Previous Article | Next Article 
Journal of Bacteriology, October 2004, p. 6698-6705, Vol. 186, No. 20
0021-9193/04/$08.00+0 DOI: 10.1128/JB.186.20.6698-6705.2004
GadY, a Small-RNA Regulator of Acid Response Genes in Escherichia coli
Jason A. Opdyke,
Ju-Gyeong Kang,
,
and Gisela Storz*
Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland
Received 28 April 2004/
Accepted 9 June 2004
A previous bioinformatics-based search for small RNAs in Escherichia coli identified a novel RNA named IS183. The gene encoding this small RNA is located between and on the opposite strand of genes encoding two transcriptional regulators of the acid response, gadX (yhiX) and gadW (yhiW). Given that IS183 is encoded in the gad gene cluster and because of its role in regulating acid response genes reported here, this RNA has been renamed GadY. We show that GadY exists in three forms, a long form consisting of 105 nucleotides and two processed forms, consisting of 90 and 59 nucleotides. The expression of this small RNA is highly induced during stationary phase in a manner that is dependent on the alternative sigma factor
S. Overexpression of the three GadY RNA forms resulted in increased levels of the mRNA encoding the GadX transcriptional activator, which in turn caused increased levels of the GadA and GadB glutamate decarboxylases. A promoter mutation which abolished gadY expression resulted in a reduction in the amount of gadX mRNA during stationary phase. The gadY gene was shown to overlap the 3' end of the gadX gene, and this overlap region was found to be necessary for the GadY-dependent accumulation of gadX mRNA. We suggest that during stationary phase, GadY forms base pairs with the 3'-untranslated region of the gadX mRNA and confers increased stability, allowing for gadX mRNA accumulation and the increased expression of downstream acid resistance genes.
* Corresponding author. Mailing address: NIH, Building 18T, Room 101, 18 Library Dr., MSC 5430, Bethesda, MD 20892-5430. Phone: (301) 402-0968. Fax: (301) 402-0078. E-mail:
storz{at}helix.nih.gov.
J.A.O. and J.-G.K. contributed equally to this study.
Present address: Cardiovascular Branch, National Heart Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892.
Journal of Bacteriology, October 2004, p. 6698-6705, Vol. 186, No. 20
0021-9193/04/$08.00+0 DOI: 10.1128/JB.186.20.6698-6705.2004
This article has been cited by other articles:
-
Shavkunov, K. S., Masulis, I. S., Tutukina, M. N., Deev, A. A., Ozoline, O. N.
(2009). Gains and unexpected lessons from genome-scale promoter mapping. Nucleic Acids Res
0: gkp490v1-gkp490
[Abstract]
[Full Text]
-
Cheng, R., Miao, C., Gong, Q., Gu, Y., Lu, X., Han, F., Yu, W.
(2009). Specific gene silencing by artificial trans-encoded small noncoding RNAs in bacteria. Nucleic Acids Res
0: gkp447v1-gkp447
[Abstract]
[Full Text]
-
Wu, Y., Outten, F. W.
(2009). IscR Controls Iron-Dependent Biofilm Formation in Escherichia coli by Regulating Type I Fimbria Expression. J. Bacteriol.
191: 1248-1257
[Abstract]
[Full Text]
-
Pulvermacher, S. C., Stauffer, L. T., Stauffer, G. V.
(2009). Role of the Escherichia coli Hfq protein in GcvB regulation of oppA and dppA mRNAs. Microbiology
155: 115-123
[Abstract]
[Full Text]
-
Andre, G., Even, S., Putzer, H., Burguiere, P., Croux, C., Danchin, A., Martin-Verstraete, I., Soutourina, O.
(2008). S-box and T-box riboswitches and antisense RNA control a sulfur metabolic operon of Clostridium acetobutylicum. Nucleic Acids Res
36: 5955-5969
[Abstract]
[Full Text]
-
Shokeen, S., Patel, S., Greenfield, T. J., Brinkman, C., Weaver, K. E.
(2008). Translational Regulation by an Intramolecular Stem-Loop Is Required for Intermolecular RNA Regulation of the par Addiction Module. J. Bacteriol.
190: 6076-6083
[Abstract]
[Full Text]
-
Padalon-Brauch, G., Hershberg, R., Elgrably-Weiss, M., Baruch, K., Rosenshine, I., Margalit, H., Altuvia, S.
(2008). Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res
36: 1913-1927
[Abstract]
[Full Text]
-
Ruiz, C., McMurry, L. M., Levy, S. B.
(2008). Role of the Multidrug Resistance Regulator MarA in Global Regulation of the hdeAB Acid Resistance Operon in Escherichia coli. J. Bacteriol.
190: 1290-1297
[Abstract]
[Full Text]
-
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
[Abstract]
[Full Text]
-
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
[Abstract]
[Full Text]
-
Guisbert, E., Rhodius, V. A., Ahuja, N., Witkin, E., Gross, C. A.
(2007). Hfq Modulates the {sigma}E-Mediated Envelope Stress Response and the {sigma}32-Mediated Cytoplasmic Stress Response in Escherichia coli. J. Bacteriol.
189: 1963-1973
[Abstract]
[Full Text]
-
Barnett, T. C., Bugrysheva, J. V., Scott, J. R.
(2007). Role of mRNA Stability in Growth Phase Regulation of Gene Expression in the Group A Streptococcus. J. Bacteriol.
189: 1866-1873
[Abstract]
[Full Text]
-
Mandin, P., Repoila, F., Vergassola, M., Geissmann, T., Cossart, P.
(2007). Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res
35: 962-974
[Abstract]
[Full Text]
-
Urban, J. H., Vogel, J.
(2007). Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res
35: 1018-1037
[Abstract]
[Full Text]
-
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
[Abstract]
[Full Text]
-
Lung, B., Zemann, A., Madej, M. J., Schuelke, M., Techritz, S., Ruf, S., Bock, R., Huttenhofer, A.
(2006). Identification of small non-coding RNAs from mitochondria and chloroplasts. Nucleic Acids Res
34: 3842-3852
[Abstract]
[Full Text]
-
Kobayashi, A., Hirakawa, H., Hirata, T., Nishino, K., Yamaguchi, A.
(2006). Growth Phase-Dependent Expression of Drug Exporters in Escherichia coli and Its Contribution to Drug Tolerance.. J. Bacteriol.
188: 5693-5703
[Abstract]
[Full Text]
-
Hirakawa, H., Inazumi, Y., Senda, Y., Kobayashi, A., Hirata, T., Nishino, K., Yamaguchi, A.
(2006). N-Acetyl-D-Glucosamine Induces the Expression of Multidrug Exporter Genes, mdtEF, via Catabolite Activation in Escherichia coli.. J. Bacteriol.
188: 5851-5858
[Abstract]
[Full Text]
-
Huttenhofer, A., Vogel, J.
(2006). Experimental approaches to identify non-coding RNAs. Nucleic Acids Res
34: 635-646
[Abstract]
[Full Text]
-
GOTTESMAN, S., McCULLEN, C.A., GUILLIER, M., VANDERPOOL, C.K., MAJDALANI, N., BENHAMMOU, J., THOMPSON, K.M., FitzGERALD, P.C., SOWA, N.A., FitzGERALD, D.J.
(2006). Small RNA Regulators and the Bacterial Response to Stress. Cold Spring Harb Symp Quant Biol
71: 1-11
[Abstract]
-
Mey, A. R., Craig, S. A., Payne, S. M.
(2005). Characterization of Vibrio cholerae RyhB: the RyhB Regulon and Role of ryhB in Biofilm Formation. Infect. Immun.
73: 5706-5719
[Abstract]
[Full Text]
-
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
[Abstract]
[Full Text]
-
Davis, B. M., Quinones, M., Pratt, J., Ding, Y., Waldor, M. K.
(2005). Characterization of the Small Untranslated RNA RyhB and Its Regulon in Vibrio cholerae. J. Bacteriol.
187: 4005-4014
[Abstract]
[Full Text]
-
Antal, M., Bordeau, V., Douchin, V., Felden, B.
(2005). A Small Bacterial RNA Regulates a Putative ABC Transporter. J. Biol. Chem.
280: 7901-7908
[Abstract]
[Full Text]
-
Weber, H., Polen, T., Heuveling, J., Wendisch, V. F., Hengge, R.
(2005). Genome-Wide Analysis of the General Stress Response Network in Escherichia coli: {sigma}S-Dependent Genes, Promoters, and Sigma Factor Selectivity. J. Bacteriol.
187: 1591-1603
[Abstract]
[Full Text]
-
Kawano, M., Reynolds, A. A., Miranda-Rios, J., Storz, G.
(2005). Detection of 5'- and 3'-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res
33: 1040-1050
[Abstract]
[Full Text]
-
Altuvia, S.
(2004). Regulatory Small RNAs: the Key to Coordinating Global Regulatory Circuits. J. Bacteriol.
186: 6679-6680
[Full Text]