The dynamic progression of evolved character states for aromatic amino acid biosynthesis in Gram-negative bacteria Free

Abstract

A systematic analysis of the evolution of aromatic amino acid biosynthesis in the Proteobacteria, previously focussed mainly upon the γ subdivision, has now been extended to the β subdivision. Five lineages were studied, represented by , rRNA Group-III pseudomonads/, and rRNA Group-II pseudomonads/Within the phenylalanine pathway, the bifunctional P-protein (chorismate mutase/prephenate dehydratase) was present in each lineage and must have evolved in a common ancestor of the β and γ subdivisions. Each P-protein was found to be subject to activation by L-tyrosine, and to feedback inhibition by L-phenylalanine. Phenylalanine-inhibited (DS-phe) and tyrosine-inhibited (DS-tyr) isoenzymes of 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase probably existed in the common β-subdivision ancestor, with DS-tyr being lost in and The participation of DS-phe in a dissociable multienzyme complex with one or more other common-pathway enzymes is known to exist in The same complex is indicated by two peaks of DS-phe seen in chromatographic profiles of Group-III pseudomonads and It is concluded that the contemporary DS-phe species present in subdivisions γ and β must have had independent origins. Tyrosine biosynthesis was found to be quite diverse within the β subdivision. possessed an arogenate dehydrogenase which was specific for NADP. In all other lineages, a broad-specificity cyclohexadienyl dehydrogenase (CDH) was present. In the CDH was specific for NADwhile the remaining CDH species could utilize either NADor NADP. Only the CDH species within the rRNA Group-II pseudomonad/lineage was feedback-inhibited by L-tyrosine, and this correlated with an allosteric pattern where activation of the prephenate dehydratase component of the P-protein by L-tyrosine was relatively poor. However, the CDH enzyme present in and was subject to inhibition by 4-hydroxyphenylpyruvate, this being competitive with respect to the cyclohexadienyl substrate. The monofunctional species of chorismate mutase (CM-F) and cyclohexadienyl dehydratase, widely distributed among the γ-subdivision assemblage and recently shown to be periplasmic enzymes, were demonstrated in , a member of rRNA homology Group-II.

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1994-12-01
2024-03-28
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References

