Rewiring global regulator cAMP receptor protein (CRP) to improve E. coli tolerance towards low pH

Journal of Biotechnology

Volumn 173, Issue 1, 2014, Pages 68-75

  Basak, Souvik ^a   Geng, Hefang ^a   Jiang, Rongrong ^a  

^a Nanyang Technological University   (Singapore)

Author keywords

CAMP receptor protein; Random mutagenesis; Strain engineering; Transcriptional engineering

Indexed keywords

CAMP RECEPTOR PROTEINS; DIFFERENTIAL BINDING; GLUTAMATE DECARBOXYLASE; RANDOM MUTAGENESIS; REVERSE TRANSCRIPTION PCR; STRAIN ENGINEERING; TRANSCRIPTION PROFILES; TRANSCRIPTIONAL ENGINEERINGS;

BINDING ENERGY; ENGINEERING; ESCHERICHIA COLI; MUTAGENESIS; POLYMERASE CHAIN REACTION; PROTEINS;

TRANSCRIPTION;

CYCLIC AMP BINDING PROTEIN; GLUTAMATE DECARBOXYLASE;

ACID TOLERANCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GROWTH INHIBITION; GROWTH RATE; HEAT TOLERANCE; MUTAGENESIS; MUTANT; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS; TRANSCRIPTION REGULATION;

CAMP RECEPTOR PROTEIN; RANDOM MUTAGENESIS; STRAIN ENGINEERING; TRANSCRIPTIONAL ENGINEERING;

ACETIC ACID; ADAPTATION, PHYSIOLOGICAL; BINDING SITES; CYCLIC AMP RECEPTOR PROTEIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GLUTAMATE DECARBOXYLASE; METABOLIC ENGINEERING; MUTAGENESIS; PROMOTER REGIONS, GENETIC; SUCCINIC ACID; TEMPERATURE;

EID: 84893352171     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.01.015     Document Type: Article

References (64)

