A bacterial basic region leucine zipper histidine kinase regulating toluene degradation.

The two-component signal transduction pathways in bacteria use a histidine-aspartate phosphorelay circuit to mediate cellular changes in response to environmental stimuli. Here we describe a novel two-component todST system, which activates expression of the toluene degradation (tod) pathway in Pseudomonas putida F1. The todS gene is predicted to encode a sensory hybrid kinase with two unique properties--a basic region leucine zipper dimerization motif at the N terminus and a duplicated histidine kinase motif. Evidence from a synthetic peptide model suggests that TodS binds as a dimer to a pseudopalindromic sequence (5'-TGACTCA), which resembles the recognition sequence of the eukaryotic transcription factors Fos and Jun. These results provide additional evidence that bacteria and eukaryotes share common regulatory motifs. The todT gene product, a response regulator, was overproduced as a fusion protein in Escherichia coli, and the purified protein was found to bind specifically to a 6-bp palindromic DNA structure in the tod control region. The phosphorylated form of TodT appears to be the activator of tod structural genes. This is the first report of a two-component system that regulates aromatic metabolism in bacteria.

[1]  J. Hoch,et al.  Two-component signal transduction , 1995 .

[2]  D. Gibson,et al.  Initial Studies on the Regulation of Toluene Degradation by Pseudomonas Putida F1 , 1988 .

[3]  V. de Lorenzo,et al.  Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes. , 1993, Gene.

[4]  Y. Wang,et al.  Sequence and expression of the todGIH genes involved in the last three steps of toluene degradation by Pseudomonas putida F1. , 1994, Gene.

[5]  T. Mizuno,et al.  A novel device of bacterial signal transducers. , 1994, The EMBO journal.

[6]  J. Whitlock The aromatic hydrocarbon receptor, dioxin action, and endocrine homeostasis , 1994, Trends in Endocrinology & Metabolism.

[7]  G. Ditta,et al.  The oxygen sensor FixL of Rhizobium meliloti is a membrane protein containing four possible transmembrane segments , 1993, Journal of bacteriology.

[8]  C. Yanisch-Perron,et al.  Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. , 1985, Gene.

[9]  T. Curran,et al.  Parallel association of Fos and Jun leucine zippers juxtaposes DNA binding domains. , 1989, Science.

[10]  Y. Wang,et al.  Sequence and expression of an isocitrate dehydrogenase-encoding gene from a polycyclic aromatic hydrocarbon oxidizer, Sphingomonas yanoikuyae B1. , 1996, Gene.

[11]  V. Lorenzo,et al.  Regulatory noise in prokaryotic promoters: how bacteria learn to respond to novel environmental signals , 1996, Molecular microbiology.

[12]  David J. States,et al.  Identification of protein coding regions by database similarity search , 1993, Nature Genetics.

[13]  M. Jobling,et al.  Construction of vectors with the p15a replicon, kanamycin resistance, inducible lacZ alpha and pUC18 or pUC19 multiple cloning sites. , 1990, Nucleic acids research.

[14]  K. Volz,et al.  Structural conservation in the CheY superfamily. , 1993, Biochemistry.

[15]  B. Wanner Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria? , 1992, Journal of bacteriology.

[16]  S. Iuchi,et al.  Phosphorylation/dephosphorylation of the receiver module at the conserved aspartate residue controls transphosphorylation activity of histidine kinase in sensor protein ArcB of Escherichia coli. , 1993, The Journal of biological chemistry.

[17]  W. DeGrado,et al.  Design of DNA-binding peptides based on the leucine zipper motif. , 1990, Science.

[18]  J. S. Parkinson,et al.  Communication modules in bacterial signaling proteins. , 1992, Annual review of genetics.

[19]  R. Tjian,et al.  Leucine repeats and an adjacent DNA binding domain mediate the formation of functional cFos-cJun heterodimers. , 1989, Science.

[20]  Lawrence P. Wackett,et al.  Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. , 1983, Science.

[21]  H. Hennecke,et al.  Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[22]  P. S. Kim,et al.  Sequence-specific DNA binding by a short peptide dimer. , 1990, Science.

[23]  T. Curran,et al.  Transcription factor interactions: basics on zippers , 1991 .

[24]  A. Ninfa,et al.  Is acetyl phosphate a global signal in Escherichia coli? , 1993, Journal of bacteriology.

[25]  C. Harwood,et al.  Construction and use of a new broad-host-range lacZ transcriptional fusion vector, pHRP309, for gram- bacteria. , 1993, Gene.

[26]  D. Gibson,et al.  Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli. , 1989, The Journal of biological chemistry.

[27]  M. Simon,et al.  Protein histidine kinases and signal transduction in prokaryotes and eukaryotes. , 1994, Trends in genetics : TIG.