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

Volumn 93, Issue 2, 2012, Pages 707-722

  Wu, Chongde ^a   Zhang, Juan ^a   Chen, Wei ^a   Wang, Miao ^a   Du, Guocheng ^a   Chen, Jian ^a  

^a JIANGNAN UNIVERSITY   (China)

Author keywords

2D DIGE; Acid stress; i TRAQ; Lactobacillus casei; Physiological analysis

Indexed keywords

2D DIGE; ACID STRESS; I-TRAQ; LACTOBACILLUS CASEI; PHYSIOLOGICAL ANALYSIS;

ARGININE; BIOSYNTHESIS; CELL CULTURE; DAIRY PRODUCTS; GLUCOSE; INDUSTRIAL APPLICATIONS; LACTIC ACID; PHYSIOLOGY; PLANTS (BOTANY); RNA;

ACID RESISTANCE;

ADENOSINE TRIPHOSPHATASE; ARGININE; ASPARTIC ACID; CHAPERONE; LACTIC ACID; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE;

AMINO ACID; BACTERIUM; COMPARATIVE STUDY; ELECTROKINESIS; FERMENTATION; MUTATION; PH; PHYSIOLOGICAL RESPONSE; PHYSIOLOGY; PROTEOMICS; TOLERANCE;

ACIDITY; ARTICLE; BACTERIAL STRAIN; CELL METABOLISM; CELL PH; CELL SURVIVAL; DNA REPLICATION; ENZYME ACTIVITY; GLYCOLYSIS; LACTOBACILLUS CASEI; NONHUMAN; PHYSIOLOGY; PROTEIN EXPRESSION; PROTEOMICS; RNA SYNTHESIS; RNA TRANSLATION; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; WILD TYPE;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; CYTOPLASM; DRUG TOLERANCE; HYDROGEN-ION CONCENTRATION; LACTIC ACID; LACTOBACILLUS CASEI; MUTATION; PROTEOME; PROTON PUMPS; STRESS, PHYSIOLOGICAL; UNITED STATES;

LACTOBACILLUS CASEI;

EID: 84856275260     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3757-6     Document Type: Article

References (61)