1. Aono R., Aibe K., et al. Preparation of organic solvent tolerant mutants from Escherichia coli K-12. Agric. Biol. Chem. 1991, 55(7):1935-1938.
2. Baba T., Ara T., et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2006, 2:2006.0008.
3. Basak S., Hao S., et al. Error-prone PCR of global transcription factor cyclic AMP receptor protein for enhanced organic solvent (toluene) tolerance. Process Biochem. 2012, 47:2152-2158.
4. Basak S., Jiang R. Enhancing E. coli tolerance towards oxidative stress via engineering its global regulator cAMP receptor protein (CRP). PLoS ONE 2012, 7(12):e51179.
5. Bergholz T.M., Vanaja S.K., et al. Gene expression induced in Escherichia coli O57:H7 upon exposure to model apple juice. Appl. Environ. Microbiol. 2009, 75(11):3542-3553.
6. Blank G., Cho C.H., et al. Acid tolerance of Escherichia coli following cold shock treatment. J. Food Saf. 2003, 23(2):127-144.
7. Bruno-Bárcena J.M., Azcárate-Peril M.A., et al. Role of antioxidant enzymes in bacterial resistance to organic acids. Appl. Environ. Microbiol. 2010, 76(9):2747-2753.
8. Budin-Verneuil A., Pichereau V., et al. Proteomic characterization of the acid tolerance response in Lactococcus lactis MG1363. Proteomics 2005, 5(18):4794-4807.
9. Calhoun L.N., Kim J.N., et al. The DNA-binding protein Dps functions as a global regulator in starved Salmonella enterica serovar enteritidis during starvation. Int. J. Microbiol. Res. 2011, 3(3):136-137.
10. Castanie-Cornet M.P., Foster J.W. Escherichia coli acid resistance: cAMP receptor protein and a 20bp cis-acting sequence control pH and stationary phase expression of the gadA and gadBC glutamate decarboxylase genes. Microbiology 2001, 147(Pt 3):709-715.
11. Castanie-Cornet M.P., Penfound T.A., et al. Control of acid resistance in Escherichia coli. J. Bacteriol. 1999, 181(11):3525-3535.
12. Chang Y.Y., Cronan J.E. Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol. Microbiol. 2002, 33(2):249-259.
13. Cheville A.M., Arnold K.W., et al. rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 1996, 62(5):1822-1824.
14. Choi S.H., Baumler D.J., et al. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 2000, 66(9):3911-3916.
15. Chong H., Huang L., et al. Improving ethanol tolerance of Escherichia coli by rewiring its global regulator cAMP receptor protein (CRP). PLoS ONE 2013, 8(2):e57628.
16. De Biase D., Tramonti A., et al. The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol. Microbiol. 1999, 32(6):1198-1211.
17. Deng Y., Ryu J.H., et al. Tolerance of acid-adapted and non-adapted Escherichia coli O157:H7 cells to reduced pH as affected by type of acidulant. J. Appl. Microbiol. 1999, 86(2):203-210.
18. Foster J.W. Acid stress responses of Salmonella and E. coli: survival mechanisms, regulation, and implications for pathogenesis. J. Microbiol. 2001, 39(2):89-94.
19. Grant M.A. Comparison of Escherichia coli O157:H7 enrichment in spiked produce samples. J. Food. Prot. 2008, 71(1):139-145.
20. Grotewold E. Transcription factors for predictive plant metabolic engineering: are we there yet?. Curr. Opin. Biotechnol. 2008, 19(2):138-144.
21. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 2002, 66(3):373-395.
22. Hickey E.W., Hirshfield I.N. Low pH induced effects on patterns of protein synthesis and on internal pH in Escherichia coli and Salmonella typhimurium. Appl. Environ. Microbiol. 1990, 56(4):1038-1045.
23. Hung K.F., Byrd J.J., et al. Reduction of acid tolerance by tetracycline in Escherichia coli expressing tetA(C) is reversed by cations. Appl. Environ. Microbiol. 2006, 72(6):4472-4474.
24. Hungund B.S., Gupta S.G. Strain improvement of Gluconacetobacter xylinus NCIM 2526 for bacterial cellulose production. African J. Biotechnol. 2010, 9(32):5170-5172.
25. Kannaiah Goud R., Venkata Mohan S. Acidic and alkaline shock pretreatment to enrich acidogenic biohydrogen producing mixed culture: long term synergetic evaluation of microbial inventory, dehydrogenase activity and bio-electro kinetics. RSC Adv. 2012, 2:6336-6353.
26. Kannan G., Wilks J.C., et al. Rapid acid treatment of Escherichia coli: transcriptomic response and recovery. BMC Microbiol. 2008, 8(37).
27. Keasling J.D. Manufacturing molecules through metabolic engineering. Science 2010, 330:1355-1358.
28. King T., Lucchini S., et al. Transcriptomic analysis of Escherichia coli O157:H7 and K-12 cultures exposed to inorganic and organic acids in stationary phase reveals acidulant- and strain-specific acid tolerance responses. Appl. Environ. Microbiol. 2010, 76(19):6514-6528.
29. Kumar P., Joshi D.C., et al. Mapping conformational transitions in cyclic AMP receptor protein crystal structure and normal-mode analysis of Mycobacterium tuberculosis apo-cAMP receptor protein. Biophys. J. 2010, 98:305-314.
30. Leenanon B., Drake M.A. Acid stress, starvation, and cold stress affect poststress behavior of Escherichia coli O157:H7 and nonpathogenic Escherichia coli. J. Food Prot. 2001, 64(7):970-974.
31. Loewen P.C., Hu B., et al. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 1998, 44:707-717.
32. Ma H.W., Kumar B., et al. An extended transcriptional regulatory network of Escherichia coli and analysis of its hierarchical structure and network motifs. Nucleic Acids Res. 2004, 32(22):6643-6649.
