pH-Dependent Catabolic Protein Expression during Anaerobic Growth of Escherichia coli K-12

Journal of Bacteriology

Volumn 186, Issue 1, 2004, Pages 192-199

  Yohannes, Elizabeth ^a   Barnhart, D Michael ^a   Slonczewski, Joan L ^a  

^a KENYON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DSBA PROTEIN; ESCHERICHIA COLI PROTEIN; GENE PRODUCT; GLUTAMATE DECARBOXYLASE; OUTER MEMBRANE PROTEIN A; PERIPLASMIC PROTEIN; PROTEIN ACKA; PROTEIN DEGQ; PROTEIN DHAKLM; PROTEIN GAPA; PROTEIN GATY; PROTEIN GUAB; PROTEIN HDEA; PROTEIN HISC; PROTEIN HISD; PROTEIN HMPA; PROTEIN LPD; PROTEIN MALB; PROTEIN MGLB; PROTEIN NIKA; PROTEIN OPPA; PROTEIN PROX; PROTEIN TNAA; SERINE DEAMINASE; TOLC PROTEIN; UNCLASSIFIED DRUG;

ALKALINITY; ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM CULTURE; CULTURE MEDIUM; ESCHERICHIA COLI K 12; FERMENTATION TECHNIQUE; GADA GENE; GADB GENE; HYPOTHESIS; NONHUMAN; OXIDATION REDUCTION REACTION; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SDAA GENE;

ANAEROBIOSIS; CULTURE MEDIA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; PROTEOME;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI K12; NEGIBACTERIA;

EID: 0347622754     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.1.192-199.2004     Document Type: Article

References (69)