1. Abdullah-Al-Mahin SS, Higashi C, Matsumoto S, Sonomoto K (2010) Improvement of multiple-stress tolerance and lactic acid production in Lactococcus lactis NZ9000 under conditions of thermal stress by heterologous expression of Escherichia coli dnaK. Appl Environ Microb 76(13):4277-4285
2. Belli WA, Marquis RE (1991) Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture. Appl Environ Microb 57(4):1134-1138
3. Bender G, Marquis R (1987) Membrane ATPases and acid tolerance of Actinomyces viscosus and Lactobacillus casei. Appl Environ Microb 53(9):2124-2128
4. Breeuwer P, Drocourt J, Rombouts F, Abee T (1996) A novel method for continuous determination of the intracellular pH in bacteria with the internally conjugated fluorescent probe 5 (and 6-)-carboxyfluorescein succinimidyl ester. Appl Environ Microb 62(1):178-183
5. Broadbent JR, Larsen RL, Deibel V, Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192:2445-2458
6. Brown ED, Vivas EI, Walsh CT, Kolter R (1995) MurA (MurZ), the enzyme that catalyzes the first committed step in peptidoglycan biosynthesis, is essential in Escherichia coli. J Bacteriol 177(14):4194-4197
7. Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich DS, Maguin E (2005) Proteomic characterization of the acid tolerance response in Lactococcus lactis MG1363. Proteomics 5(18):4794-4807. doi: 10.1002/pmic.200401327 (Pubitemid 43016900)
8. Carranza P, Grunau A, Schneider T, Hartmann I, Lehner A, Stephan R, Gehrig P, Grossmann J, Groebel K, Hoelzle LE, Eberl L, Riedel K (2010) A gel-free quantitative proteomics approach to investigate temperature adaptation of the food-borne pathogen Cronobacter turicensis 3032. Proteomics 10(18):3248-3261. doi: 10.1002/pmic.200900460
9. Casiano-Colon A, Marquis R (1988) Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl Environ Microb 54(6):1318-1324
10. Cotter PD, Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol R 67(3):429-453. doi: 10.1128/mmbr.37.3.429-453.2003 (Pubitemid 37122528)
11. De Angelis M, Bini L, Pallini V, Cocconcelli PS, Gobbetti M (2001) The acid-stress response in Lactobacillus sanfranciscensis CB1. Microbiol 147:1863-1873 (Pubitemid 32684928)
12. De Angelis M, Di Cagno R, Huet C, Crecchio C, Fox P, Gobbetti M (2004) Heat shock response in Lactobacillus plantarum. Appl Environ Microb 70(3):1336-1346 (Pubitemid 38365111)
13. De Angelis M, Gobbetti M (2004) Environmental stress responses in Lactobacillus: a review. Proteomics 4(1):106-122 (Pubitemid 38140879)
14. Desmond C, Fitzgerald GF, Stanton C, Ross RP (2004) Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl Environ Microb 70(10):5929-5936. doi: 10.1128/aem.70.10.5929-5936.2004 (Pubitemid 39471838)
15. Fernández M, Zú iga M (2006) Amino acid catabolic pathways of lactic acid bacteria. Crit Rev Microbiol 32(3):155-183 (Pubitemid 44221661)
16. Fountoulakis M, Lahm H (1998) Hydrolysis and amino acid composition analysis of proteins. J Chromatogr A 826(2):109-134 (Pubitemid 28543135)
17. Friedberg E (2003) DNA damage and repair. Nature 421(6921):436-440 (Pubitemid 36157951)
18. Greenacre EJ, Brocklehurst TF (2006) The acetic acid tolerance response induces cross-protection to salt stress in Salmonella typhimurium. Int J Food Microbiol 112(1):62-65. doi: 10.1016/j.ijfoodmicro.2006.05.012 (Pubitemid 44472628)
19. Hartke A, Bouche S, Giard JC, Benachour A, Boutibonnes P, Auffray Y (1996) The lactic acid stress response of Lactococcus lactis subsp. lactis. Curr Microbiol 33(3):194-199 (Pubitemid 26272376)
20. Hormann S, Scheyhing C, Behr J, Pavlovic M, Ehrmann M, Vogel R (2006) Comparative proteome approach to characterize the high-pressure stress response of Lactobacillus sanfranciscensis DSM 20451T. Proteomics 6(6):1878-1885
21. Hutkins RW, Nannen NL (1993) pH homeostasis in lactic acid bacteria. J Dairy Sci 76(8):2354-2365
22. Jung YJ, Min KJ, Yoon KS (2009) Responses of acid-stressed Salmonella typhimurium in broth and chicken patties to subsequent antimicrobial stress with ε-polylysine and combined potassium lactate and sodium diacetate. Food Microbiol 26:467-474
23. Kleerebezem M, Vaughan EE (2009) Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 63:269-290. doi: 10.1146/annurev.micro.091208.073341
24. Kornberg H, Reeves R (1972) Inducible phosphoenolpyruvate-dependent hexose phosphotransferase activities in Escherichia coli. Biochem J 128(5):1339-1344
25. Lambert R, Stratford M (1999) Weak-acid preservatives: modelling microbial inhibition and response. J Appl Microbiol 86(1):157-164 (Pubitemid 29055024)
26. Langereis J, Prinsen B, Coppens C, Koenderman L, Ulfman L (2009) A 2D-DIGE approach to identify proteins involved in inside-out control of integrins. J Proteome Res 8(11):3824-3833
27. Lebeer S, Vanderleyden J, De Keersmaecker SCJ (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol R 72(4):728-764
28. LeBlanc D, Crow V, Lee L, Garon C (1979) Influence of the lactose plasmid on the metabolism of galactose by Streptococcus lactis. J Bacteriol 137(2):878-884 (Pubitemid 9122322)
29. Lee KB, Lee HG, Pi KB, Choi YJ (2008) The effect of low pH on protein expression by the probiotic bacterium Lactobacillus reuteri. Proteomics 8(8):1624-1630 (Pubitemid 351580208)
30. Len ACL, Harty DWS, Jacques NA (2004a) Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiol 150:1339-1351. doi: 10.1099/mic.0.27008-0 (Pubitemid 38744736)
31. Len MCL, Harty DWS, Jacques NA (2004b) Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiol 150:1353-1366. doi: 10.1099/mic.0.26888-0 (Pubitemid 38744737)
32. Leverrier P, Vissers J, 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(3):215-230 (Pubitemid 38316645)