33. Mao Y., Doyle M.P., et al. Insertion mutagenesis of wca reduces acid and heat tolerance of enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 2001, 183(12):3811-3815.
34. Martinez A., Kolter R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 1997, 179(16):5188-5194.
35. Maurer L.M., Yohannes E., et al. pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J. Bacteriol. 2005, 187(1):304-319.
36. Morel F., Delmas F., et al. Improved acid tolerance of a recombinant strain of Escherichia coli expressing genes from the acidophilic bacterium Oenococcus oeni. Lett. Appl. Microbiol. 2001, 33(2):126-130.
37. Nair S., Finkel S.E. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 2004, 186(13):4192-4198.
38. Passner J.M., Schultz S.C., et al. Modeling the cAMP-induced allosteric transition using the crystal structure of CAP-cAMP at 2.1Å resolution. J. Mol. Biol. 2000, 304(5):847-859.
39. Rowbury R.J., Goodson M. Glucose-induced acid tolerance appearing at neutral pH in log-phase Escherichia coli and its reversal by cyclic AMP. J. Appl. Microbiol. 1998, 85(3):615-620.
40. Rowbury R.J., Goodson M., et al. Sodium chloride induces an NhaA/NhaR-independent acid sensitivity at neutral external pH in Escherichia coli. Appl. Environ. Microbiol. 1994, 60(5):1630-1634.
41. Ryu J.H., Beuchat L.R. Influence of acid tolerance responses on survival, growth, and thermal cross-protection of Escherichia coli O157:H7 in acidified media and fruit juices. Int. J. Food Microbiol. 1998, 45(3):185-193.
42. Sánchez A.M., Bennett G.N., et al. Efficient succinic acid production from glucose through overexpression of pyruvate carboxylase in an Escherichia coli alcohol dehydrogenase and lactate dehydrogenase mutant. Biotechnol. Prog. 2005, 21(2):358-365.
43. Sang Ho C., Baumler D.J., et al. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 2000, 66(9):3911-3916.
44. Santos P.M., Di B.I., et al. New broad-host-range promoter probe vectors based on the plasmid RK2 replicon. FEMS Microbiol. Lett. 2001, 195(1):91-96.
45. Schultz J.E., Matin A. Molecular and functional characterization of a carbon starvation gene of Escherichia coli. J. Mol. Biol. 1991, 218(1):129-140.
46. Slonczewski J.L., Rosen B.P., et al. pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate. Proc. Natl. Acad. Sci. 1981, 78(10):6271-6275.
47. Small P., Blankenhorn D., et al. Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J. Bacteriol. 1994, 176(6):1729-1737.
48. Stephanopoulos G. Challenges in engineering microbes for biofuels production. Science 2007, 315(5813):801-804.
49. Stim-Herndon K.P., Flores T.M., et al. Molecular characterization of adiY, a regulatory gene which affects expression of the biodegradative acid-induced arginine decarboxylase gene (adiA) of Escherichia coli. Microbiology 1996, 147(5):1311-1320.
50. Stincone A., Daudi N., et al. A systems biology approach sheds new light on Escherichia coli acid resistance. Nucleic Acids Res. 2011, 39(17):7512-7528.
51. Suthers P.F., Cameron D.C. Production of 3-hydroxy propionic acid in recombinant organisms. PCT WO 01-16346 2001.
52. Sweetlove L.J., Last R.L., et al. Predictive metabolic engineering: a goal for systems biology. Plant Physiol. 2003, 132(2):420-425.
53. Taherzadeh M.J., Karimi K. Acid-based hydrolysis processes for ethanol from lignocellulosic materials: a review. BioResources 2007, 2(3):472-499.
54. Van Dyk T.K., Templeton L.J., et al. Characterization of the Escherichia coli AaeAB efflux pump: a metabolic relief valve. J. Bacteriol. 2004, 186(21):7196-7204.
55. Vemuri G.N., Eiteman M.A., et al. Effects of growth mode and pyruvate carboxylase on succinic acid production by metabolically engineered strains of Escherichia coli. Appl. Environ. Microbiol. 2002, 68(4):1715-1727.
56. Wang G., Doyle M.P. Heat shock response enhances acid tolerance of Escherichia coli O157:H7. Lett. Appl. Microbiol. 1998, 26(1):31-34.
57. Wang Y. Development of Acetic-acid Tolerant Zymomonas mobilis Strains through Adaptation 2008, 118. (Master of Science), Chemical and Biomolecular Engineering, Georgia Institute of Technology.
58. Warnecke T., Gill R.T. Organic acid toxicity, tolerance, and production in Escherichia coli biorefining applications. Microb. Cell Fact. 2005, 4.
59. Wei P., Li Z., et al. Genome shuffling in the ethanologenic yeast Candida krusei to improve acetic acid tolerance. Biotechnol. Appl. Biochem. 2008, 49(2):113-120.
60. Yohannes E., Barnhart D.M., et al. pH-dependent catabolic protein expression during anaerobic growth of Escherichia coli K-12. J. Bacteriol. 2004, 186:192-199.
61. Yu K., Hu S., et al. A high throughput colorimetric assay to measure the activity of glutamate decarboxylase. Enzyme Microb. Technol. 2011, 49(3):272-276.
62. Zhang H., Chong H., et al. Random mutagenesis of global transcription factor cAMP receptor protein for improved osmotolerance. Biotechnol. Bioeng. 2012, 109(5):1165-1172.
63. Zhang H., Chong H., et al. Engineering global transcription factor cyclic AMP receptor protein of Escherichia coli for improved 1-butanol tolerance. Appl. Microbiol. Biotechnol. 2012, 94(4):1107-1117.
64. Zilberstein D., Agmon V., et al. Escherichia coli intracellular pH, membrane potential, and cell growth. J. Bacteriol. 1984, 158(1):246-252.