project.org: Vienna, Austria.
29. Leverrier P, Vissers JP, Rouault A, Boyaval P, Jan G. Mass spectrometry proteomic analysis of stress adaptation reveals both common and distinct response pathways in Propionibacterium freudenreichii. Arch. Microbiol. 2004;181:215-230. PMID: 14730419
30. Morris JS, Clark BN, Wei W, Gutstein HB. Evaluating the performance of new approaches to spot quantification and differential expression in 2-dimensional gel electrophoresis studies. Proteome Res. 2010;9:595-604.
31. Anastasiou R, Leverrier P, Krestas I, Rouault A, Kalantzopoulos G, Boyaval P et al. Changes in protein synthesis during thermal adaptation of Propionibacterium freudenreichii subsp. shermanii. Int. J. Food Microbiol. 2006;108:301-314. PMID: 16473425
32. Salvat-Brunaud D, Thierry A, Maubois JL. Development of a medium simulating Emmental juice for propionibacteria growth. J. Dairy Res. 1997;64:573-580.
33. Fitz A. Über Spaltpilzgährungen. Berichte der deutschen chemischen Gesellschaft 1878;11:1890-1899.
34. Crow VL. Metabolism of aspartate by Propionibacterium freudenreichii subsp. shermanii: Effect on lactate fermentation. Appl. Environ. Microbiol. 1986;52:359-365. PMID: 16347135
35. T adaptation strategies in conditions mimicking cheese ripening in the cold. Plos One 2012;7:e29083. doi: 10.1371/journal.pone.0029083 PMID: 22253706
36. Thierry A, Maillard MB. Production of cheese flavour compounds derived from amino acid catabolism by Propionibacterium freudenreichii. Lait 2002;82:17-32.
37. Rallu F, Gruss A, Maguin E. Lactococcus lactis and stress. Anton. Leeuw. Int. J. G. 1996;70:243-251.
38. Flahaut S, Hartke A, Giard JC, Benachour A, Boutibonnes P, Auffray Y. Relationship between stress response towards bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol. Lett. 1996;138:49-54. PMID: 8674969
39. Wu R, Zhang W, Sun T, Wu J, Yue X, Meng H et al. Proteomic analysis of responses of a new probiotic bacterium Lactobacillus casei Zhang to low acid stress. Int. J. Food Microbiol. 2011;147:181-187. doi: 10.1016/j.ijfoodmicro.2011.04.003 PMID: 21561676
40. Begley M, Gahan CGM, Hill C. Bile stress response in Listeria monocytogenes LO28: Adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl. Environ. Microbiol. 2002;68:6005-6012. PMID: 12450822
41. Fröhlich-Wyder MT, Bachmann HP Cheeses with propionic acid fermentation. Cheese. Chemistry, Physics and Microbiology: major cheese groups. London: Elsevier; 2004. pp. 141-156.
42. Le Boucher C, Courant F, Jeanson S, Chereau S, Maillard MB, Royer AL et al. First mass spectrometry metabolic fingerprinting of bacterial metabolism in a model cheese. Food Chem. 2013;141:1032-1040. doi: 10.1016/j.foodchem.2013.03.094 PMID: 23790883
43. Boyaval P, Deborde C, Corre C, Blanco C, Begue E. Stress and osmoprotection in propionibacteria. Lait 1999;79:59-69.
44. Wood JM. Bacterial osmoregulation: A paradigm for the study of cellular homeostasis. Annu. Rev. Microbiol. 2011;65:215-238. doi: 10.1146/annurev-micro-090110-102815 PMID: 21663439
45. Lee S, Ahn S, Lee H, Kim WI, Kim HY, Ryu JG et al. Gene-related strain variation of Staphylococcus aureus for homologous resistance response to acid stress. J. Food Prot. 2014;77:1794-1798. doi: 10. 4315/0362-028X. JFP-14-070 PMID: 25285500
46. Hu Y, Lu P, Zhang Y, Li L, Chen S. Characterization of an aspartate-dependent acid survival system in Yersinia pseudotuberculosis. FEBS Lett. 2010;584:2311-2314. doi: 10.1016/j.febslet.2010.03.045 PMID: 20371246
47. Thierry A, Deutsch SM, Falentin H, Dalmasso M, Cousin FJ, Jan G. New insights into physiology and metabolism of Propionibacterium freudenreichii. Int. J. Food Microbiol. 2011;149:19-27. doi: 10. 1016/j.ijfoodmicro.2011.04.026 PMID: 21620505
48. Castro JM, Tornadijo ME, Fresno JM, Sandoval H. Biocheese: A food probiotic carrier. Biomed. Res. Int. 2015;2015:723056. Epub; 2015 Feb. 23:723056. doi: 10.1155/2015/723056 PMID: 25802862