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. 1997 Mar;179(5):1828–1831. doi: 10.1128/jb.179.5.1828-1831.1997

Identification of the lrp gene in Bradyrhizobium japonicum and its role in regulation of delta-aminolevulinic acid uptake.

N D King 1, M R O'Brian 1
PMCID: PMC178902  PMID: 9045849

Abstract

The heme precursor delta-aminolevulinic acid (ALA) is taken up by the dipeptide permease (Dpp) system in Escherichia coli. In this study, we identified a Bradyrhizobium japonicum genomic library clone that complemented both ALA and dipeptide uptake activities in E. coli dpp mutants. The complementing B. japonicum DNA encoded a product with 58% identity to the E. coli global transcriptional regulator Lrp (leucine-responsive regulatory protein), implying the presence of Dpp-independent ALA uptake activity in those cells. Data support the conclusion that the Lrp homolog induced the oligopeptide permease system in the complemented cells by interfering with the repressor activity of the endogenous Lrp, thus conferring oligopeptide and ALA uptake activities. ALA uptake by B. japonicum was effectively inhibited by a tripeptide and, to a lesser extent, by a dipeptide, and a mutant strain that expressed the lrp homolog from a constitutive promoter was deficient in ALA uptake activity. The data show that Lrp negatively affects ALA uptake in E. coli and B. japonicum. Furthermore, the product of the isolated B. japonicum gene is both a functional and structural homolog of E. coli Lrp, and thus the regulator is not restricted to enteric bacteria.

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Selected References

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  1. Abouhamad W. N., Manson M. D. The dipeptide permease of Escherichia coli closely resembles other bacterial transport systems and shows growth-phase-dependent expression. Mol Microbiol. 1994 Dec;14(5):1077–1092. doi: 10.1111/j.1365-2958.1994.tb01340.x. [DOI] [PubMed] [Google Scholar]
  2. Abouhamad W. N., Manson M., Gibson M. M., Higgins C. F. Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol Microbiol. 1991 May;5(5):1035–1047. doi: 10.1111/j.1365-2958.1991.tb01876.x. [DOI] [PubMed] [Google Scholar]
  3. Andrews J. C., Blevins T. C., Short S. A. Regulation of peptide transport in Escherichia coli: induction of the trp-linked operon encoding the oligopeptide permease. J Bacteriol. 1986 Feb;165(2):428–433. doi: 10.1128/jb.165.2.428-433.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Andrews J. C., Short S. A. Genetic analysis of Escherichia coli oligopeptide transport mutants. J Bacteriol. 1985 Feb;161(2):484–492. doi: 10.1128/jb.161.2.484-492.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Calvo J. M., Matthews R. G. The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol Rev. 1994 Sep;58(3):466–490. doi: 10.1128/mr.58.3.466-490.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chauhan S., O'Brian M. R. Bradyrhizobium japonicum delta-aminolevulinic acid dehydratase is essential for symbiosis with soybean and contains a novel metal-binding domain. J Bacteriol. 1993 Nov;175(22):7222–7227. doi: 10.1128/jb.175.22.7222-7227.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Elliott T. Transport of 5-aminolevulinic acid by the dipeptide permease in Salmonella typhimurium. J Bacteriol. 1993 Jan;175(2):325–331. doi: 10.1128/jb.175.2.325-331.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Frustaci J. M., O'Brian M. R. Characterization of a Bradyrhizobium japonicum ferrochelatase mutant and isolation of the hemH gene. J Bacteriol. 1992 Jul;174(13):4223–4229. doi: 10.1128/jb.174.13.4223-4229.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kuykendall L. D., Elkan G. H. Rhizobium japonicum derivatives differing in nitrogen-fixing efficiency and carbohydrate utilization. Appl Environ Microbiol. 1976 Oct;32(4):511–519. doi: 10.1128/aem.32.4.511-519.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leong S. A., Ditta G. S., Helinski D. R. Heme biosynthesis in Rhizobium. Identification of a cloned gene coding for delta-aminolevulinic acid synthetase from Rhizobium meliloti. J Biol Chem. 1982 Aug 10;257(15):8724–8730. [PubMed] [Google Scholar]
  11. McGinnis S. D., O'Brian M. R. The Rhizobial hemA Gene Is Required for Symbiosis in Species with Deficient [delta]-Aminolevulinic Acid Uptake Activity. Plant Physiol. 1995 Aug;108(4):1547–1552. doi: 10.1104/pp.108.4.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Newman E. B., D'Ari R., Lin R. T. The leucine-Lrp regulon in E. coli: a global response in search of a raison d'être. Cell. 1992 Feb 21;68(4):617–619. doi: 10.1016/0092-8674(92)90135-y. [DOI] [PubMed] [Google Scholar]
  13. O'Brian M. R. Heme synthesis in the rhizobium-legume symbiosis: a palette for bacterial and eukaryotic pigments. J Bacteriol. 1996 May;178(9):2471–2478. doi: 10.1128/jb.178.9.2471-2478.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Olson E. R., Dunyak D. S., Jurss L. M., Poorman R. A. Identification and characterization of dppA, an Escherichia coli gene encoding a periplasmic dipeptide transport protein. J Bacteriol. 1991 Jan;173(1):234–244. doi: 10.1128/jb.173.1.234-244.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Platko J. V., Willins D. A., Calvo J. M. The ilvIH operon of Escherichia coli is positively regulated. J Bacteriol. 1990 Aug;172(8):4563–4570. doi: 10.1128/jb.172.8.4563-4570.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sangwan I., O'brian M. R. Evidence for an inter-organismic heme biosynthetic pathway in symbiotic soybean root nodules. Science. 1991 Mar 8;251(4998):1220–1222. doi: 10.1126/science.251.4998.1220. [DOI] [PubMed] [Google Scholar]
  17. Verkamp E., Backman V. M., Björnsson J. M., Söll D., Eggertsson G. The periplasmic dipeptide permease system transports 5-aminolevulinic acid in Escherichia coli. J Bacteriol. 1993 Mar;175(5):1452–1456. doi: 10.1128/jb.175.5.1452-1456.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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