PQQ: Biosynthetic Studies in Methylobacterium AM1 and Hyphomicrobium X Using Specific 13C Labeling and NMR

  • David R. Houck
  • John L. Hanners
  • Clifford J. Unkefer
  • Mario A. G. van Kleef
  • Johannis A. Duine

Abstract

Using 13C labeling and NMR spectroscopy we have determined biosynthetic precursors of pyrroloquinoline quinone (PQQ) in two closely related serine-type methylotrophs, Methylobacterium AM1 and Hyphomicrobium X. Analysis of the 13C-labeling data revealed that PQQ is constructed from two amino acids: the portion containing N-6,C-7,8,9 and the two carboxylic acid groups,C-7′and 9′, is derived-intact -from glutamate. The remaining portion is derived from tyrosine; the phenol side chain provides the six carbons of the ring containing the orthoquinone, whereas internal cyclization of the amino acid backbone forms the pyrrole-2-carboxylic acid moiety. This is analogous to the cyclization of dopaquinone to form dopachrome. Dopaquinone is a product of the oxidation of tyrosine (via dopa) in reactions catalyzed by monophenol monooxygenase (EC 1.14.18.1). Starting with tyrosine and glutamate, we will discuss possible biosynthetic routes to PQQ.

Keywords

Shikimate Pathway Biosynthetic Precursor Acinetobacter Calcoaceticus Methanol Dehydrogenase Pyrroloquinoline Quinone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Anthony, C., 1982. The biochemistry of methylotrophs. Academic Press, Inc., New York 1–40.Google Scholar
  2. Bax, A., Freeman, R. and Morris, G., 1981a. Correlation of proton chemical shifts by two-dimensional fourier transform NMR. J. Mag. Reson. 42:164–168.Google Scholar
  3. Bax, A. and Freeman, R., 1981b. Investigation of complex networks of spin-spin coupling by two-dimensional NMR. J. Mag. Reson. 44: 542–561.Google Scholar
  4. Beardsmore, A.J., Aperghis, P.N.G. and Quayle, J.R., 1982. Characterization of the assimilatory and dissimilatory pathways of carbon metabolism during growth of Methylophilus methylotrophus on methanol. J. Gen Microbiol. 128:1423–1439.Google Scholar
  5. Canovas, F.G., Garcia-Carmona, F., Sanchez, J.V., Pastor, J.L.I., and Teruel, J.A.L., 1982. The role of pH in the melanin biosynthesis pathway. J. Biol. Chem. 257:8738–8744.PubMedGoogle Scholar
  6. Duine, J.A. and Frank Jzn. J., 1980. The prosthetic group of methanol dehydrogenase. Purification and some of its properties. Biochem.J. 187:221–226.PubMedGoogle Scholar
  7. Duine, J.A. and Frank Jzn. J., 1981. Quinoproteins: a novel class of dehydrogenases. Trends Biochem. Sc. 6:278–280.CrossRefGoogle Scholar
  8. Duine, J.A. Frank, Jzn. J. and Jongejan, J.A.,1986. PQQ and quinoprotein enzymes in microbiological reviews. FEMS Microbiol Rev. 32:165–178.CrossRefGoogle Scholar
  9. Duine, J.A. Frank, J.Jzn, and Verwiel, P.E.J., 1981. Structure and activity of the prosthetic group of methanol dehydrogenase. Eur. J. Biochem. 118:395–399.CrossRefGoogle Scholar
  10. Dunstan, P.M., Anthony, C. and Drabble, W.T., 1972. Microbial metabolism of C1 and C2 compounds. The involvement of glycollate in the metabolism of ethanol and of acetate by Pseudomonas AM1. Biochem. J. 128: 99–106.PubMedGoogle Scholar
  11. Dunstan, P.M., Anthony, C. and Drabble, W.T., 1972. Microbial metabolism of C1 and C2 compounds. The role of glyoxylate, glycollate and acetate in the growth of Pseudomonas AM1 on ethanol and on C1 compounds. Biochem. J. 128:107–115.PubMedGoogle Scholar
  12. Goosen, N., Vermaas, D.A.M. and Putte, P.van de, 1987. Cloning of the genes involved in the synthesis of coenzyme pyrroloquinoline quinone from Acinetobacter calcoaceticus. J. Bacteriol. 169:303–307.PubMedGoogle Scholar
  13. Gorisch, H., 1987. Chorismate Mutase from Streptomyces aureofaciens. Methods Enzymol. 142:463–472.PubMedCrossRefGoogle Scholar
  14. Haslam, E., 1974. The Shikimate Pathway; Wiley, New York.Google Scholar
  15. Hirs, C.H.W., Moore, S. and Stein, W.H., 1954. Chromatography of amino acids on ion exchange resins. Use of volatile acids for elution. J. Am.Chem. Soc. 76:6063–6065.CrossRefGoogle Scholar
  16. Houck, D.R., Hanners, J.L. and Unkefer, C.J. 1988. Biosynthesis of Pyrroloquinoline quinone. 1. Identification of the biosynthetic precursors using 13C labeling and NMR spectroscopy. J. Am. Chem. Soc. 110:6920–6921.CrossRefGoogle Scholar
  17. Huber, M. Hintermann, G. and Lerch, K., 1985. Primary structure of tyrosinase from Streptomyces glaucescens. Biochem. 24:6038–6044.CrossRefGoogle Scholar
  18. Kleef, M.A.G. van and Duine, J.A., 1988. L-Tyrosine is the precursor of PQQ biosynthesis in Hyphomicrobium X. FEBS Lett. 237:91–97.PubMedCrossRefGoogle Scholar
  19. LeMaster, D.M. and Cronan, J.E., Jr., 1982. Biosynthetic production of 13C-labeled amino acids with site-specific enrichment. J. Biol. Chem. 257: 1224–1230.PubMedGoogle Scholar
  20. Lerch, K., 1982. Primary structure of tyrosinase from Neurospora crassa II. Complete amino acid sequence and chemical structure of a tripeptide containing an unusual thioether. J. Biol. Chem. 257:6414–6419.PubMedGoogle Scholar
  21. Lobenstein-Verbeek, C.L., Jongejan, J.A., Frank, Jzn. J. and Duine, J.A., 1984. Bovine serum amine oxidase: a mammalian enzyme having covalently-bound PQQ as a prosthetic group. FEBS Lett. 170:305–309.PubMedCrossRefGoogle Scholar
  22. Meer, R.A. van der and Duine, J.A., 1986. Covalently-bound Pyrroloquinoline quinone is the organic prosthetic group in human placental lysyl oxidase. Biochem. J. 239: 789–791.PubMedGoogle Scholar
  23. Meer, R.A. van der and Duine J.A., 1988. Pyrroloquinoline quinone is the organic cofactor in soybean lipoxygenase-1. FEBS Lett. 235:194–200.CrossRefGoogle Scholar
  24. Meer, R.A. van der, Jongejan, J.A., and Duine, J.A., 1988. Dopamine-β-hydroxylase from bovine medulla contains covalently-bound pyrroloquinoline quinone. FEBS Lett. 231:303–307.PubMedCrossRefGoogle Scholar
  25. Meer, R.A. van der, Jongejan, J.A., Frank, Jzn. J., and Duine, J.A., 1986. Hydrazone formation of 2,4-dinitrophenylhydrazine with PQQ in porcine kidney diamine oxidase. FEBS Lett. 206:111–114.PubMedCrossRefGoogle Scholar
  26. Putter, I., Barreto, A., Markley, J.L. and Jardetzkey, O., 1969. Nuclear magnetic resonance studies of the structure and binding sites of enzymes. X. Preparation of selectively deuterated analogs of staphylococcal nuclease. Proc. Nat. Acad. Sci. USA 64:1396–1403.PubMedCrossRefGoogle Scholar
  27. Walker, T.E., Matheny, C., Storm, C.B. and Hayden, H., 1986. An efficient chemomicrobiological synthesis of stable Isotope-labeled L-tyrosine and phenylalanine. J. Org. Chem. 51:1175–1179.CrossRefGoogle Scholar
  28. Walker, T.E. and London, R.E., 1987. Biosynthetic preparation of L-[13C]-and [15N]glutamate by Brevibacterium flavum. Appl. Env. Microbiol. 53:92–98.Google Scholar
  29. White, R.H. and Rudolf, F.B., 1978. The Origin of the nitrogen in the thiazole ring of thiamine in Escherichia coli. Biochim. Biophys. Acta. 542:340–347.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1989

Authors and Affiliations

  • David R. Houck
    • 1
  • John L. Hanners
    • 1
  • Clifford J. Unkefer
    • 1
  • Mario A. G. van Kleef
    • 2
  • Johannis A. Duine
    • 2
  1. 1.Los Alamos National LaboratoryUniversity of CaliforniaLos AlamosUSA
  2. 2.Laboratory of Microbiology and EnzymologyDelft University of TechnologyDelftThe Netherlands

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