Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential

Journal of Bacteriology

Volumn 186, Issue 18, 2004, Pages 6032-6041

  Richard, Hope ^a   Foster, John W ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; ARGININE; GLUTAMIC ACID;

ARTICLE; BACTERIAL SURVIVAL; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DECARBOXYLATION; ESCHERICHIA COLI; MEMBRANE POTENTIAL; NONHUMAN; PH; PRIORITY JOURNAL; STOMACH ACID;

ACIDS; ADAPTATION, PHYSIOLOGICAL; AGMATINE; ARGININE; BIOLOGICAL TRANSPORT; CARBOXY-LYASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLUTAMIC ACID; HYDROGEN-ION CONCENTRATION; MEMBRANE POTENTIALS; PROTON-TRANSLOCATING ATPASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 4444226939     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.18.6032-6041.2004     Document Type: Article

References (61)

1. - channels. Nature 427:803-807.
2. Anantharam, V., M. J. Allison, and P. C. Maloney. 1989. Oxalate:formate exchange. The basis for energy coupling in Oxalobacter. J. Biol. Chem. 264:7244-7250.
3. Applebaum, D., D. L. Sabo, E. H. Fischer, and D. R. Morris. 1975. Biodegradative ornithine decarboxylase of Escherichia coli. Purification, properties, and pyridoxal 5′-phosphate binding site. Biochemistry 14:3675-3681.
4. Atkinson, W. H., and H. H. Winkler. 1981. A centrifugal filtration method for the study of transport of nicotinamide adenine and pyruvate by Rickettsia prowazekii, p. 411-420. In W. Burgerdorfer and R. L. Anacker (ed.), Rickettsiae and rickettsial disease. Academic Press, Inc., New York, N.Y.
5. Boeker, E. A., and E. E. Snell. 1972. Amino acid decarboxylases. Enzymes 6:217-250.
6. Booth, I. R. 1985. Regulation of cytoplasmic pH in bacteria. Microbiol. Rev. 49:359-378.
7. Booth, I. R. 1999. The regulation of intracellular pH in bacteria, p. 19-27. In R. Poole (ed.), Bacterial responses to pH. John Wiley & Sons, Ltd., Chichester, England.
8. Booth, I. R., W. J. Mitchell, and W. A. Hamilton. 1979. Quantitative analysis of proton-linked transport systems. The lactose permease of Escherichia coli. Biochem. J. 182:687-696.
9. Brey, R. N., B. P. Rosen, and E. N. Sorensen. 1980. Cation/proton antiport systems in Escherichia coli. Properties of the potassium/proton antiporter. J. Biol. Chem. 255:39-44.
10. 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.
11. 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.
12. De Biase, D., A. Tramonti, F. Bossa, and P. Visca. 1999. The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol. Microbiol. 32:1198-1211.
13. Foster, J. W., and H. K. Hall. 1991. Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J. Bacteriol. 173:5129-5135.
14. Foster, J. W., and M. Moreno. 1999. Inducible acid tolerance mechanisms in enteric bacteria. Novartis Found. Symp. 221:55-69.
15. Gong, S., H. Richard, and J. W. Foster. 2003. YjdE (AdiC) is the arginine: agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli. J. Bacteriol. 185:4402-4409.
16. Goulbourne, E., Jr., M. Matin, E. Zychlinsky, and A. Matin. 1986. Mechanism of ApH maintenance in active and inactive cells of an obligately acidophilic bacterium. J. Bacteriol. 166:59-65.
17. Gould, J. M., and W. A. Cramer. 1977. Relationship between oxygen-induced proton efflux and membrane energization in cells of Escherichia coli. J. Biol. Chem. 252:5875-5882.
18. Hakansson, K., M. Carlsson, L. A. Svensson, and A. Liljas. 1992. Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes. J. Mol. Biol. 227:1192-1204.
19. Hersh, B. M., F. T. Farooq, D. N. Barstad, D. L. Blankenshorn, and J. L. Slonczewski. 1996. A glutamate-dependent acid resistance gene in Escherichia coli. J. Bacteriol. 178:3978-3981.
20. Hsung, J. C., and A. Haug. 1977. Membrane potential of Thermoplasma acidophila. FEBS Lett. 73:47-50.
21. Iyer, R., T. M. Iverson, A. Accardi, and C. Miller. 2002. A biological role for prokaryotic ClC chloride channels. Nature 419:715-718.
22. Iyer, R., C. Williams, and C. Miller. 2003. Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J. Bacteriol. 185:6556-6561.
23. + on the proton motive force of respiring Escherichia coli at alkaline pH. J. Bacteriol. 163:423-429.
24. Kashket, E. R. 1985. The proton motive force in bacteria: a critical assessment of methods. Annu. Rev. Microbiol. 39:219-242.
25. Khan, S., and R. Macnab. 1980. Proton chemical potential, proton electrical potential and bacterial motility. J. Mol. Biol. 138:599-614.
26. Kobayashi, H. 1985. A proton-translocating ATPase regulates pH of the bacterial cytoplasm. J. Biol. Chem. 260:72-76.
27. Kroll, R. G., and I. R. Booth. 1983. The relationship between intracellular pH, the pH gradient and potassium transport in Escherichia coli. J. Biochem. 216:706-719.
28. Krulwich, T. A. 1986. Bioenergetics of alkalophilic bacteria. J. Membr. Biol. 89:113-125.
29. Kumar, S., N. S. Punekar, V. SatyaNarayan, and K. V. Venkatesh. 2000. Metabolic fate of glutamate and evaluation of flux through the 4-aminobutyrate (GABA) shunt in Aspergillus niger. Biotechnol. Bioeng. 67:575-584.
30. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
31. Lin, J., I. S. Lee, J. Frey, J. L. Slonczewski, and J. W. Foster. 1995. Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J. Bacteriol. 177:4097-4104.
32. Lin, J., M. P. Smith, K. C. Chapin, H. S. Balk, G. N. Bennett, and J. W. Foster. 1996. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl. Environ. Microbiol. 62:3094-3100.
33. Malashkevich, V. N., D. De Blase, Z. Markovic-Housley, M. P. Schlunegger, F. Bossa, and J. N. Jansonius. 1998. Crystallization and preliminary X-ray analysis of the beta-isoform of glutamate decarboxylase from Escherichia coli. Acta Crystallogr. D 54:1020-1022.
34. + entry and ATP formation in Escherichia coli. Biochem. Biophys. Res. Commun. 83:1496-1501.
35. Matin, A., B. Wilson, E. Zychlinsky, and M. Matin. 1982. Proton motive force and the physiological basis of delta pH maintenance in Thiobacillus acidophilus. J. Bacteriol. 150:582-591.
36. Matin, A., E. Zychlinsky, M. Keyhan, and G. Sachs. 1996. Capacity of Helicobacter pylori to generate ionic gradients at low pH is similar to that of bacteria which grow under strongly acidic conditions. Infect. Immun. 64:1434-1436.
37. Michels, M., and E. P. Bakker. 1985. Generation of a large, protonophore-sensitive proton motive force and pH difference in the acidophilic bacteria Thermoplasma acidophilum and Bacillus acidocaldarius. J. Bacteriol. 161:231-237.
38. Molenaar, D., J. S. Bosscher, B. ten Brink, A. J. Driessen, and W. N. Konings. 1993. Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J. Bacteriol. 175:2864-2870.
39. Mooney, C., D. J. Munster, P. F. Bagshow, and R. A. Allardyck. 1993. Helicobacter pylori acid resistance. Lancet 335:1232.
40. Olsen, E. B., J. B. Russell, and T. Henick-Kling. 1991. Electrogenic L-malate transport by Lactobacillus plantarum: a basis for energy derivation from malolactic fermentation. J. Bacteriol. 173:6199-6206.
41. Padan, E., and T. A. Krulwich. 2000. Sodium stress. ASM Press, Washington, D.C.
42. + antiporters: molecular biology, biochemistry, and physiology, vol. 2. Elsevier Science, Amsterdam, The Netherlands.
43. Park, Y. K., B. Bearson, S. H. Bang, I. S. Bang, and J. W. Foster. 1996. Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol. Microbiol. 20:605-611.
44. Poolman, B., D. Molenaar, E. J. Smid, T. Ubbink, T. Abee, P. P. Renault, and W. N. Konings. 1991. Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J. Bacteriol. 173:6030-6037.
45. Rektorschek, M., A. Buhmann, D. Weeks, D. Schwan, K. W. Bensch, S. Eskandari, D. Scott, G. Sachs, and K. Melchers. 2000. Acid resistance of Helicobacter pylori depends on the UreI membrane protein and an inner membrane proton barrier. Mol. Microbiol. 36:141-152.
46. Richard, H. T., and J. W. Foster. 2003. Acid resistance in Escherichia coli. Adv. Appl. Microbiol. 52:167-186.
47. Rottenberg, H. 1979. The measurement of membrane potential and ApH in cells, organelles, and vesicles. Methods Enzymol. 55:547-569.
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. J. Biochem. 13:662-670.
49. Salema, M., B. Poolman, J. S. Lolkema, M. C. Dias, and W. N. Konings. 1994. Uniport of monoanionic L-malate in membrane vesicles from Leuconostoc oenos. Eur. J. Biochem. 225:289-295.
50. Scott, D. R., D. Weeks, C. Hong, S. Postius, K. Melchers, and G. Sachs. 1998. The role of internal urease in acid resistance of Helicobacter pylori. Gastroenterology 114:58-70.
51. 31P nuclear magnetic resonance of methylphosphonate and phosphate. Proc. Natl. Acad. Sci. USA 78:6271-6275.
52. 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.
53. Smith, J. L. 2003. The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J. Food Prot. 66:1292-1303.
54. Stingl, K., E. M. Uhlemann, R. Schmid, K. Altendorf, and E. P. Bakker. 2002. Energetics of Helicobacter pylori and its implications for the mechanism of urease-dependent acid tolerance at pH 1. J. Bacteriol. 184:3053-3060.
55. Sukhareva, B. S., A. S. Tikhonenko, and E. L. Darii. 1994. Study of the quaternary structure of glutamate carboxylase from Escherichia coli. Mol. Biol. (Moscow) 28:1407-1411.
56. Tanabe, M., K. Nishio, Y. Iko, Y. Sambongi, A. Iwamoto-Kihara, Y. Wada, and M. Futai. 2001. Rotation of a complex of the γ subunit and c ring of Escherichia coli ATP synthase: the rotor and stator are interchangeable. J. Biol. Chem. 276:15269-15274.
57. 31P NMR in bacterial suspensions using phenyl phosphonate as a probe. Biochem. Biophys. Res. Commun. 138:1106-1109.
58. Vogel, H. J., and D. M. Bonner. 1956. Acetylornithase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218:97-106.
59. +-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287:482-485.
60. Winkler, H. H., and T. H. Wilson. 1966. The role of energy coupling in the transport of beta-galactosides by Escherichia coli. J. Biol. Chem. 241:2200-2211.
61. Zilberstein, D., V. Agmon, S. Schuldiner, and E. Padan. 1982. The sodium/proton antiporter is part of the pH homeostasis mechanism in Escherichia coli. J. Biol. Chem. 257:3687-3691.