1. Abshire, K. Z., and F. C. Neidhardt. 1993. Analysis of proteins synthesized by Salmonella typhimurium during growth within a host macrophage. J. Bacteriol. 175:3734-3743.
2. Aliabadi, Z., Y. K. Park, J. L. Slonczewski, and J. W. Foster. 1988. Novel regulatory loci controlling oxygen and pH-regulated gene expression in Salmonella typhimurium. J. Bacteriol. 170:842-851.
3. Alonzo, S., M. Heyde, P. Laloi, and R. Portalier. 1998. Analysis of the effect exerted by extracellular pH on the maltose regulon in Escherichia coli K-12. Microbiology 144:3317-3325.
4. Andersen, C., B. Schiffier, A. Charbit, and R. Benz. 2002. pH-induced collapse of the extracellular loops closes Escherichia coli maltoporin and allows the study of asymmetric sugar binding. J. Biol. Chem. 277:41318-41325.
5. Arnold, C. N., J. McElhanon, A. Lee, R. Leonhart, and D. A. Siegele. 2001. Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J. Bacteriol. 183:2178-2186.
6. Auger, E. A., K. E. Redding, T. Plumb, L. C. Childs, S. Y. Meng, and G. N. Bennett. 1989. Construction of lac fusions to the inducible arginine and lysine decarboxylase genes of Escherichia coli K-12. Mol. Microbiol. 3:609-620.
7. Blankenhorn, D., J. Phillips, and J. L. Slonczewski. 1999. Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J. Bacteriol. 181:2209-2216.
8. Böck, A., and G. Sawers. 1996. Fermentation, p. 262-282. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
9. Bunch, P. K., F. Mat-Jan, N. Lee, and D. P. Clark. 1997. The ldhA gene encoding the fermentative lactate dehydrogenase of Escherichia coli. Microbiology 143:187-195.
10. Campbell, J. W., R. M. Morgan-Kiss, and J. Cronan, Jr. 2003. A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic beta-oxidation pathway. Mol. Microbiol. 47:793-805.
11. Castanie-Cornet, M. P., and J. W. Foster. 2001. Escherichia coli acid resistance: cAMP receptor protein and a 20 bp cis-acting sequence control pH and stationary phase expression of the gadA and gadBC glutamate decarboxylase genes. Microbiology 147:709-715.
12. Castanie-Cornet, M. P., T. A. Penfound, D. Smith, J. F. Elliott, and J. W. Foster. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181:3525-3535.
13. de Pina, K., C. Navarro, L. McWalter, D. H. Boxer, N. C. Price, S. M. Kelly, M. A. Mandrand-Berthelot, and L. F. Wu. 1995. Purification and characterization of the periplasmic nickel-binding protein NikA of Escherichia coli K12. Eur. J. Biochem. 227:857-865.
14. Drasar, B. S., M. Shiner, and G. M. McLeod. 1969. Studies on the intestinal flora. I. The bacterial flora of the gastrointestinal tract in healthy and achlorhydric persons. Gastroenterology 56:71-79.
15. Foster, J. W. 2000. Microbial responses to acid stress, p. 99-115. In G. Storz, and R. Hengge-Aronis (ed.), Bacterial stress responses. ASM Press, Washington, D.C.
16. Gajiwala, K. S., and S. K. Burley. 2000. HdeA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J. Mol. Biol. 295:605-612.
17. Gehring. K., C. H. Cheng, H. Nikaido, and B. K. Jap. 1991. Stoichiometry of maltodextrin-binding sites in LamB, an outer membrane protein from Escherichia coli. J. Bacteriol. 173:1873-1878.
18. Giannella, R. A., S. A. Broitman, and N. Zamcheck. 1973. Influence of gastric acidity on bacterial and parasitic enteric infections. A perspective. Ann. Intern. Med. 78:271-276.
19. Grisolia, V., M. S. Carlomagno, A. G. Nappo, and C. B. Bruni. 1985. Cloning, structure, and expression of the Escherichia coli K-12 hisC gene. J. Bacteriol. 164:1317-1323.
20. Gutknecht, R., R. Beutler, L. F. Garcia-Alles, U. Baumann, and B. Erni. 2001. The dihydroxyacetone kinase of Escherichia coli utilizes a phosphoprotein instead of ATP as phosphoryl donor. EMBO J. 20:2480-2486.
21. Hall, H. K., K. L. Karem, and J. W. Foster. 1995. Molecular responses of microbes to environmental pH stress. Adv. Microb. Physiol. 37:229-272.
22. Hand, N. J., and T. J. Silhavy. 2000. A practical guide to the construction and use of lac fusions in Escherichia coli. Methods Enzymol. 326:11-35.
23. Haruyama, K., T. Nakai, I. Miyahara, K. Hirotsu, H. Mizuguchi, H. Hayashi, and H. Kagamiyama. 2001. Structures of Escherichia coli histidinolphosphateaminotransferase and its complexes with histidinol-phosphate and N-(5′-phosphopyridoxyl)-L-glutamate: double substrate recognition of the enzyme. Biochemistry 40:4633-4644.
24. Hersh, B. M., F. T. Farooq, D. N. Barstad, D. Blankenhorn, and J. L. Slonczewski. 1996. A glutamate-dependent acid resistance gene in Escherichia coli. J. Bacteriol. 178:3978-3981.
25. Hogg, R. W., C. Voelker, and I. Von Carlowitz. 1991. Nucleotide sequence and analysis of the mgl operon of Escherichia coli K12. Mol. Gen. Genet. 229:453-459.
26. + ions. J. Biol. Chem. 266:21753-21759.
27. Katayama, A., A. Tsujii, A. Wada, T. Nishino, and A. Ishihama. 2002. Systematic search for zinc-binding proteins in Escherichia coli. Eur. J. Biochem. 269:2403-2413.
28. Kessler, D., and J. Knappe. 1996. Anaerobic dissimilation of pyruvate, p. 199-204. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
29. Kihara, M., and R. M. Macnab. 1981. Cytoplasmic pH mediates pH taxis and weak-acid repellent taxis of bacteria. J. Bacteriol. 145:1209-1221.
30. Kirkpatrick, C., L. M. Maurer, N. E. Oyelakin, Y. N. Yoncheva, R. Maurer, and J. L. Slonczewski. 2001. Acetate and formate stress: opposite responses in the proteome of Escherichia coli. J. Bacteriol. 183:6466-6477.
31. Kolmar, H., P. R. H. Waller, and R. T. Sauer. 1996. The DegP and DegQ periplasmic endoproteases of Escherichia coli: specificity for cleavage sites and substrate conformation. J. Bacteriol. 178:5925-5929.
32. Lambert, L. A., K. Abshire, D. Blankenhorn, and J. L. Slonczewski. 1997. Proteins induced in Escherichia coli by benzoic acid. J. Bacteriol. 179:7595-7599.
33. Lee, I. S., J. L. Slonczewski, and J. W. Foster. 1994. A low-pH-inducible, stationary-phase acid tolerance response in Salmonella ryphimurium. J. Bacteriol. 176:1422-1426.
34. Leveque, F., M. Gazeau, M. Fromant, S. Blanquet, and P. Plateau. 1991. Control of Escherichia coli lysyl-tRNA synthetase expression by anaerobiosis. J. Bacteriol. 173:7903-7910.
35. Lin, E. C. C. 1996. Dissimilatory pathways for sugars, polyols, and carboxylates, p. 307-342. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
36. Luckey, M., and H. Nikaido. 1980. Specificity of diffusion channels produced by lambda phage receptor protein of Escherichia coli. Proc. Natl. Acad. Sci. 77:167-171.
37. Ma, Z., H. Richard, D. L. Tucker, T. Conway, and J. W. Foster. 2002. Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J. Bacteriol. 184:7001-7012.
38. Masuda, N., and G. M. Church. 2003. Regulatory network of acid resistance genes in Escherichia coli. Mol. Microbiol. 48:699-712.
39. McFall, E., and E. B. Newman. 1996. Amino acids as carbon sources, p. 358-379. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, D.C.
40. Menzel, R. 1989. A microtiter plate-based system for the semiautomated growth and assay of bacterial cells for beta-galactosidase activity. Anal. Biochem. 181:40-50.
41. Mukai, M., C. E. Mills, R. K. Poole, and S. R. Yeh. 2001. Flavohemoglobin, a globin with a peroxidase-like catalytic site. J. Biol. Chem. 276:7272-7277.
42. Muller, D. J., and A. Engel. 1999. Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. J. Mol. Biol. 285:1347-1351.
43. + in cells. Biochim. Biophys. Acta 1185:129-151.
44. Paulsen, I. T., J. Reizer, R. Z. Jin, E. C. C. Lin, and M. H. Saier, Jr. 2000. Functional genomic studies of dihydroxyacetone utilization in Escherichia coli. Microbiology 146:2343-2344.
45. Poole, R. K., M. F. Anjum, J. Membrillo-Hernández, S. O. Kim, M. N. Hughes, and V. Stewart. 1996. Nitric oxide, nitrate, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J. Bacteriol. 178:5487-5492.
46. Roe, A. J., D. McLaggan, I. Davidson, C. O'Byrne, and I. R. Booth. 1998. Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. J. Bacteriol. 180:767-772.
