Summary
The tppB locus of Salmonella typhimurium encodes the anaerobically-induced tripeptide permease. We have demonstrated that expression of tppB requires the function of the ompR and envZ gene products, originally identified as positive regulatory proteins required for the osmotic regulation of porin expression. Significantly, tppB expression is not osmotically regulated. We have also identified three additional genes whose expression depends on OmpR. Thus OmpR and EnvZ serve a more general regulatory role than has previously been supposed. This study provides the first detailed genetic analysis of the ompB locus of S. typhimurium.
Similar content being viewed by others
References
Ames GF-L (1974) Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs. J Biol Chem 249:634–644
Andrews JC, Short SA (1985) Genetic analysis of Escherichia coli oligopeptide transport mutants. J Bacteriol 161:484–492
Ardeshir F, Higgins CF, Ames GF-L (1981) Physical map of the Salmonella typhimurium histidine transport operon: correlation with the genetic map. J Bacteriol 147:401–409
Auerswald EA, Ludwig G, Schaller H (1981) Structural analysis of Tn5. Cold Spring Harbor Symp Quant Biol 45:107–113
Cairney J, Booth IR, Higgins CF (1985a) Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine. J Bacteriol 164:1218–1223
Cairney J, Booth IR, Higgins CF (1985b) Osmoregulation of gene expression in Salmonella typhimurium: proU encodes on osmotically induced betaine transport system. J Bacteriol 164:1224–1232
Castilho BA, Olfson P, Casadaban MJ (1984) Plasmid insertion mutagenesis and lac gene fusion with mini-Mu bacteriophage transposons. J Bacteriol 158:488–495
Cavard D, Pages JM, Lazdunski CJ (1982) A protease as a possible sensor of environmental conditions in E. coli outer membrane. Mol Gen Genet 188:508–512
Comeau DE, Ikenaka K, Tsung K, Inouye M (1985) Primary characterisation of the protein products of the Escherichia ompB locus: structure and regulation of synthesis of the OmpR and EnvZ proteins. J Bacteriol 164:578–584
Drummond M, Whitty P, Wooton J (1986) Sequence and domain relationships of ntrC and nifA from Klebsiella pneumoniae: homologies to other regulatory proteins. EMBO J 5:441–447
Garrett S, Taylor RK, Silhavy TJ (1983) Isolation and characterization of chain-terminating nonsense mutations in a porin regulator gene, envZ. J Bacteriol 156:62–69
Garrett S, Taylor RK, Silhavy TJ, Berman ML (1985) Isolation and characterization of ompB strains of Escherichia coli by a general method based on gene fusion. J Bacteriol 162:840–844
Gibson MM, Price M, Higgins CF (1984) Genetic characterisation and molecular cloning of the tripeptide permease (tpp) genes of Salmonella typhimurium. J Bacteriol 160:122–130
Hall MN, Silhavy TJ (1981a) The ompB locus and the regulation of the major outer membrane porin proteins of Escherichia coli K-12. J Mol Biol 146:23–43
Hall MN, Silhavy TJ (1981b) Genetic analysis of the ompB locus in Escherichia coli K-12. J Mol Biol 151:1–15
Higgins CF, Gibson MM (1986) Peptide transport in bacteria. Methods Enzymol 125:365–377
Hiles ID, Higgins CF (1986) Peptide uptake by Salmonella typhimurium: The periplasmic oligopeptide-binding protein. Eur J Biochem 158:561–567
Hughes KT, Roth JR (1984) Conditionally transposition-defective derivative of Mud1 (Amp Lac). J Bacteriol 159:130–137
Jamieson DJ, Higgins CF (1984) Anaerobic and leucine-dependent expression of a peptide transport gene in Salmonella typhimurium. J Bacteriol 160:131–136
Jamieson DJ, Higgins CF (1986) Anaerobic gene expression in Salmonella typhimurium: two genetically distinct pathways for transcriptional regulation. J Bacteriol 168:389–397
Kustu S, Burton D, Garcia E, McCarter L, McFarland N (1979) Nitrogen control in Salmonella: regulation by the glnR and glnF gene products. Proc Natl Acad Sci USA 76:4576–4580
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lederberg EM, Cohen SN (1974) Transformation of Salmonella typhimurium by plasmid deoxyribonucleic acid. J Bacteriol 119:1072–1074
Liljestrom P, Maattanen PL, Palva ET (1982) Cloning the regulatory locus ompB of Salmonella typhimurium LT-2. Mol Gen Genet 188:190–194
Lundrigran M, Earhart CF (1981) Reduction in three iron-regulated membrane proteins and protein a by the Escherichia coli K-12 perA mutation. J Bacteriol 146:804–807
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning. A laboratory manual. Cold Spring Harbor Press, Cold Spring Habor, New York
Manson MD, Blank V, Brade G, Higgins CF (1986) Peptide chemotaxis in E. coli: roles for the Tap signal transducer and the dipeptide permease. Nature 321:253–256
Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
Pugsley AP, Schwartz M, Lavina, Moreno F (1983) On the effect of ompR on colicin E2 production. FEMS Microbiol Letts 19:87–92
Rigby PWJ, Dieckmann M, Rhodes C, Berg P (1977) Labelling deoxynucleic acid to high specific activity in vitro by nick translation with DNA polymerase. J Mol Biol 113:237–251
Roth JR (1970) Genetic techniques in studies of bacterial metabolism. Methods Enzymol 17A:3–35
Sanger FS, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
van Alphen W, Lugtenberg B (1977) Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J Bacteriol 131:623–630
Vieira J, Messing J (1982) The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259–268
Wandersman C, Moreno F, Schwartz M (1980) Pleiotropic mutations rendering Escherichia coli K-12 resistant to bacteriophage TP1. J Bacteriol 143:1374–1383
Wanner BL, Sarthy A, Beckwith J (1979) Escherichia coli pleiotropic mutant that reduces amounts of several periplasmic and outer membrane proteins. J Bacteriol 140:229–239
Way JC, Davis MA, Morisato D, Roberts DE, Kleckner N (1984) New Tn10 derivatives for transposon mutagenesis and for the construction of lacZ operon fusions by transposition. Gene 32:369–379
Wurtzel ET, Chou M-Y, Inouye M (1982) Osmoregulation of gene expression. I. DNA sequence of the ompR gene of the ompB operon of Escherichia coli and characterisation of its gene product. J Biol Chem 257:13685–13691
Author information
Authors and Affiliations
Additional information
Communicated by J. Lengeler
Rights and permissions
About this article
Cite this article
Gibson, M.M., Ellis, E.M., Graeme-Cook, K.A. et al. OmpR and EnvZ are pleiotropic regulatory proteins: Positive regulation of the tripeptide permease (tppB) of Salmonella typhimurium . Mol Gen Genet 207, 120–129 (1987). https://doi.org/10.1007/BF00331499
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00331499