33. MacLellan SR, Helmann JD, Antelmann H (2009) The YvrI alternative sigma factor is essential for acid stress induction of oxalate decarboxylase in Bacillus subtilis. J Bacteriol 191(3):931-939. doi: 10.1128/jb.01435-08
34. Matsui R, Cvitkovitch D (2010) Acid tolerance mechanisms utilized by Streptococcus mutans. Future Microbiol 5(3):403-417
35. Maurer L, Yohannes E, Bondurant S, Radmacher M, Slonczewski J (2005) pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol 187(1):304-319 (Pubitemid 40024207)
36. Men H, Park P, Ge M, Walker S (1998) Substrate synthesis and activity assay for MurG. J Am Chem Soc 120(10):2484-2485 (Pubitemid 28149801)
37. Nascimento MM, Lemos JAC, Abranches J, Goncalves RB, Burne RA (2004) Adaptive acid tolerance response of Streptococcus sobrinus. J Bacteriol 186(19):6383-6390 (Pubitemid 39258119)
38. O'Driscoll B, Gahan C, Hill C (1997) Two-dimensional polyacrylamide gel electrophoresis analysis of the acid tolerance response in Listeria monocytogenes LO28. Appl Environ Microb 63(7):2679-2685 (Pubitemid 27292860)
39. O'Sullivan E, Condon S (1997) Intracellular pH is a major factor in the induction of tolerance to acid and other stresses in Lactococcus lactis. Appl Environ Microb 63(11):4210-4215 (Pubitemid 27485741)
40. Odriscoll B, Gahan CGM, Hill C (1996) Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl Environ Microb 62(5):1693-1698 (Pubitemid 26143445)
41. Parvez S, Malik KA, Kang SA, Kim HY (2006) Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 100(6):1171-1185. doi: 10.1111/j.1365-2672.2006.02963.x (Pubitemid 43739184)
42. Peran L, Camuesco D, Comalada M, Bailon E, Henriksson A, Xaus J, Zarzuelo A, Galvez J (2007) A comparative study of the preventative effects exerted by three probiotics, Bifidobacterium lactis, Lactobacillus casei and Lactobacillus acidophilus, in the TNBS model of rat colitis. J Appl Microbiol 103(4):836-844 (Pubitemid 47493215)
43. Postma P, Lengeler J, Jacobson G (1993) Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol Mol Biol R 57(3):543-594 (Pubitemid 23262509)
44. Randazzo CL, Restuccia C, Romano AD, Caggia C (2004) Lactobacillus casei, dominant species in naturally fermented Sicilian green olives. Int J Food Microbiol 90(1):9-14 (Pubitemid 37522203)
45. Senouci-Rezkallah K, Schmitt P, Jobin M (2011) Amino acids improve acid tolerance and internal pH maintenance in Bacillus cereus ATCC14579 strain. Food Microbiol 28:364-372
46. Serrazanetti DI, Guerzoni ME, Corsetti A, Vogel R (2009) Metabolic impact and potential exploitation of the stress reactions in lactobacilli. Food Microbiol 26(7):700-711
47. Siegumfeldt H, Rechinger KB, Jakobsen M (2000) Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl Environ Microb 66(6):2330-2335 (Pubitemid 30353934)
48. Sixma T (2001) DNA mismatch repair: MutS structures bound to mismatches. Curr Opin Struc Biol 11(1):47-52 (Pubitemid 32155551)
49. Spoering A, Vulic M, Lewis K (2006) GlpD and PlsB participate in persister cell formation in Escherichia coli. J Bacteriol 188(14):5136-5144 (Pubitemid 44051479)
50. Streit F, Delettre J, Corrieu G, Beal C (2008) Acid adaptation of Lactobacillus delbrueckii subsp. bulgaricus induces physiological responses at membrane and cytosolic levels that improves cryotolerance. J Appl Microbiol 105 (4):1071-1080. doi: 10.1111/j.1365-2672.2008.03848.x
51. Takahashi N, Xiao JZ, Miyaji K, Yaeshiima T, Hiramatsu A, Iwatsuki K, Kokubo S, Hosono A (2004) Selection of acid tolerant bifidobacteria and evidence for a low-pH-inducible acid tolerance response in Bifidobacterium longum. J Dairy Res 71(3):340-345. doi: 10.1017/s0022029904000251 (Pubitemid 39059433)
52. Vadeboncoeur C, Pelletier M (1997) The phosphoenolpyruvate: sugar phosphotransferase system of oral streptococci and its role in the control of sugar metabolism. FEMS Microbiol Rev 19(3):187-207 (Pubitemid 27067133)
53. Vadeboncoeur C, St Martin S, Brochu D, Hamilton I (1991) Effect of growth rate and pH on intracellular levels and activities of the components of the phosphoenolpyruvate: sugar phosphotransferase system in Streptococcus mutans Ingbritt. Infect Immun 59(3):900-906
54. Viana R, Pérez-Martínez G, Deutscher J, Monedero V (2005) The glycolytic genes pfk and pyk from Lactobacillus casei are induced by sugars transported by the phosphoenolpyruvate: sugar phosphotransferase system and repressed by CcpA. Arch Microbiol 183(6):385-393 (Pubitemid 41218976)
55. Vrancken G, Rimaux T, Weckx S, De Vuyst L, Leroy F (2009) Environmental pH determines citrulline and ornithine release through the arginine deiminase pathway in Lactobacillus fermentum IMDO 130101. Int J Food Microbiol 135(3):216-222
56. Waddington L, Cyr T, Hefford M, Hansen L, Kalmokoff M (2010) Understanding the acid tolerance response of bifidobacteria. J Appl Microbiol 108(4):1408-1420
57. Warnecke T, Gill RT (2005) Organic acid toxicity, tolerance, and production in Escherichia coli biorefining applications. Microb Cell Fact 4(1):25-32 (Pubitemid 41471958)
58. Wilkins JC, Beighton D, Homer KA (2003) Effect of acidic pH on expression of surface-associated proteins of Streptococcus oralis. Appl Environ Microb 69(9):5290-5296 (Pubitemid 37150753)
59. Wu R, Wang W, Yu D, Zhang W, Li Y, Sun Z, Wu J, Meng H, Zhang H (2009) Proteomic analysis of Lactobacillus casei Zhang, a new probiotic bacterium isolated from traditionally home-made Koumiss in Inner Mongolia of China. Mol Cell Proteomics 10:2321-2338
60. Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6(3):222-233 (Pubitemid 351256317)
61. Zhu Y, Zhang Y, Li Y (2009) Understanding the industrial application potential of lactic acid bacteria through genomics. Appl Microbiol Biot 83(4):597-610