Mechanism Analysis of Acid Tolerance Response of Bifidobacterium longum subsp. longum BBMN 68 by Gene Expression Profile Using RNA-Sequencing

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Jin, Junhua ^a   Zhang, Bing ^b   Guo, Huiyuan ^a,c   Cui, Jianyun ^a   Jiang, Lu ^a,d   Song, Shuhui ^b   Sun, Min ^b   Ren, Fazheng ^a,d   Chang, Yung Fu ^e  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b Chinese Academy of Sciences   (China)

^c Beijing Higher Institution Engineering Research Center of Animal Product   (China)

^d Beijing Key Laboratory of Nutrition   (China)

^e Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATHIONINE; CYSTEINE; GAMMA GLUTAMYLCYSTEINE; PROTON;

ACID TOLERANCE; ACIDITY; ADAPTATION; ARTICLE; BIFIDOBACTERIUM LONGUM; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HIGH THROUGHPUT SEQUENCING; INTRACELLULAR SIGNALING; NONHUMAN; NUCLEOTIDE SEQUENCE; OVERALL SURVIVAL; PH; RNA SEQUENCE; SURVIVAL RATE; UPREGULATION;

ADENOSINE TRIPHOSPHATASES; BIFIDOBACTERIUM; DNA, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; RNA, BACTERIAL; SEQUENCE ANALYSIS, RNA;

BIFIDOBACTERIUM LONGUM;

EID: 84870898411     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050777     Document Type: Article

References (56)

1. Masco L, Huys G, De Brandt E, Temmerman R, Swings J, (2005) Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. International Journal of Food Microbiology 102: 221-230.
2. Champagne CP, Gardner NJ, Roy D, (2005) Challenges in the addition of probiotic cultures to foods. Critical Reviews in Food Science and Nutrition 45: 61-84.
3. O'May GA, Reynolds N, Smith AR, Kennedy A, Macfarlane GT, (2005) Effect of pH and antibiotics on microbial overgrowth in the stomachs and duodena of patients undergoing percutaneous endoscopic gastrostomy feeding. Journal of Clinical Microbiology 43: 3059-3065.
4. Hamilton IR, Buckley ND, (1991) Adaptation by Streptococcus mutans to acid tolerance. Oral microbiology and immunology 6: 65-71.
5. Matsui R, Cvitkovitch D, (2010) Acid tolerance mechanisms utilized by Streptococcus mutans. Future Microbiology 5: 403-417.
6. Rallu F, Gruss A, Maguin E, (1996) Lactococcus lactis and stress. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology 70: 243-251.
7. Van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, et al. (2002) Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology 82: 187-216.
8. De Angelis M, Bini L, Pallini V, Cocconcelli PS, Gobbetti M, (2001) The acid-stress response in Lactobacillus sanfranciscensis CB1. Microbiology 147: 1863-1873.
9. Maus JE, Ingham SC, (2003) Employment of stressful conditions during culture production to enhance subsequent cold- and acid-tolerance of bifidobacteria. Journal of Applied Microbiology 95: 146-154.
10. Saarela M, Rantala M, Hallamaa K, Nohynek L, Virkajärvi I, et al. (2004) Stationary-phase acid and heat treatments for improvement of the viability of probiotic lactobacilli and bifidobacteria. Journal of Applied Microbiology 96: 1205-1214.
11. Ventura M, Canchaya C, Van Sinderen D, Fitzgerald GF, Zink R, (2004) Bifidobacterium lactis DSM 10140: Identificafion of the atp (atpBEFHAGDC) operon and analysis of its genetic structure, characteristics, and phylogeny. Applied and Environmental Microbiology 70: 3110-3121.
12. Jin J, Liu S, Zhao L, Ge K, Mao X, et al. (2011) Changes in ffh, uvrA, groES and dnaK mRNA abundance as a function of acid-adaptation and growth phase in Bifidobacterium longum BBMN68 isolated from healthy centenarians. Current Microbiology 62: 612-617.
13. Sánchez B, Champomier-Vergès MC, Collado MDC, Anglade P, Baraige F, et al. (2007) Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Applied and Environmental Microbiology 73: 6450-6459.
14. Waddington L, Cyr T, Hefford M, Hansen LT, Kalmokoff M, (2010) Understanding the acid tolerance response of bifidobacteria. Journal of Applied Microbiology 108: 1408-1420.
15. Matsumoto M, Ohishi H, Benno Y, (2004) H+-ATPase activity in Bifidobacterium with special reference to acid tolerance. International Journal of Food Microbiology 93: 109-113.
16. Cappa F, Cattivelli D, Cocconcelli PS, (2005) The uvrA gene is involved in oxidative and acid stress responses in Lactobacillus helveticus CNBL1156. Research in Microbiology 156: 1039-1047.
17. Jayaraman GC, Penders JE, Burne RA, (1997) Transcriptional analysis of the Streptococcus mutans hrcA, grpE and dnaK genes and regulation of expression in response to heat shock and environmental acidification. Molecular Microbiology 25: 329-341.
18. Hanna MN, Ferguson RJ, Li YH, Cvitkovitch DG, (2001) uvrA is an acid-inducible gene involved in the adaptive response to low pH in Streptococcus mutans. Journal of Bacteriology 183: 5964-5973.
19. Zúñiga M, Champomier-Verges M, Zagorec M, Pérez-Martínez C, (1998) Structural and functional analysis of the gene cluster encoding the enzymes of the arginine deiminase pathway of Lactobacillus sake. Journal of Bacteriology 180: 4154-4159.
20. Tonon T, Lonvaud-Funel A, (2000) Metabolism of arginine and its positive effect on growth and revival of Oenococcus oeni. Journal of Applied Microbiology 89: 526-531.
21. Wen ZT, Burne RA, (2004) LuxS-Mediated Signaling in Streptococcus mutans is Involved in Regulation of Acid and Oxidative Stress Tolerance and Biofilm Formation. Journal of Bacteriology 186: 2682-2691.
22. Moslehi-Jenabian S, Gori K, Jespersen L, (2009) AI-2 signalling is induced by acidic shock in probiotic strains of Lactobacillus spp. International Journal of Food Microbiology 135: 295-302.
23. Yang H, Liu A, Zhang M, Ibrahim SA, Pang Z, et al. (2009) Oral administration of live bifidobacterium substrains isolated from centenarians enhances intestinal function in mice. Current Microbiology 59: 439-445.
24. Yang Hy, Liu Sl, Ibrahim SA, Zhao L, Jiang Jl, et al. (2009) Oral administration of live Bifidobacterium substrains isolated from healthy centenarians enhanced immune function in BALB/c mice. Nutrition Research 29: 281-289.
25. Hao Y, Huang D, Guo H, Xiao M, An H, et al. (2011) Complete genome sequence of bifidobacterium longum subsp. longum BBMN68, a new strain from a healthy Chinese centenarian. Journal of Bacteriology 193: 787-788.
26. Cui P, Lin Q, Ding F, Xin C, Gong W, et al. (2010) A comparison between ribo-minus RNA-sequencing and polyA-selected RNA-sequencing. Genomics 96: 259-265.
27. Zhao W, Liu W, Tian D, Tang B, Wang Y, et al. (2011) wapRNA: A web-based application for the processing of RNA sequences. Bioinformatics 27: 3076-3077.
28. Vandecasteele SJ, Peetermans WE, Merckx R, Van Ranst M, Van Eldere J, (2002) Use of gDNA as internal standard for gene expression in staphylococci in vitro and in vivo. Biochemical and Biophysical Research Communications 291: 528-534.
29. Even S, Lindley ND, Loubière P, Cocaign-Bousquet M, (2002) Dynamic response of catabolic pathways to autoacidification in Lactococcus lactis: Transcript profiling and stability in relation to metabolic and energetic constraints. Molecular Microbiology 45: 1143-1152.
30. Chang YY, Cronan JE Jr, (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Molecular Microbiology 33: 249-259.
31. To TMH, Grandvalet C, Tourdot-Maréchal R, (2011) Cyclopropanation of membrane unsaturated fatty acids is not essential to the acid stress response of Lactococcus lactis subsp. cremoris. Applied and Environmental Microbiology 77: 3327-3334.
32. Lee YJ, Ishiwata A, Ito Y, (2009) Synthesis of undecaprenyl pyrophosphate-linked glycans as donor substrates for bacterial protein N-glycosylation. Tetrahedron 65: 6310-6319.
33. Sakoh M, Ito K, Akiyama Y, (2005) Proteolytic activity of HtpX, a membrane-bound and stress-controlled protease from Escherichia coli. Journal of Biological Chemistry 280: 33305-33310.
34. Matuszewska E, Kwiatkowska J, Ratajczak E, Kuczyńska-Wiśnik D, Laskowska E, (2009) Role of Escherichia coli heat shock proteins IbpA and IbpB in protection of alcohol dehydrogenase AdhE against heat inactivation in the presence of oxygen. Acta Biochimica Polonica 56: 55-61.
35. Kitagawa M, Miyakawa M, Matsumura Y, Tsuchido T, (2002) Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. European Journal of Biochemistry 269: 2907-2917.
36. Ventura M, Kenny JG, Zhang Z, Fitzgerald GF, van Sinderen D, (2005) The clpB gene of Bifidobacterium breve UCC 2003: Transcriptional analysis and first insights into stress induction. Microbiology 151: 2861-2872.
37. Ventura M, Zhang Z, Cronin M, Canchaya C, Kenny JG, et al. (2005) The ClgR protein regulates transcription of the clpP operon in Bifidobacterium breve UCC 2003. Journal of Bacteriology 187: 8411-8426.
38. Zhang J, Fu RY, Hugenholtz J, Li Y, Chen J, (2007) Glutathione protects Lactococcus lactis against acid stress. Applied and Environmental Microbiology 73: 5268-5275.
39. Kim EK, Cha CJ, Cho YJ, Cho YB, Roe JH, (2008) Synthesis of γ-glutamylcysteine as a major low-molecular-weight thiol in lactic acid bacteria Leuconostoc spp. Biochemical and Biophysical Research Communications 369: 1047-1051.
40. Vercruysse M, Fauvart M, Jans A, Beullens S, Braeken K, et al. (2011) Stress response regulators identified through genome-wide transcriptome analysis of the (p)ppGpp-dependent response in Rhizobium etli. Genome Biology 12: R17.
41. Svitil AL, Cashel M, Zyskind JW, (1993) Guanosine tetraphosphate inhibits protein synthesis in vivo. A possible protective mechanism for starvation stress in Escherichia coli. Journal of Biological Chemistry 268: 2307-2311.
42. Brockmann-Gretza O, Kalinowski J, (2006) Global gene expression during stringent response in Corynebacterium glutamicum in presence and absence of the rel gene encoding (p)ppGpp synthase. BMC Genomics 7: 230.
43. Rao NN, Gómez-García MR, Kornberg A, (2009) Inorganic polyphosphate: Essential for growth and survival. Annu Rev Biochem 78: 605-647.
44. Peng L, Luo WY, Zhao T, Wan CS, Jiang Y, et al. (2012) Polyphosphate kinase 1 is required for the pathogenesis process of meningitic Escherichia coli K1 (RS218). Future Microbiology 7: 411-423.
45. Qian Y, Borowski WJ, Calhoon WD, (2011) Intracellular granule formation in response to oxidative stress in Bifidobacterium. International Journal of Food Microbiology 145: 320-325.
46. Gutierrez JA, Crowley PJ, Cvitkovitch DG, Brady LJ, Hamilton IR, et al. (1999) Streptococcus mutans ffh, a gene encoding a homologue of the 54 kDa subunit of the signal recognition particle, is involved in resistance to acid stress. Microbiology 145: 357-366.
47. Kremer BHA, Van der Kraan M, Crowley PJ, Hamilton IR, Brady LJ, et al. (2001) Characterization of the sat operon in Streptococcus mutans: Evidence for a role of Ffh in acid tolerance. Journal of Bacteriology 183: 2543-2552.
48. Senadheera D, Krastel K, Mair R, Persadmehr A, Abranches J, et al. (2009) Inactivation of VicK affects acid production and acid survival of Streptococcus mutans. Journal of Bacteriology 191: 6415-6424.
49. Shao H, Demuth DR, (2010) Quorum sensing regulation of biofilm growth and gene expression by oral bacteria and periodontal pathogens. Periodontology 2000 52: 53-67.
50. Serrazanetti DI, Ndagijimana M, Sado-Kamdem SL, Corsetti A, Vogel RF, et al. (2011) Acid stress-mediated metabolic shift in Lactobacillus sanfranciscensis LSCE1. Applied and Environmental Microbiology 77: 2656-2666.
51. Broadbent JR, Larsen RL, Deibel V, Steele JL, (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. Journal of Bacteriology 192: 2445-2458.
52. Wu C, Zhang J, Chen W, Wang M, Du G, et al. (2012) A combined physiological and proteomic approach to reveal lactic-acid-induced alterations in Lactobacillus casei Zhang and its mutant with enhanced lactic acid tolerance. Applied Microbiology and Biotechnology 93: 707-722.
53. Vendeville A, Winzer K, Heurlier K, Tang CM, Hardie KR, (2005) Making 'sense' of metabolism: Autoinducer-2, LuxS and pathogenic bacteria. Nature Reviews Microbiology 3: 383-396.
54. Loenen WAM, (2006) S-Adenosylmethionine: Jack of all trades and master of everything? Biochemical Society Transactions 34: 330-333.
55. Jiang M, Cao Y, Guo ZF, Chen M, Chen X, et al. (2007) Menaquinone biosynthesis in Escherichia coli: Identification of 2-succinyl-5-enolpyruvyl-6-hydroxy-3-cyclohexene-1-carboxylate as a novel intermediate and re-evaluation of MenD activity. Biochemistry 46: 10979-10989.
56. Parry-Hanson AA, Jooste PJ, Buys EM, (2010) Relative gene expression in acid-adapted Escherichia coli O157:H7 during lactoperoxidase and lactic acid challenge in Tryptone Soy Broth. Microbiological Research 165: 546-556.