Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1989 Apr;171(4):1952–1959. doi: 10.1128/jb.171.4.1952-1959.1989

Evidence that the transcription activator encoded by the Pseudomonas putida nahR gene is evolutionarily related to the transcription activators encoded by the Rhizobium nodD genes.

M A Schell 1, M Sukordhaman 1
PMCID: PMC209844  PMID: 2703465

Abstract

The nahR gene of the 83-kilobase naphthalene degradation plasmid NAH7 of Pseudomonas putida encodes a 34-kilodalton polypeptide which binds to the nah and sal promoters to activate transcription of the degradation genes in response to the inducer salicylate. The DNA sequence of the nahR gene was determined, and a derived amino acid sequence of the NahR protein was obtained. A computer search for homologous proteins showed that within the first 124 amino-terminal residues, NahR has approximately 35% identity with the transcriptional activator proteins encoded by the nodD genes of Rhizobium species. Allowing for ultraconservative amino acid substitutions, greater than 47% overall similarity was found between NahR and NodD, while 32% similarity was found between NahR and another transcription activator, LysR of Escherichia coli. The region of greatest similarity among all three proteins contained a probable helix-turn-helix DNA-binding motif as suggested by homology with the proposed consensus sequence for Cro-like DNA-binding domains. The high level of amino acid identity between NahR and NodD, in conjunction with the observations that nahR and nodD are 45% homologous in DNA sequence, are divergently transcribed from homologous promoters near the structural genes they control, and have similar DNA-binding sites, strongly suggests that these two genes evolved from a common ancestor.