  1. Ahmad S., Jensen R.A. Evolution of the biochemical pathway for aromatic amino acid biosynthesis in Serpens flexibilis in relationship to its phylogenetic position. Arch Microbiol 1987; 147:8–12
    [Google Scholar]
  2. Ahmad S., Jensen R.A. New prospects for deducing the evolutionary history of metabolic pathways in prokaryotes: aromatic biosynthesis as a case-in-point. Origins Life Evol Biosphere 1988a; 18:41–57
    [Google Scholar]
  3. Ahmad S., Jensen R.A. Phylogenetic distribution of components of the overflow pathway to L-phenylalanine within the enteric lineage of bacteria. Curr Microbiol 1988b; 16:295–302
    [Google Scholar]
  4. Ahmad S., Rightmire B., Jensen R.A. Evolution of the regulatory isozymes of 3-deoxy-D-itr'«o-heptulosonate-7-phos-phate synthase present in the Escherichia coli genealogy. J Bacterial 1986; 165:146–154
    [Google Scholar]
  5. Ahmad S., Johnson J.L., Jensen R.A. The recent evolutionary origin of the phenylalanine-sensitive isoenzyme of 3-deoxy-D-ijrrffo«0-heptulosonate-7-phosphate synthase in the enteric lineage of bacteria. J Mol Evol 1987; 25:159–167
    [Google Scholar]
  6. Arciero D., Balny C., Hooper A.B. Spectroscopic and rapid kinetic studies of reduction of cytochrome ¿554 by hydroxylamine oxidoreductase from Nitrosomonas europaea. Biochemistry 1991; 30:11466–11472
    [Google Scholar]
  7. Ballou C.E. Preparation and properties of D-erythrose 4-phosphate. Methods Enzymol 1963; 6:479–484
    [Google Scholar]
  8. Berry A., Johnson J.L., Jensen R.A. Phenylalanine hydroxylase and isozymes of 3-deoxy-D-i7ra£/«o-heptulosonate-7-phosphate synthase in relationship to the phylogenetic position of Pseudomonas acidovorans (Ps sp ATCC 11299a). Arch Microbiol 1985; 141:32–39
    [Google Scholar]
  9. Berry A., Jensen R.A., Hendry A.T. Enzymatic arrangement and allosteric regulation of the aromatic amino acid pathway in Neisseria gonorrhoeae. Arch Microbiol 1987; 149:87–94
    [Google Scholar]
  10. Bhatnagar R.K., Berry A., Henry A.T., Jensen R.A. The biochemical basis for growth inhibition by L-phenylalanine in Neisseria gonorrhoeae. Mol Microbiol 1989; 3:429–436
    [Google Scholar]
  11. Bonner C.A., Jensen R.A. Arogenate dehydrogenase. Methods Enyymol 1987; 142:488–494
    [Google Scholar]
  12. Bonner C.A., Fischer R.S., Ahmad S., Jensen R.A. Remnants of an ancient pathway to L-phenylalanine and L-tyrosine in enteric bacteria: evolutionary implications and biotechnological impact. Appl Environ Microbiol 1990; 56:3741–3747
    [Google Scholar]
  13. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–254
    [Google Scholar]
  14. Byng G.S., Whitaker R.J., Gherna R.L., Jensen R.A. Variable enzymological patterning in tyrosine biosynthesis as a means of determining natural relatedness among the Pseudo-monadaceae. J Bacteriol 1980; 144:247–257
    [Google Scholar]
  15. Byng G.S., Johnson J.L., Whitaker R.J., Gherna R.L., Jensen R.A. The evolutionary pattern of aromatic amino acid biosynthesis and the emerging phylogeny of pseudomonad bacteria. J Mol Evol 1983; 19:272–282
    [Google Scholar]
  16. Byng G.S., Berry A., Jensen R.A. Evolution of aromatic biosynthesis and fine-tuned phylogenetic positioning of Azomonas, Azotobacter and rRNA Group I pseudomonads. Arch Microbiol 1986; 144:222–227
    [Google Scholar]
  17. Fischer R., Jensen R.A. Arogenate dehydratase. Methods Ensymol 1987a; 142:495–502
    [Google Scholar]
  18. Fischer R., Jensen R.A. Prephenate dehydrogenase (monofunctional). Methods Ensymol 1987b; 142:503–507
    [Google Scholar]
  19. Fox G.E., Stackebrandt E., Hespell R.B., Gibson J., Maniloff J., Dyer T.A., Wolfe R.S., Balch W.E., Tanner R., Magrum L., Zablen L.B., Blakemore R., Gupta R., Bonen L., Lewis B.J., Stahl D.A., Luehrsen K.R., Chen K.N., Woese C.R. The phylogeny of prokaryotes. Science 1980; 209:457–463
    [Google Scholar]
  20. Friedrich C.G., Schlegel H.G. Aromatic amino acid biosynthesis in Alcaligenes eutrophus H16. J Bacteriol 1975; 103:133–140
    [Google Scholar]
  21. Friedrich C.G., Friedrich B., Schlegel H.G. Purification and properties of chorismate mutase-prephenate dehydratase and prephenate dehydrogenase from Alcaligenes eutrophus. J Bacteriol 1976a; 126:712–722
    [Google Scholar]
  22. Friedrich C.G., Friedrich B., Schlegel H.G. Regulation of chorismate mutase-prephenate dehydratase and prephenate dehydrogenase from Alcaligenes eutrophus. J Bacteriol 1976b; 126:723–732
    [Google Scholar]
  23. Gibson F. Chorismic acid. Purification and some chemical and physical studies. Biochem J 1964; 90:256–261
    [Google Scholar]
  24. Guroff G., Ito T. Induced soluble phenylalanine hydroxylase from Pseudomonas sp grown on phenylalanine or tyrosine. Biochim Biophys Acta 1963; 77:159–161
    [Google Scholar]
  25. Hendry A.T. Growth responses of Neisseria gonorrhoeae auxotvpes to required amino acids and bases in liquid medium. Can J Microbiol 1983; 29:1309–1313
    [Google Scholar]
  26. Imhoff J.F., Triier H.G., Pfenning N. Rearrangement of the species and genera of the phototrophic “purple nonsulfur bacteria”. Int J Syst Bacteriol 1984; 34:340–343
    [Google Scholar]
  27. Jensen R.A. Biochemical pathways can be traced backward through evolutionary time. Mol Biol Evol 1985; 2:92–108
    [Google Scholar]
  28. Jensen R.A. An emerging outline of the evolutionary history of aromatic amino acid biosynthesis. In The Evolution of Metabolic Function 1992 Edited by Mortlock R.P. Boca Raton, FL: CRC Press; pp 205–236
    [Google Scholar]
  29. Jensen R.A., Ahmad S. Nested gene fusions as markers of phylogenetic branchpoints in prokaryotes. Trends Ecol Evol 1990; 5:219–224
    [Google Scholar]
  30. Jensen R.A., Nester E.W. Regulatory enzymes of aromatic amino acid biosynthesis in Bacillus subtilis. I. Purification and properties of 3-deoxy-D-arabino-heptulosonate-7-phosphate synthetase. J Biol Chem 1966; 241:3365–3372
    [Google Scholar]
  31. Koops H.-P., Böttcher B., Möler U.C., Pommerening-Röser A., Stehr G. Classification of eight new species of ammonia-oxidizing bacteria: Nitrosomonas cummunis sp. nov., Nitrosomonas ureae sp. nov., Nitrosomonas aestuarii sp. nov., Nitrosomonas marina sp. nov., Nitrosomonas nitrosa sp. nov., Nitrosomonas eutropha sp nov, Nitrosomonas oligoropha sp nov and Nitrosomonas halophila sp nov. J Gen Microbiol 1991; 137:1689–1699
    [Google Scholar]
  32. Larsen N., Olsen G.J., Maidak B.L., McCaughey J., Overbeek R., Macke T.J., Marsh T.L., Woese C.R. The ribosomal database project. Nucleic Acids Res 1993; 21:3021–3023
    [Google Scholar]
  33. Palleroni N.J., Kinisawa R., