A 750 bp sensory integration region directs global control of the Escherichia coli GadE acid resistance regulator

Molecular Microbiology

Volumn 71, Issue 6, 2009, Pages 1435-1450

  Sayed, Atef K ^a   Foster, John W ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN EVGA; PROTEIN GADE; PROTEIN GADX; PROTEIN YDEO; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; ESCHERICHIA COLI; GADE GENE; GENE FUSION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; LACZ GENE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; RNA TRANSLATION; SALMONELLA; SIGNAL TRANSDUCTION; START CODON;

CULTURE MEDIA; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GLUCOSE; HYDROGEN-ION CONCENTRATION; LAC OPERON; PROMOTER REGIONS, GENETIC; RNA, BACTERIAL; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE;

ESCHERICHIA COLI; SALMONELLA;

EID: 62449255253     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06614.x     Document Type: Article

References (52)

1. Berry, E.D., Barkocy-Gallagher, G.A. Siragusa, G.R. (2004) Stationary-phase acid resistance and injury of recent bovine Escherichia coli O157 and non-O157 biotype I Escherichia coli isolates. J Food Prot 67 : 583 590.
2. Bhagwat, A.A. Bhagwat, M. (2004) Comparative analysis of transcriptional regulatory elements of glutamate-dependent acid-resistance systems of Shigella flexneri and Escherichia coli O157:H7. FEMS Microbiol Lett 234 : 139 147.
3. Bhagwat, A.A., Chan, L., Han, R., Tan, J., Kothary, M., Jean-Gilles, J. Tall, B.D. (2005) Characterization of enterohemorrhagic Escherichia coli strains based on acid resistance phenotypes. Infect Immun 73 : 4993 5003.
4. Bhagwat, A.A., Tan, J., Sharma, M., Kothary, M., Low, S., Tall, B.D. Bhagwat, M. (2006) Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl Environ Microbiol 72 : 4978 4986.
5. Bordi, C., Theraulaz, L., Mejean, V. Jourlin-Castelli, C. (2003) Anticipating an alkaline stress through the Tor phosphorelay system in Escherichia coli. Mol Microbiol 48 : 211 223.
6. Bougdour, A., Cunning, C., Baptiste, P.J., Elliott, T. Gottesman, S. (2008) Multiple pathways for regulation of sigmaS (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol Microbiol 68 : 298 313.
7. + for all three chromosomally located systems of DNA restriction and modification. J Bacteriol 156 : 471 474.
8. Cabedo, H., Macian, F., Villarroya, M., Escudero, J.C., Martinez-Vicente, M., Knecht, E. Armengod, M.E. (1999) The Escherichia coli trmE (mnmE) gene, involved in tRNA modification, codes for an evolutionarily conserved GTPase with unusual biochemical properties. EMBO J 18 : 7063 7076.
9. Caldon, C.E., Yoong, P. March, P.E. (2001) Evolution of a molecular switch: universal bacterial GTPases regulate ribosome function. Mol Microbiol 41 : 289 297.
10. Castanie-Cornet, M.P. Foster, J.W. (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., Penfound, T.A., Smith, D., Elliott, J.F. Foster, J.W. (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181 : 3525 3535.
12. Dame, R.T., Wyman, C. Goosen, N. (2000) H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res 28 : 3504 3510.
13. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
14. Elliott, T. (1992) A method for constructing single-copy lac fusions in Salmonella typhimurium and its application to the hemA-prfA operon. J Bacteriol 174 : 245 253.
15. Elseviers, D., Petrullo, L.A. Gallagher, P.J. (1984) Novel E. coli mutants deficient in biosynthesis of 5-methylaminomethyl-2-thiouridine. Nucleic Acids Res 12 : 3521 3534.
16. Foster, J.W. (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2 : 898 907.
17. Giangrossi, M., Zattoni, S., Tramonti, A., De Biase, D. Falconi, M. (2005) Antagonistic role of H-NS and GadX in the regulation of the glutamate decarboxylase-dependent acid resistance system in Escherichia coli. J Biol Chem 280 : 21498 21505.
18. Gong, S., Ma, Z. Foster, J.W. (2004) The Era-like GTPase TrmE conditionally activates gadE and glutamate-dependent acid resistance in Escherichia coli. Mol Microbiol 54 : 948 961.
19. Hersh, B.M., Farooq, F.T., Barstad, D.N., Blankenshorn, D.L. Slonczewski, J.L. (1996) A glutamate-dependent acid resistance gene in Escherichia coli. J Bacteriol 178 : 3978 3981.
20. Heuveling, J., Possling, A. Hengge, R. (2008) A role for Lon protease in the control of the acid resistance genes of Escherichia coli. Mol Microbiol 69 : 534 547.
21. Hommais, F., Krin, E., Coppee, J.Y., Lacroix, C., Yeramian, E., Danchin, A. Bertin, P. (2004) GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 150 : 61 72.
22. Jordi, B.J., Fielder, A.E., Burns, C.M., Hinton, J.C., Dover, N., Ussery, D.W. Higgins, C.F. (1997) DNA binding is not sufficient for H-NS-mediated repression of proU expression. J Biol Chem 272 : 12083 12090.
23. Kieboom, J. Abee, T. (2006) Arginine-dependent acid resistance in Salmonella enterica serovar Typhimurium. J Bacteriol 188 : 5650 5653.
24. Lin, J., Lee, I.S., Frey, J., Slonczewski, J.L. Foster, J.W. (1995) Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri and Escherichia coli. J Bacteriol 177 : 4097 4104.
25. Ma, Z., Richard, H., Tucker, D.L., Conway, T. Foster, J.W. (2002) Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J Bacteriol 184 : 7001 7012.
26. Ma, Z., Gong, S., Richard, H., Tucker, D.L., Conway, T. Foster, J.W. (2003a) GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol Microbiol 49 : 1309 1320.
27. Ma, Z., Richard, H. Foster, J.W. (2003b) pH-dependent modulation of cyclic AMP levels and GadW-dependent repression of RpoS affect synthesis of the GadX regulator and Escherichia coli acid resistance. J Bacteriol 185 : 6852 6859.
28. Ma, Z., Masuda, N. Foster, J.W. (2004) Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli. J Bacteriol 186 : 7378 7389.
29. Masuda, N. Church, G.M. (2002) Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol 184 : 6225 6234.
30. Masuda, N. Church, G.M. (2003) Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 48 : 699 712.
31. Mittenhuber, G. (2001) Comparative genomics of prokaryotic GTP-binding proteins (the Era, Obg, EngA, ThdF (TrmE), YchF and YihA families) and their relationship to eukaryotic GTP-binding proteins (the DRG, ARF, RAB, RAN, RAS and RHO families). J Mol Microbiol Biotechnol 3 : 21 35.
32. Navarre, W.W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S.J. Fang, F.C. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313 : 236 238.
33. Opdyke, J.A., Kang, J.G. Storz, G. (2004) GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186 : 6698 6705.
34. Richard, H. Foster, J.W. (2004) Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol 186 : 6032 6041.
35. Richard, H. Foster, J.W. (2007) Sodium regulates Escherichia coli acid resistance, and influences GadX- and GadW-dependent activation of gadE. Microbiology 153 : 3154 3161.
36. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
37. Sayed, A.K., Odom, C. Foster, J.W. (2007) The Escherichia coli AraC-family regulators GadX and GadW activate gadE, the central activator of glutamate-dependent acid resistance. Microbiology 153 : 2584 2592.
38. Scrima, A., Vetter, I.R., Armengod, M.E. Wittinghofer, A. (2004) The structure of the TrmE GTP-binding protein and its implications for tRNA modification. EMBO J 24 : 23 33.
39. Simons, R.W., Houman, F. Kleckner, N. (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53 : 85 96.
40. Small, P., Blankenhorn, D., Welty, D., Zinser, E. Slonczewski, J.L. (1994) Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J Bacteriol 176 : 1729 1737.
41. Studemann, A., Noirclerc-Savoye, M., Klauck, E., Becker, G., Schneider, D. Hengge, R. (2003) Sequential recognition of two distinct sites in sigma(S) by the proteolytic targeting factor RssB and ClpX. EMBO J 22 : 4111 4120.
42. Tjaden, B., Saxena, R.M., Stolyar, S., Haynor, D.R., Kolker, E. Rosenow, C. (2002) Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays. Nucleic Acids Res 30 : 3732 3738.
43. Tramonti, A., Visca, P., De Canio, M., Falconi, M. De Biase, D. (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.
44. Tramonti, A., De Canio, M., Delany, I., Scarlato, V. De Biase, D. (2006) Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli. J Bacteriol 188 : 8118 8127.
45. Tucker, D.L., Tucker, N., Ma, Z., Foster, J.W., Miranda, R.L., Cohen, P.S. Conway, T. (2003) Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol 185 : 3190 3201.
46. Tupper, A.E., Owen-Hughes, T.A., Ussery, D.W., Santos, D.S., Ferguson, D.J., Sidebotham, J.M., et al. (1994) The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J 13 : 258 268.
47. Urbonavicius, J., Stahl, G., Durand, J.M., Ben Salem, S.N., Qian, Q., Farabaugh, P.J. Bjork, G.R. (2003) Transfer RNA modifications that alter +1 frameshifting in general fail to affect -1 frameshifting. RNA 9 : 760 768.
48. Vogel, H.J. Bonner, D.M. (1956) Acetylornithase of Escherichia coli: partial purification and some properties. J Biol Chem 218 : 97 106.
49. Weber, H., Polen, T., Heuveling, J., Wendisch, V.F. Hengge, R. (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187 : 1591 1603.
50. Yamanaka, K., Hwang, J. Inouye, M. (2000) Characterization of GTPase activity of TrmE, a member of a novel GTPase superfamily, from Thermotoga maritima. J Bacteriol 182 : 7078 7082.
51. Zhou, Y. Gottesman, S. (2006) Modes of regulation of RpoS by H-NS. J Bacteriol 188 : 7022 7025.
52. Zwir, I., Shin, D., Kato, A., Nishino, K., Latifi, T., Solomon, F., et al. (2005) Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci USA 102 : 2862 2867.