1887

Abstract

Aromatic amino acid decarboxylases (AADCs) are found in various organisms and play distinct physiological roles. AADCs from higher eukaryotes have been well studied because they are involved in the synthesis of biologically important molecules such as neurotransmitters and alkaloids. In contrast, bacterial AADCs have received less attention because of their simplicity in physiology and in target substrate (tyrosine). In the present study, we found that KT2440 possesses an AADC homologue (PP_2552) that is more closely related to eukaryotic enzymes than to bacterial enzymes, and determined the genetic and enzymic characteristics of the homologue. The purified enzyme converted 3,4-dihydroxyphenyl--alanine (DOPA) to dopamine with and values of 0.092 mM and 1.8 s, respectively. The enzyme was essentially inactive towards other aromatic amino acids such as 5-hydroxy--tryptophan, -phenylalanine, -tryptophan and -tyrosine. The observed strict substrate specificity is distinct from that of any AADC characterized so far. The proposed name of this enzyme is DOPA decarboxylase (DDC). Expression of the gene was induced by DOPA, as revealed by quantitative RT-PCR analysis. DDC is encoded in a cluster together with a LysR-type transcriptional regulator and a major facilitator superfamily transporter. This genetic organization is conserved among all sequenced strains that inhabit the rhizosphere environment, where DOPA acts as a strong allelochemical. These findings suggest the possible involvement of this enzyme in detoxification of the allelochemical in the rhizosphere, and the potential occurrence of a horizontal gene transfer event between the pseudomonad and its host organism.

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2012-12-01
2020-01-21
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References

  1. Armstrong S. K., Brickman T. J., Suhadolc R. J.. ( 2012;). Involvement of multiple distinct Bordetella receptor proteins in the utilization of iron liberated from transferrin by host catecholamine stress hormones. Mol Microbiol84:446–462 [CrossRef][PubMed]
    [Google Scholar]
  2. Beauchamp C. J., Kloepper J. W.. ( 2003;). Spatial and temporal distribution of a bioluminescent-marked Pseudomonas putida on soybean root. Luminescence18:346–351 [CrossRef][PubMed]
    [Google Scholar]
  3. Bertoldi M., Borri Voltattorni C.. ( 2003;). Reaction and substrate specificity of recombinant pig kidney Dopa decarboxylase under aerobic and anaerobic conditions. Biochim Biophys Acta1647:42–47 [CrossRef][PubMed]
    [Google Scholar]
  4. Bertoldi M., Cellini B., Montioli R., Borri Voltattorni C.. ( 2008;). Insights into the mechanism of oxidative deamination catalyzed by DOPA decarboxylase. Biochemistry47:7187–7195 [CrossRef][PubMed]
    [Google Scholar]
  5. Borri Voltattorni C., Minelli A., Vecchini P., Fiori A., Turano C.. ( 1979;). Purification and characterization of 3,4-dihydroxyphenylalanine decarboxyase from pig kidney. Eur J Biochem93:181–188 [CrossRef][PubMed]
    [Google Scholar]
  6. Burkhard P., Dominici P., Borri-Voltattorni C., Jansonius J. N., Malashkevich V. N.. ( 2001;). Structural insight into Parkinson’s disease treatment from drug-inhibited DOPA decarboxylase. Nat Struct Biol8:963–967 [CrossRef][PubMed]
    [Google Scholar]
  7. Christenson J. G., Dairman W., Udenfriend S.. ( 1970;). Preparation and properties of a homogeneous aromatic l-amino acid decarboxylase from hog kidney. Arch Biochem Biophys141:356–367 [CrossRef][PubMed]
    [Google Scholar]
  8. Connil N., Le Breton Y., Dousset X., Auffray Y., Rincé A., Prévost H.. ( 2002;). Identification of the Enterococcus faecalis tyrosine decarboxylase operon involved in tyramine production. Appl Environ Microbiol68:3537–3544 [CrossRef][PubMed]
    [Google Scholar]
  9. de Weger L. A., van Arendonk J. J., Recourt K., van der Hofstad G. A., Weisbeek P. J., Lugtenberg B.. ( 1988;). Siderophore-mediated uptake of Fe3+ by the plant growth-stimulating Pseudomonas putida strain WCS358 and by other rhizosphere microorganisms. J Bacteriol170:4693–4698[PubMed]
    [Google Scholar]
  10. Dominici P., Tancini B., Barra D., Voltattorni C. B.. ( 1987;). Purification and characterization of rat-liver 3,4-dihydroxyphenylalanine decarboxylase. Eur J Biochem169:209–213 [CrossRef][PubMed]
    [Google Scholar]
  11. Facchini P. J., De Luca V.. ( 1994;). Differential and tissue-specific expression of a gene family for tyrosine/dopa decarboxylase in opium poppy. J Biol Chem269:26684–26690[PubMed]
    [Google Scholar]
  12. Facchini P. J., De Luca V.. ( 1995;). Phloem-specific expression of tyrosine/dopa decarboxylase genes and the biosynthesis of isoquinoline alkaloids in opium poppy. Plant Cell7:1811–1821[PubMed][CrossRef]
    [Google Scholar]
  13. Facchini P. J., Huber-Allanach K. L., Tari L. W.. ( 2000;). Plant aromatic l-amino acid decarboxylases: evolution, biochemistry, regulation, and metabolic engineering applications. Phytochemistry54:121–138 [CrossRef][PubMed]
    [Google Scholar]
  14. Han Q., Ding H., Robinson H., Christensen B. M., Li J.. ( 2010;). Crystal structure and substrate specificity of Drosophila 3,4-dihydroxyphenylalanine decarboxylase. PLoS ONE5:e8826 [CrossRef][PubMed]
    [Google Scholar]
  15. Hayashi H., Mizuguchi H., Kagamiyama H.. ( 1993;). Rat liver aromatic l-amino acid decarboxylase: spectroscopic and kinetic analysis of the coenzyme and reaction intermediates. Biochemistry32:812–818 [CrossRef][PubMed]
    [Google Scholar]
  16. Iyer L. M., Aravind L., Coon S. L., Klein D. C., Koonin E. V.. ( 2004;). Evolution of cell–cell signaling in animals: did late horizontal gene transfer from bacteria have a role?. Trends Genet20:292–299 [CrossRef][PubMed]
    [Google Scholar]
  17. Jebai F., Hanoun N., Hamon M., Thibault J., Peltre G., Gros F., Krieger M.. ( 1997;). Expression, purification, and characterization of rat aromatic l-amino acid decarboxylase in Escherichia coli . Protein Expr Purif11:185–194 [CrossRef][PubMed]
    [Google Scholar]
  18. Kaminaga Y., Schnepp J., Peel G., Kish C. M., Ben-Nissan G., Weiss D., Orlova I., Lavie O., Rhodes D.. & other authors ( 2006;). Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J Biol Chem281:23357–23366 [CrossRef][PubMed]
    [Google Scholar]
  19. Kang I., Oh H. M., Vergin K. L., Giovannoni S. J., Cho J. C.. ( 2010;). Genome sequence of the marine alphaproteobacterium HTCC2150, assigned to the Roseobacter clade. J Bacteriol192:6315–6316 [CrossRef][PubMed]
    [Google Scholar]
  20. Kawalleck P., Keller H., Hahlbrock K., Scheel D., Somssich I. E.. ( 1993;). A pathogen-responsive gene of parsley encodes tyrosine decarboxylase. J Biol Chem268:2189–2194[PubMed]
    [Google Scholar]
  21. Kezmarsky N. D., Xu H., Graham D. E., White R. H.. ( 2005;). Identification and characterization of a l-tyrosine decarboxylase in Methanocaldococcus jannaschii . Biochim Biophys Acta1722:175–182 [CrossRef][PubMed]
    [Google Scholar]
  22. Koonin E. V., Makarova K. S., Aravind L.. ( 2001;). Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol55:709–742 [CrossRef][PubMed]
    [Google Scholar]
  23. López-Meyer M., Nessler C. L.. ( 1997;). Tryptophan decarboxylase is encoded by two autonomously regulated genes in Camptotheca acuminata which are differentially expressed during development and stress. Plant J11:1167–1175 [CrossRef][PubMed]
    [Google Scholar]
  24. Matilla M. A., Pizarro-Tobias P., Roca A., Fernández M., Duque E., Molina L., Wu X., van der Lelie D., Gómez M. J.. & other authors ( 2011;). Complete genome of the plant growth-promoting rhizobacterium Pseudomonas putida BIRD-1. J Bacteriol193:1290 [CrossRef][PubMed]
    [Google Scholar]
  25. Molina M. A., Ramos J. L., Espinosa-Urgel M.. ( 2006;). A two-partner secretion system is involved in seed and root colonization and iron uptake by Pseudomonas putida KT2440. Environ Microbiol8:639–647 [CrossRef][PubMed]