Full text

PDF
1956

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Appelbaum E. R., Thompson D. V., Idler K., Chartrain N. Rhizobium japonicum USDA 191 has two nodD genes that differ in primary structure and function. J Bacteriol. 1988 Jan;170(1):12–20. doi: 10.1128/jb.170.1.12-20.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barnsley E. A. The induction of the enzymes of naphthalene metabolism in pseudomonads by salicylate and 2-aminobenzoate. J Gen Microbiol. 1975 May;88(1):193–196. doi: 10.1099/00221287-88-1-193. [DOI] [PubMed] [Google Scholar]
  3. Chou P. Y., Fasman G. D. Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol Relat Areas Mol Biol. 1978;47:45–148. doi: 10.1002/9780470122921.ch2. [DOI] [PubMed] [Google Scholar]
  4. Dente L., Cesareni G., Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. doi: 10.1093/nar/11.6.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dodd I. B., Egan J. B. Systematic method for the detection of potential lambda Cro-like DNA-binding regions in proteins. J Mol Biol. 1987 Apr 5;194(3):557–564. doi: 10.1016/0022-2836(87)90681-4. [DOI] [PubMed] [Google Scholar]
  6. Dunn N. W., Gunsalus I. C. Transmissible plasmid coding early enzymes of naphthalene oxidation in Pseudomonas putida. J Bacteriol. 1973 Jun;114(3):974–979. doi: 10.1128/jb.114.3.974-979.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Egelhoff T. T., Fisher R. F., Jacobs T. W., Mulligan J. T., Long S. R. Nucleotide sequence of Rhizobium meliloti 1021 nodulation genes: nodD is read divergently from nodABC. DNA. 1985 Jun;4(3):241–248. doi: 10.1089/dna.1985.4.241. [DOI] [PubMed] [Google Scholar]
  8. Fisher R. F., Brierley H. L., Mulligan J. T., Long S. R. Transcription of Rhizobium meliloti nodulation genes. Identification of a nodD transcription initiation site in vitro and in vivo. J Biol Chem. 1987 May 15;262(14):6849–6855. [PubMed] [Google Scholar]
  9. Fisher R. F., Egelhoff T. T., Mulligan J. T., Long S. R. Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev. 1988 Mar;2(3):282–293. doi: 10.1101/gad.2.3.282. [DOI] [PubMed] [Google Scholar]
  10. Fisher R. F., Swanson J. A., Mulligan J. T., Long S. R. Extended Region of Nodulation Genes in Rhizobium meliloti 1021. II. Nucleotide Sequence, Transcription Start Sites and Protein Products. Genetics. 1987 Oct;117(2):191–201. doi: 10.1093/genetics/117.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frantz B., Chakrabarty A. M. Organization and nucleotide sequence determination of a gene cluster involved in 3-chlorocatechol degradation. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4460–4464. doi: 10.1073/pnas.84.13.4460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harayama S., Rekik M., Wasserfallen A., Bairoch A. Evolutionary relationships between catabolic pathways for aromatics: conservation of gene order and nucleotide sequences of catechol oxidation genes of pWW0 and NAH7 plasmids. Mol Gen Genet. 1987 Dec;210(2):241–247. doi: 10.1007/BF00325689. [DOI] [PubMed] [Google Scholar]
  13. Henikoff S., Haughn G. W., Calvo J. M., Wallace J. C. A large family of bacterial activator proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6602–6606. doi: 10.1073/pnas.85.18.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hong G. F., Burn J. E., Johnston A. W. Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Nucleic Acids Res. 1987 Dec 10;15(23):9677–9690. doi: 10.1093/nar/15.23.9677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Horvath B., Bachem C. W., Schell J., Kondorosi A. Host-specific regulation of nodulation genes in Rhizobium is mediated by a plant-signal, interacting with the nodD gene product. EMBO J. 1987 Apr;6(4):841–848. doi: 10.1002/j.1460-2075.1987.tb04829.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  17. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  18. Mead D. A., Skorupa E. S., Kemper B. Single stranded DNA SP6 promoter plasmids for engineering mutant RNAs and proteins: synthesis of a 'stretched' preproparathyroid hormone. Nucleic Acids Res. 1985 Feb 25;13(4):1103–1118. doi: 10.1093/nar/13.4.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mulligan J. T., Long S. R. Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6609–6613. doi: 10.1073/pnas.82.19.6609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nakai C., Kagamiyama H., Nozaki M., Nakazawa T., Inouye S., Ebina Y., Nakazawa A. Complete nucleotide sequence of the metapyrocatechase gene on the TOI plasmid of Pseudomonas putida mt-2. J Biol Chem. 1983 Mar 10;258(5):2923–2928. [PubMed] [Google Scholar]
  21. Pabo C. O., Sauer R. T. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. doi: 10.1146/annurev.bi.53.070184.001453. [DOI] [PubMed] [Google Scholar]
  22. Rostas K., Kondorosi E., Horvath B., Simoncsits A., Kondorosi A. Conservation of extended promoter regions of nodulation genes in Rhizobium. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1757–1761. doi: 10.1073/pnas.83.6.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schell M. A. Cloning and expression in Escherichia coli of the naphthalene degradation genes from plasmid NAH7. J Bacteriol. 1983 Feb;153(2):822–829. doi: 10.1128/jb.153.2.822-829.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schell M. A. Homology between nucleotide sequences of promoter regions of nah and sal operons of NAH7 plasmid of Pseudomonas putida. Proc Natl Acad Sci U S A. 1986 Jan;83(2):369–373. doi: 10.1073/pnas.83.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schell M. A., Poser E. F. Demonstration, characterization, and mutational analysis of NahR protein binding to nah and sal promoters. J Bacteriol. 1989 Feb;171(2):837–846. doi: 10.1128/jb.171.2.837-846.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schell M. A. Transcriptional control of the nah and sal hydrocarbon-degradation operons by the nahR gene product. Gene. 1985;36(3):301–309. doi: 10.1016/0378-1119(85)90185-4. [DOI] [PubMed] [Google Scholar]
  28. Schell M. A., Wender P. E. Identification of the nahR gene product and nucleotide sequences required for its activation of the sal operon. J Bacteriol. 1986 Apr;166(1):9–14. doi: 10.1128/jb.166.1.9-14.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shearman C. A., Rossen L., Johnston A. W., Downie J. A. The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl-carrier protein and is regulated by nodD plus a factor in pea root exudate. EMBO J. 1986 Apr;5(4):647–652. doi: 10.1002/j.1460-2075.1986.tb04262.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stragier P., Patte J. C. Regulation of diaminopimelate decarboxylase synthesis in Escherichia coli. III. Nucleotide sequence and regulation of the lysR gene. J Mol Biol. 1983 Aug 5;168(2):333–350. doi: 10.1016/s0022-2836(83)80022-9. [DOI] [PubMed] [Google Scholar]
  31. Stragier P., Richaud F., Borne F., Patte J. C. Regulation of diaminopimelate decarboxylase synthesis in Escherichia coli. I. Identification of a lysR gene encoding an activator of the lysA gene. J Mol Biol. 1983 Aug 5;168(2):307–320. doi: 10.1016/s0022-2836(83)80020-5. [DOI] [PubMed] [Google Scholar]
  32. Streber W. R., Timmis K. N., Zenk M. H. Analysis, cloning, and high-level expression of 2,4-dichlorophenoxyacetate monooxygenase gene tfdA of Alcaligenes eutrophus JMP134. J Bacteriol. 1987 Jul;169(7):2950–2955. doi: 10.1128/jb.169.7.2950-2955.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  34. Yen K. M., Gunsalus I. C. Plasmid gene organization: naphthalene/salicylate oxidation. Proc Natl Acad Sci U S A. 1982 Feb;79(3):874–878. doi: 10.1073/pnas.79.3.874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yen K. M., Gunsalus I. C. Regulation of naphthalene catabolic genes of plasmid NAH7. J Bacteriol. 1985 Jun;162(3):1008–1013. doi: 10.1128/jb.162.3.1008-1013.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. You I. S., Ghosal D., Gunsalus I. C. Nucleotide sequence of plasmid NAH7 gene nahR and DNA binding of the nahR product. J Bacteriol. 1988 Dec;170(12):5409–5415. doi: 10.1128/jb.170.12.5409-5415.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES