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. 1992 Mar;174(5):1568–1573. doi: 10.1128/jb.174.5.1568-1573.1992

arcD, the first gene of the arc operon for anaerobic arginine catabolism in Pseudomonas aeruginosa, encodes an arginine-ornithine exchanger.

H J Verhoogt 1, H Smit 1, T Abee 1, M Gamper 1, A J Driessen 1, D Haas 1, W N Konings 1
PMCID: PMC206552  PMID: 1311296

Abstract

In the absence of oxygen and nitrate, Pseudomonas aeruginosa metabolizes arginine via the arginine deiminase pathway, which allows slow growth on rich media. The conversion of arginine to ornithine, CO2, and NH3 is coupled to the production of ATP from ADP. The enzymes of the arginine deiminase pathway are organized in the arcDABC operon. The arcD gene encodes a hydrophobic polytopic membrane protein. Translocation of arginine and ornithine in membrane vesicles derived from an Escherichia coli strain harboring a recombinant plasmid carrying the arcD gene was studied. Arginine and ornithine uptake was coupled to the proton motive force with a bias toward the transmembrane electrical potential. Accumulated ornithine was readily exchangeable for external arginine or lysine. The exchange was several orders of magnitude faster than proton motive force-driven transport. The ArcD protein was reconstituted in proteoliposomes after detergent solubilization of membrane vesicles. These proteoliposomes mediate a stoichiometric exchange between arginine and ornithine. It is concluded that the ArcD protein is a transport system that catalyzes an electroneutral exchange between arginine and ornithine to allow high-efficiency energy conversion in the arginine deiminase pathway.

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Selected References

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  1. Ambudkar S. V., Maloney P. C. Bacterial anion exchange. Use of osmolytes during solubilization and reconstitution of phosphate-linked antiport from Streptococcus lactis. J Biol Chem. 1986 Aug 5;261(22):10079–10086. [PubMed] [Google Scholar]
  2. Baur H., Luethi E., Stalon V., Mercenier A., Haas D. Sequence analysis and expression of the arginine-deiminase and carbamate-kinase genes of Pseudomonas aeruginosa. Eur J Biochem. 1989 Jan 15;179(1):53–60. doi: 10.1111/j.1432-1033.1989.tb14520.x. [DOI] [PubMed] [Google Scholar]
  3. Baur H., Stalon V., Falmagne P., Luethi E., Haas D. Primary and quaternary structure of the catabolic ornithine carbamoyltransferase from Pseudomonas aeruginosa. Extensive sequence homology with the anabolic ornithine carbamoyltransferases of Escherichia coli. Eur J Biochem. 1987 Jul 1;166(1):111–117. doi: 10.1111/j.1432-1033.1987.tb13489.x. [DOI] [PubMed] [Google Scholar]
  4. Celis T. F., Rosenfeld H. J., Maas W. K. Mutant of Escherichia coli K-12 defective in the transport of basic amino acids. J Bacteriol. 1973 Nov;116(2):619–626. doi: 10.1128/jb.116.2.619-626.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cunin R., Glansdorff N., Piérard A., Stalon V. Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev. 1986 Sep;50(3):314–352. doi: 10.1128/mr.50.3.314-352.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DAVIS B. D., MINGIOLI E. S. Mutants of Escherichia coli requiring methionine or vitamin B12. J Bacteriol. 1950 Jul;60(1):17–28. doi: 10.1128/jb.60.1.17-28.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Driessen A. J., Hellingwerf K. J., Konings W. N. Mechanism of energy coupling to entry and exit of neutral and branched chain amino acids in membrane vesicles of Streptococcus cremoris. J Biol Chem. 1987 Sep 15;262(26):12438–12443. [PubMed] [Google Scholar]
  8. Driessen A. J., Kodde J., de Jong S., Konings W. N. Neutral amino acid transport by membrane vesicles of Streptococcus cremoris is subject to regulation by internal pH. J Bacteriol. 1987 Jun;169(6):2748–2754. doi: 10.1128/jb.169.6.2748-2754.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Driessen A. J., Molenaar D., Konings W. N. Kinetic mechanism and specificity of the arginine-ornithine antiporter of Lactococcus lactis. J Biol Chem. 1989 Jun 25;264(18):10361–10370. [PubMed] [Google Scholar]
  10. Driessen A. J., Poolman B., Kiewiet R., Konings W. Arginine transport in Streptococcus lactis is catalyzed by a cationic exchanger. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6093–6097. doi: 10.1073/pnas.84.17.6093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Driessen A. J., Smid E. J., Konings W. N. Transport of diamines by Enterococcus faecalis is mediated by an agmatine-putrescine antiporter. J Bacteriol. 1988 Oct;170(10):4522–4527. doi: 10.1128/jb.170.10.4522-4527.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Driessen A. J., de Vrij W., Konings W. N. Functional incorporation of beef-heart cytochrome c oxidase into membranes of Streptococcus cremoris. Eur J Biochem. 1986 Feb 3;154(3):617–624. doi: 10.1111/j.1432-1033.1986.tb09443.x. [DOI] [PubMed] [Google Scholar]
  13. Driessen A. J., van Leeuwen C., Konings W. N. Transport of basic amino acids by membrane vesicles of Lactococcus lactis. J Bacteriol. 1989 Mar;171(3):1453–1458. doi: 10.1128/jb.171.3.1453-1458.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fan C. L., Miller D. L., Rodwell V. W. Metabolism of basic amino acids in Pseudomonas putida. Transport of lysine, ornithine, and arginine. J Biol Chem. 1972 Apr 25;247(8):2283–2288. [PubMed] [Google Scholar]
  15. Galimand M., Gamper M., Zimmermann A., Haas D. Positive FNR-like control of anaerobic arginine degradation and nitrate respiration in Pseudomonas aeruginosa. J Bacteriol. 1991 Mar;173(5):1598–1606. doi: 10.1128/jb.173.5.1598-1606.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gamper M., Zimmermann A., Haas D. Anaerobic regulation of transcription initiation in the arcDABC operon of Pseudomonas aeruginosa. J Bacteriol. 1991 Aug;173(15):4742–4750. doi: 10.1128/jb.173.15.4742-4750.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kagawa Y., Kandrach A., Racker E. Partial resolution of the enzymes catalyzing oxidative phosphorylation. XXVI. Specificity of phospholipids required for energy transfer reactions. J Biol Chem. 1973 Jan 25;248(2):676–684. [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. Lüthi E., Baur H., Gamper M., Brunner F., Villeval D., Mercenier A., Haas D. The arc operon for anaerobic arginine catabolism in Pseudomonas aeruginosa contains an additional gene, arcD, encoding a membrane protein. Gene. 1990 Mar 1;87(1):37–43. doi: 10.1016/0378-1119(90)90493-b. [DOI] [PubMed] [Google Scholar]
  20. Lüthi E., Mercenier A., Haas D. The arcABC operon required for fermentative growth of Pseudomonas aeruginosa on arginine: Tn5-751-assisted cloning and localization of structural genes. J Gen Microbiol. 1986 Oct;132(10):2667–2675. doi: 10.1099/00221287-132-10-2667. [DOI] [PubMed] [Google Scholar]
  21. Mercenier A., Simon J. P., Vander Wauven C., Haas D., Stalon V. Regulation of enzyme synthesis in the arginine deiminase pathway of Pseudomonas aeruginosa. J Bacteriol. 1980 Oct;144(1):159–163. doi: 10.1128/jb.144.1.159-163.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mercenier A., Stalon V., Simon J. P., Haas D. Mapping of the arginine deiminase gene in Pseudomonas aeruginosa. J Bacteriol. 1982 Feb;149(2):787–788. doi: 10.1128/jb.149.2.787-788.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Newman M. J., Wilson T. H. Solubilization and reconstitution of the lactose transport system from Escherichia coli. J Biol Chem. 1980 Nov 25;255(22):10583–10586. [PubMed] [Google Scholar]
  24. Poolman B., Driessen A. J., Konings W. N. Regulation of arginine-ornithine exchange and the arginine deiminase pathway in Streptococcus lactis. J Bacteriol. 1987 Dec;169(12):5597–5604. doi: 10.1128/jb.169.12.5597-5604.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Poolman B. Precursor/product antiport in bacteria. Mol Microbiol. 1990 Oct;4(10):1629–1636. doi: 10.1111/j.1365-2958.1990.tb00539.x. [DOI] [PubMed] [Google Scholar]
  26. Rella M., Mercenier A., Haas D. Transposon insertion mutagenesis of Pseudomonas aeruginosa with a Tn5 derivative: application to physical mapping of the arc gene cluster. Gene. 1985;33(3):293–303. doi: 10.1016/0378-1119(85)90237-9. [DOI] [PubMed] [Google Scholar]
  27. SHOESMITH J. H., SHERRIS J. C. Studies on the mechanism of arginine-activated motility in a Pseudomonas strain. J Gen Microbiol. 1960 Feb;22:10–24. doi: 10.1099/00221287-22-1-10. [DOI] [PubMed] [Google Scholar]
  28. Short J. M., Fernandez J. M., Sorge J. A., Huse W. D. Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties. Nucleic Acids Res. 1988 Aug 11;16(15):7583–7600. doi: 10.1093/nar/16.15.7583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  30. Vander Wauven C., Piérard A., Kley-Raymann M., Haas D. Pseudomonas aeruginosa mutants affected in anaerobic growth on arginine: evidence for a four-gene cluster encoding the arginine deiminase pathway. J Bacteriol. 1984 Dec;160(3):928–934. doi: 10.1128/jb.160.3.928-934.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zimmermann A., Reimmann C., Galimand M., Haas D. Anaerobic growth and cyanide synthesis of Pseudomonas aeruginosa depend on anr, a regulatory gene homologous with fnr of Escherichia coli. Mol Microbiol. 1991 Jun;5(6):1483–1490. doi: 10.1111/j.1365-2958.1991.tb00794.x. [DOI] [PubMed] [Google Scholar]
  32. van Schie B. J., Hellingwerf K. J., van Dijken J. P., Elferink M. G., van Dijl J. M., Kuenen J. G., Konings W. N. Energy transduction by electron transfer via a pyrrolo-quinoline quinone-dependent glucose dehydrogenase in Escherichia coli, Pseudomonas aeruginosa, and Acinetobacter calcoaceticus (var. lwoffi). J Bacteriol. 1985 Aug;163(2):493–499. doi: 10.1128/jb.163.2.493-499.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

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