    [Google Scholar]
  26. Moreno-Arribas V., Lonvaud-Funel A.. ( 2001;). Purification and characterization of tyrosine decarboxylase of Lactobacillus brevis IOEB 9809 isolated from wine. FEMS Microbiol Lett195:103–107 [CrossRef][PubMed]
    [Google Scholar]
  27. Morgan B. A., Johnson W. A., Hirsh J.. ( 1986;). Regulated splicing produces different forms of dopa decarboxylase in the central nervous system and hypoderm of Drosophila melanogaster . EMBO J5:3335–3342[PubMed]
    [Google Scholar]
  28. Nakagawa A., Minami H., Kim J. S., Koyanagi T., Katayama T., Sato F., Kumagai H.. ( 2011;). A bacterial platform for fermentative production of plant alkaloids. Nat Commun2:326 [CrossRef][PubMed]
    [Google Scholar]
  29. Nelson K. E., Weinel C., Paulsen I. T., Dodson R. J., Hilbert H., Martins dos Santos V. A., Fouts D. E., Gill S. R., Pop M.. & other authors ( 2002;). Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol4:799–808 [CrossRef][PubMed]
    [Google Scholar]
  30. Nishihara E., Parvez M. M., Araya H., Fujii Y.. ( 2004;). Germination growth response of different plant species to the allelochemical l-3,4-dihydroxyphenylalanine (l-DOPA). Plant Growth Regul42:181–189 [CrossRef]
    [Google Scholar]
  31. Noé W., Mollenschott C., Berlin J.. ( 1984;). Tryptophan decarboxylase from Catharanthus roseus cell suspension cultures: purification, molecular and kinetic data of homogenous protein. Plant Mol Biol3:271–288 [CrossRef]
    [Google Scholar]
  32. Parkhill J., Wren B. W., Thomson N. R., Titball R. W., Holden M. T., Prentice M. B., Sebaihia M., James K. D., Churcher C.. & other authors ( 2001;). Genome sequence of Yersinia pestis, the causative agent of plague. Nature413:523–527 [CrossRef][PubMed]
    [Google Scholar]
  33. Samanani N., Facchini P. J.. ( 2002;). Purification and characterization of norcoclaurine synthase. The first committed enzyme in benzylisoquinoline alkaloid biosynthesis in plants. J Biol Chem277:33878–33883 [CrossRef][PubMed]
    [Google Scholar]
  34. Sandrini S. M., Shergill R., Woodward J., Muralikuttan R., Haigh R. D., Lyte M., Freestone P. P.. ( 2010;). Elucidation of the mechanism by which catecholamine stress hormones liberate iron from the innate immune defense proteins transferrin and lactoferrin. J Bacteriol192:587–594 [CrossRef][PubMed]
    [Google Scholar]
  35. Thompson J. D., Higgins D. G., Gibson T. J.. ( 1994;). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res22:4673–4680 [CrossRef][PubMed]
    [Google Scholar]
  36. Vodovar N., Vallenet D., Cruveiller S., Rouy Z., Barbe V., Acosta C., Cattolico L., Jubin C., Lajus A.. & other authors ( 2006;). Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila . Nat Biotechnol24:673–679 [CrossRef][PubMed]
    [Google Scholar]
  37. Ward N. L., Challacombe J. F., Janssen P. H., Henrissat B., Coutinho P. M., Wu M., Xie G., Haft D. H., Sait M.. & other authors ( 2009;). Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol75:2046–2056 [CrossRef][PubMed]
    [Google Scholar]
  38. Yoshida E., Hidaka M., Fushinobu S., Koyanagi T., Minami H., Tamaki H., Kitaoka M., Katayama T., Kumagai H.. ( 2010;). Role of a PA14 domain in determining substrate specificity of a glycoside hydrolase family 3 β-glucosidase from Kluyveromyces marxianus . Biochem J431:39–49 [CrossRef][PubMed]
    [Google Scholar]
  39. Yoshida E., Sakurama H., Kiyohara M., Nakajima M., Kitaoka M., Ashida H., Hirose J., Katayama T., Yamamoto K., Kumagai H.. ( 2012;). Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology22:361–368 [CrossRef][PubMed]
    [Google Scholar]
  40. Yu H., Tang H., Wang L., Yao Y., Wu G., Xu P.. ( 2011;). Complete genome sequence of the nicotine-degrading Pseudomonas putida strain S16. J Bacteriol193:5541–5542 [CrossRef][PubMed]
    [Google Scholar]
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