The complete genome of propionibacterium freudenreichii CIRM-BIA1T, a hardy actinobacterium with food and probiotic applications

PLoS ONE

Volumn 5, Issue 7, 2010, Pages 1-12

  Falentin, Hélène ^a   Deutsch, Stéphanie Marie ^a   Jan, Gwenaël ^a   Loux, Valentin ^b   Thierry, Anne ^a   Parayre, Sandrine ^a   Maillard, Marie Bernadette ^a   Dherbécourt, Julien ^a   Cousin, Fabien J ^a   Jardin, Julien ^a   Siguier, Patricia ^c   Couloux, Arnaud ^d   Barbe, Valérie ^d   Vacherie, Benoit ^d   Wincker, Patrick ^d   Gibrat, Jean François ^b   Gaillardin, Claude ^e   Lortal, Sylvie ^a  

^a UMR1253   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

^c UMR   (France)

^d UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^e AGROPARISTECH   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ESTER; FATTY ACID; PROBIOTIC AGENT; PROPIONIC ACID; VITAMIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOSYNTHESIS; CHEESEMAKING; CHROMOSOME STRUCTURE; DNA BASE COMPOSITION; GENE FUNCTION; GENE INSERTION SEQUENCE; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROPIONIBACTERIUM FREUDENREICHII; PROTEIN ANALYSIS; PROTEIN FUNCTION; ACTINOBACTERIA; FOOD CONTROL; GENETICS; PROPIONIBACTERIUM;

ACTINOBACTERIA; FOOD MICROBIOLOGY; GENOME, BACTERIAL; PROBIOTICS; PROPIONIBACTERIUM;

EID: 77955388627     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011748     Document Type: Article

References (92)

1. Cousin FJ, Mater DD, Foligné B, Jan G (2010) Dairy propionibacteria as human probiotics: A review of recent evidence (in press). Dairy Sci Technol doi: 10.1051/dst/2010032.
2. von Freudenreich E, Orla-Jensen O (1906) Uber die in Emmentalerkäse stattfindene Propionsäure-gärung. Zentralbl Bakteriol 17: 529-546.
3. Cummins CS, Johnson JL (1992) The genus Propionibacterium. In: Balows E, Truper HG, Dworkin M, Harder W, Schleifer KH, eds. The prokaryotes Springer Verlag.
4. Thierry A, Maillard MB (2002) Production of cheese flavour compounds derived from amino acid catabolism by Propionibacterium freudenreichii. Lait 82: 17-32.
5. Thierry A, Maillard MB, Richoux R, Kerjean JR, Lortal S (2005) Propionibacterium freudenreichii strains quantitatively affect production of volatile compounds in Swiss cheese. Lait 85: 57-74.
6. Thierry A, Maillard MB, Bonnarme P, Roussel E (2005) The addition of Propionibacterium freudenreichii to Raclette cheese induces biochemical changes and enhances flavour development. J Agric Food Chem 53: 4157-4165.
7. Kiatpapan P, Kanamnuay N, Jongserijit B, Piao YZ, Yamashita M, et al. (2003) Production of 5-aminolevulinic acid and vitamin B-12 using metabolic engineering of Propionibacterium freudenreichii. Fermentation Biotech 862: 221-232.
8. Piao Y, Yamashita M, Kawaraichi N, Asegawa R, Ono H, et al. (2004) Production of vitamin B-12 in genetically engineered Propionibacterium freudenrei-chii. J Biosci Bioeng 98: 167-173.
9. Murooka Y, Piao Y, Kiatpapan P, Yamashita M (2005) Production of tetrapyrrole compounds and vitamin B-12 using genetically engineering of Propionibacterium freudenreichii. An overview. Lait 85: 9-22.
10. Roessner CA, Huang K-X, Warren MJ, Raux E, Scott AI (2002) Isolation and characterization of 14 additional genes specifying the anaerobic biosynthesis of cobalamin (vitamin B12) in Propionibacterium freudenreichii (P. shermanii). Microbiol 148: 1845-1853.
11. Isawa K, Hojo K, Yoda N, Kamiyama T, Makino S, et al. (2002) Isolation and identification of a new bifidogenic growth stimulator produced by Propionibac-terium freudenreichii ET-3. Biosci Biotech Biochem 66: 679-681.
12. Kaneko T, Mori H, Iwata M, Meguro S (1994) Growth stimulator for bifidobacteria produced by Propionibacterium freudenreichii and several intestinal bacteria. J Dairy Sci 77: 393-404.
13. Bouglé D, Roland N, Lebeurrier F, Arhan P (1999) Effect of propionibacteria supplementation on fecal bifidobacteria and segmental colonic transit time in healthy human subjects. Scand J Gastroenterol 34: 144-148.
14. Hojo K, Yoda N, Tsuchita H, Ohtsu T, Seki K, et al. (2002) Effect of ingested culture of Propionibacterium freudenreichii ET-3 on fecal microflora and stool frequency in healthy females. Biosci Microfl 21: 115-120.
15. Jan G, Leverrier P, Pichereau V, Boyaval P (2001) Changes in protein synthesis and morphology during acid adaptation of Propionibacterium freudenreichii. Appl Environ Microbiol 67: 2029-2036.
16. Leverrier P, Dimova D, Pichereau V, Auffray Y, Boyaval P, et al. (2003) Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: physiological and proteomic analysis. Appl Environ Microbiol 69: 3809-3818.
17. Hervé C, Fondrevez M, Chéron A, Barloy-Hubler F, Jan G (2007) Transcarboxylase mRNA: a marker which evidences P. freudenreichii survival and metabolic activity during its transit in the human gut. Int J Food Microbiol 113: 303-314.
18. Jan G, Leverrier P, Proudy I, Roland N (2002) Survival and beneficial effects of propionibacteria in the human gut: in vivo and in vitro investigations. Lait 82: 131-144.
19. Lan A, Bruneau A, Philippe C, Rochet V, Rouault A, et al. (2007) Survival and metabolic activity of selected strains of Propionibacterium freudenreichii in the gastrointestinal tract of human microbioti-associated rats. Br J Nutr 97: 714-724.
20. Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, et al. (2008) Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 14: 2029-2036.
21. Bruggemann H, Henne A, Hoster F, Liesegang H, Wiezer A, et al. (2004) The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305: 671-673.
22. Lee ZMP, Bussema C, Schmidt TM (2009) RrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucleic Acids Res 37: D489-D493.
23. Van Luijk N, Stierli MP, Miescher SS, Hervé C, Dasen G, et al. (2002) Genetics and molecular biology of propionibacteria. Lait 82: 45-57.
24. Arber W (2000) Genetic variation: molecular mechanisms and impact on microbial evolution. FEMS Microbiol Rev 24: 1-7.
25. Kichenaradja P, Siguier P, Perochon J, Chandler M (2010) ISbrowser: an extension of ISfinder for visualizing insertion sequences in prokaryotic genomes. Nucleic Acids Res 38: D62-D68.
26. Deutsch S-M, Falentin H, Dols-Lafargue M, LaPointe G, Roy D (2008) Capsular exopolysaccharide biosynthesis gene of Propionibacterium freudenreichii subsp. shermanii. Int J Food Microbiol 125: 252-258.
27. Deutsch S-M, Le Bivic P, Hervé C, Madec M-N, LaPointe G, et al. (2010) Capsular phenotype in Propionibacterium freudenreichii correlates with the expression level of gtf, a unique polysaccharide synthase encoding gene. Appl Environ Microbiol 76: 2740-2746.
28. Lee MH, Pascopella L, Jacobs WR, Hatfull GF (1991) Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guerin. P Acad Nat Sci USA 88: 3111-3115.
29. Haeseleer F, Pollet JF, Bollen A, Jacobs P (1992) Molecular cloning and sequencing of the attachment site and integrase gene of the temperate mycobacteriophage Frat1. Nucleic Acids Res 20: 1420.
30. Hervé C, Coste A, Rouault A, Fraslin JM, Gautier M (2001) First evidence of lysogeny in Propionibacterium freudenreichii subsp. shermanii. Appl Environ Microbiol 67: 231-238.
31. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712.
32. Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35: W52-W57.
33. Chopin MC, Rouault A, Ehrlich SD, Gautier M (2002) Filamentous phage active on the gram-positive bacterium Propionibacterium freudenreichii. J Bacteriol 184: 2030-2033.
34. Miskin JE, Farrell AM, Cunliffe WJ, Holland KT (1997) Propionibacterium acnes, a resident of lipid-rich human skin, produces a 33 kDa extracellular lipase encoded by gehA. Microbiol -UK 143: 1745-1755.
35. Dherbécourt J, Falentin H, Jardin J, Maillard MB, Baglinière F, et al. (2010) Identification of a secreted lipolytic esterase in Propionibacterium freudenreichii, a ripening process bacterium involved in Emmental cheese lipolysis. Appl Environ Microbiol 76: 1181-1188.
36. Dherbécourt J, Falentin H, Canaan S, Thierry A (2008) A genomic search approach to identify esterases in Propionibacterium freudenreichii involved in the formation of flavour in Emmental cheese. Microb Cell Fact 7.
37. Cummins CS, Johnson JL (1986) Genus I. Propionibacterium Orla-Jensen 1909. In: Sneath PHA, Mair NS, Sharpe ME, Holt JG, eds. Bergey's Manual of Systematic Bacteriology. Baltimore: Williams & Wilkins. pp 1346-1353.
38. Toraya T, Kuno S, Fukui S (1980) Distribution of Coenzyme B12-Dependent Diol Dehydratase and Glycerol Dehydratase in Selected Genera of Enterobac-teriaceae and Propionibacteriaceae. J Bacteriol 141: 1439-1442.
39. Bobik TA, Havemann GD, Busch RJ, Williams DS, Aldrich HC (1999) The propanediol utilization (pdu) operon of Salmonella enterica serovar Typhimurium LT2 includes genes necessary for formation of polyhedral organelles involved in coenzyme B(12)-dependent 1, 2-propanediol degradation. J Bacteriol 181: 5967-5975.
40. Sampson EM, Bobik TA (2008) Microcompartments for B12-dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. J Bacteriol 190: 2966-2971.
41. Schink B, Kremer DR, Hansen TA (1987) Pathway of propionate formation from ethanol in Pelobacter Propionicus. Arch Microbiol 147: 321-327.
42. Macy JM, Ljungdahl LG, Gottschalk G (1978) Pathway of succinate and propionate formation in Bacteroides fragilis. J Bacteriol 134: 84-91.
43. Ng SKC, Hamilton IR (1973) Carbon dioxide fixation by Veillonella parvula M4 and its relation to propionic acid formation. Can J Microbiol 19: 715-723.
44. Johns AT (1951) The mechanism of propionic acid formation by Veillonella gazogenes. J Gen Microbiol 5: 326-336.
45. Johns AT (1952) The mechanism of propionic acid formation by Clostridium-Propionicum. J Gen Microbiol 6: 123-127.
46. Wood HG (1981) Metabolic cycles in the fermentation by propionic acid bacteria. In: Estabrook RW, Srera P, eds. Current topics in cellular regulation-1981. New York: Academic Press. pp 255-287.
47. Beck S, Schink B (1995) Acetate oxidation through a modified citric acid cycle in Propionibacterium freudenreichii. Arch Microbiol 163: 182-187.
48. Deborde C (1998) Etude du métabolisme carboné primaire de bactéries propioniques laitières par Résonance Magnétique Nucléaire in vivo du 13C: des voies métaboliques aux tests de performance des souches industrielles [dissertation]. ENSAR/Agrocampus Ouest, Rennes.
49. Hall PR, Zheng R, Antony L, Pusztai-Carey M, Carey PR, et al. (2004) Transcarboxylase 5S structures: assembly and catalytic mechanism of a multienzyme complex subunit. EMBO J 23: 3621-3631.
50. Crow VL (1986) Metabolism of aspartate by Propionibacterium freudenreichii subsp. shermanii: effect on lactate fermentation. Appl Environ Microbiol 52: 359-365.
51. Fröhlich-Wyder MT, Bachmann HP (2004) Cheeses with propionic acid fermentation. In: Fox PF, McSweeney PLH, Cogan TM, Guinee TP, eds. Cheese. Chemistry, Physics and Microbiology. London: Elsevier. pp 141-156.
52. Benz M, Schink B, Brune A (1998) Humic acid reduction by Propionibacterium freudenreichii and other fermenting bacteria. Appl Environ Microbiol 64: 4507-4512.
53. Seufferheld MJ, Alvarez HM, Farias ME (2008) Role of polyphosphates in microbial adaptation to extreme environments. Appl Environ Microbiol 74: 5867-5874.
54. Clark JE, Beegen H, Wood HG (1987) Isolation of intact chains of polypho-sphate from Propionibacterium shermanii grown on glucose or lactate. J Bacteriol 168: 1212-1219.
55. Clark JE, Beegen H, Wood HG (1987) Isolation of intact chains of polypho-sphate from Propionibacterium shermanii grown on glucose or lactate. J Bacteriol 168: 1212-1219.
56. McLennan AG (2006) The Nudix hydrolase superfamily. Cell Mol Life Sci 63: 123-143.
57. Meurice G, Deborde C, Jacob D, Falentin H, Boyaval P, et al. (2004) In silico exploration of the fructose-6-phosphate phosphorylation step in glycolysis: genomic evidence of the coexistence of an atypical ATP-dependent along with a PPi-dependent phosphofructokinase in Propionibacterium freudenreichii subsp. shermanii. In Silico Biol 4: 0043.
58. Meurice G (2004) Reconstruction in silico de voies métaboliques: application aux voies glycolytiques de Propionibacterium freudenreichi subsp. shermanii [dissertation]. Rennes, France: Ecole Nationale Supérieure Agronomique de Rennes.
59. Deborde C, Corre C, Rolin DB, Nadal L, De Certaines JD, et al. (1996) Trehalose biosynthesis in dairy Propionibacterium. J Magn Reson Analysis 2: 297-304.
60. Cardoso FS, Gaspar P, Hugenholtz J, Ramos A, Santos H (2004) Enhancement of trehalose production in dairy propionibacteria through manipulation of environmental conditions. Int J Food Microbiol 91: 195-204.
61. Cardoso FS, Castro RF, Borges N, Santos H (2007) Biochemical and genetic characterization of the pathways for trehalose metabolism in Propionibacterium freudenreichii, and their role in stress response. Microbiol 153: 270-280.
62. Boyaval P, Deborde C, Corre C, Blanco C, Begué E (1999) Stress and osmoprotection in propionibacteria. Lait 79: 59-69.
63. Leverrier P, Fremont Y, Rouault A, Boyaval P, Jan G (2005) In vitro tolerance to digestive stresses of propionibacteria: influence of food matrices. Food Microbiology 22: 11-18.
64. Leverrier P (2003) Susceptibilité et adaptation de Propionibacterium freudenreichii aux stress digestifs [dissertation].
65. Lemée R, Rouault A, Guezenec S, Lortal S (1994) Autolysis of 57 strains of dairy Propionibacteria. Lait 74: 241-251.
66. Schroeckh V, Martin K (2006) Resuscitation-promoting factors: distribution among actinobacteria, synthesis during life-cycle and biological activity. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology 89: 359-365.
67. Kaprelyants AS, Gottschal JC, Kell DB (1993) Dormancy in non-sporulating bacteria. FEMS Microbiol Rev 10: 271-285.
68. Leverrier P, Vissers JPC, Rouault A, Boyaval P, Jan G (2004) Mass spectrometry proteomic analysis of stress adaptation reveals both common and distinct response pathways in Propionibacterium freudenreichii. Arch Microbiol 181: 215-230.
69. Rigoulay C, Poquet I, Madsen SM, Gruss A (2004) Expression of the Staphylococcus aureus surface proteins HtrA(1) and HtrA(2) in Lactococcus lactis. FEMS Microbiol Lett 237: 279-288.
70. Sanchez B, Reyes-Gavilan CGD, Margolles A (2006) The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environmental Microbiology 8: 1825-1833.
71. Anastasiou R, Leverrier P, Krestas I, Rouault A, Kalantzopoulos G, et al. (2006) Changes in protein synthesis during thermal adaptation of Propionibacterium freudenreichii subsp. shermanii. Int J Food Microbiol 108: 301-314.
72. Singh VK, Hattangady DS, Giotis ES, Singh AK, Chamberlain NR, et al. (2008) Insertional inactivation of branched-chain alpha-keto acid dehydrogenase in Staphylococcus aureus leads to decreased branched-chain membrane fatty acid content and increased susceptibility to certain stresses. Appl Environ Microbiol 74: 5882-5890.
73. Begley M, Gahan CGM, Hill C (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29: 625-651.
74. Yebra MJ, Zuniga M, Beaufils S, Perez-Martinez G, Deutscher J, et al. (2007) Identification of a gene cluster enabling Lactobacillus casei BL23 to utilize myo-inositol. Appl Environ Microbiol 73: 3850-3858.
75. Barinov A, Loux V, Hammani A, Nicolas P, Langella P, et al. (2009) Prediction of surface exposed proteins in Streptococcus pyogenes, with a potential application to other Gram-positive bacteria. Proteomics 9: 61-73.
76. Lebeer S, Vanderleyden J, De Keersmaecker SCJ (2008) Genes and molecules of Lactobacilli supporting probiotic action. Microbiol Mol Biol R 72: 728-764.
77. Konstantinov SR, Smidt H, de Vos WM, Bruijns SCM, Singh SK, et al. (2008) S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. P Acad Nat Sci USA 105: 19474-19479.
78. Guglielmetti S, Tamagnini I, Mora D, Minuzzo M, Scarafoni A, et al. (2008) Implication of an outer surface lipoprotein in adhesion of Bifidobacterium bifidum to Caco-2 cells. Appl Environ Microbiol 74: 4695-4702.
79. de Palencia PF, Werning ML, Sierra-Filardi E, Duenas MT, Irastorza A, et al. (2009) Probiotic properties of the 2-substituted (1,3)-beta-D-glucan-producing bacterium Pediococcus parvulus 2.6. Appl Environ Microbiol 75: 4887-4891.
80. Ouwehand AC, Suomalainen T, Tolkko S, Salminen S (2002) In vitro adhesion of propionic acid bacteria to human intestinal mucus. Lait 82: 123-130.
81. Jan G, Belzacq AS, Haouzi D, Rouault A, Metivier D, et al. (2002) Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ 9: 179-188.
82. Lan A, Lagadic-Gossmann D, Lemaire C, Brenner C, Jan G (2007) 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 12: 573-591.
83. Lan A, Bruneau A, Bensaada M, Philippe C, Bellaud P, et al. (2008) 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 100: 1251-1259.
84. Dupuis C, Corre C, Boyaval P (1995) Proteinase activity of dairy Propionibac-terium. Appl Microbiol Biotechnol 42: 750-755.
85. Suoniemi A, Tynkkynen S (2002) Cloning and characterization of an esterase from Propionibacterium freudenreichi ssp. shermanii. Lait 82: 81-89.
86. Dherbécourt J, Maillard MB, Catheline D, Thierry A (2008) Production of branched-chain aroma compounds by Propionibacterium freudenreichii: links with the biosynthesis of membrane fatty acids. J Appl Microbiol 105: 977-985.
87. Vallenet D, Nordmann P, Barbe V, Poirel L, Mangenot S, et al. (2008) Comparative Analysis of Acinetobacters: Three Genomes for Three Lifestyles. Plos One 3.
88. Bryson K, Loux V, Bossy R, Nicolas P, Chaillou S, et al. (2006) AGMIAL: implementing an annotation strategy for prokaryote genomes as a distributed system. Nucleic Acids Res 34: 3533-3545.
89. Thybert D, Avner S, Lucchetti-Miganeh C, Cheron A, Barloy-Hubler F (2008) OxyGene: an innovative platform for investigating oxidative-response genes in whole prokaryotic genomes. Bmc Genomics 9.
90. Gao F, Zhang CT (2008) Ori-Finder: A web-based system for finding oriCs in unannotated bacterial genomes. Bmc Bioinformatics 9.
91. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, et al. (2009) Circos: An information aesthetic for comparative genomics. Genome Research 19: 1639-1645.
92. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, et al. (2004) Versatile and open software for comparing large genomes. Genome Biology 5.