47. Russell, J. B., and F. Diez-Gonzalez. 1998. The effects of fermentation acids on bacterial growth. Adv. Microb. Physiol. 39:205-234.
48. Sabo, D. L., E. A. Boeker, B. Byers, H. Waron, and E. H. Fischer. 1974. Purification and physical properties of inducible Escherichia coli lysine decarboxylase. Biochemistry 13:662-670.
49. Salmon, K., S. P. Hung, K. Mekjian, P. Baldi, G. W. Hatfield, and R. P. Gunsalus. 2003. Global gene expression profiling in Escherichia coli K12: the effects of oxygen availability and FNR. J. Biol Chem. 278:29837-29855
50. Schellhorn, H. E., and V. L. Stones. 1992. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol. 174:4769-4776.
51. Silhavy, T. J., M. L. Berman, and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
52. Simons, R., W. F. Houman, and N. Kleckner, 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96.
53. Slonczewski, J. L., T. N. Gonzalez, F. M. Bartholomew, and N. J. Holt. 1987. Mu d-directed lacZ fusions regulated by low pH in Escherichia coli. J. Bacteriol. 169:3001-3006.
54. Slonczewski, J. L., and J. W. Foster. 1996. pH-regulated genes and survival at extreme pH, p. 1539-1552. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, D.C.
55. Slonczewski., J. L., and C. Kirkpatrick. 2002. Proteomic analysis of pH-dependent stress responses in Escherichia coli and Helicobacterpylori using two-dimensional gel electrophoresis. Methods Enzymol. 358:228-242.
56. Small, P., D. Blankenhorn, D. Welty, E. Zinser, and J. L. Slonczewski. 1994. Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J. Bacteriol. 176:1729-1737.
57. Smith, M. W., and F. C. Neidhardt. 1983. Proteins induced by anaerobiosis in Escherichia coli. J. Bacteriol. 154:336-343.
58. Snell, E. E. 1975. Tryptophanase: structure, catalytic activities and mechanisms of action. Adv. Enzymol. Relat. Areas Mol. Biol. 42:287-333.
59. Stancik, L. M., D. M. Stancik, B. Schimidt, D. M. Barnhart, Y. N. Yoncheva, and J. L. Slonczewski. 2002. pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J. Bacteriol. 184:4246-4258.
60. Stewart, V., R. Landick, and C. Yanofsky. 1986. Rho-dependent transcription termination in the tryptophanase operon leader region of Eschetichia coli K-12. J. Bacteriol. 166:217-223.
61. Stim, K. P., and G. N. Bennett. 1993. Nucleotide sequence of the adi gene, which encodes the biodegradative acid-induced arginine decarboxylase of Escherichia coli. J. Bacteriol. 175:1221-1234.
62. Su, H., B. F. Lang, and E. B. Newman. 1989. L-Serine degradation in Escherichia coli K-12: cloning and sequencing of the sdaA gene. J. Bacteriol. 171:5095-5102.
63. Tramonti, A., M. Visca, M. De Canio, M. Falconi, and D. De Biase. 2002. Functional characterization and regulation of gadX, a gene encoding an AraC/XylS-like transcriptional activator of the Escherichia coli glutamic acid decarboxylase system. J. Bacteriol. 184:2603-2613.
64. Tucker, D. L., N. Tucker, and T. Conway. 2002. Gene expression profiling of the pH response in Escherichia coli. J. Bacteriol. 184:6551-6558.
65. Tucker, D. L., N. Tucker, Z. Ma, J. W. Foster, R. L. Miranda, P. S. Cohen, and T. Conway. 2003. Genes of the GadX-GadW regulon in Escherichia coli. J. Bacteriol. 185:3190-3201.
66. Watson, N., D. S. Dunyak, E. L. Rosey, J. L. Slonczewski, and E. R. Olson. 1992. Identification of elements involved in transcriptional regulation of the Escherichia coli cad operon by external pH. J. Bacteriol. 174:530-540.
67. Wu, L. F., M. A. Mandrand-Berthelot, R. Waugh, C. J. Edmonds, S. E. Holt, and D. H. Boxer. 1989. Nickel deficiency gives rise to the defective hydrogenase phenotype of hydC and fnr mutants in Escherichia coli. Mol. Microbiol. 3:1709-1718.
68. Zimmerman, F. K., and K.-D. Entian (ed.) 1997. Yeast sugar metabolism. Technomic Publishing Co., Lancaster, Pa.
69. Zinser, E. R., and R. Kolter. 1999. Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase. J. Bacteriol. 181:5800-5807.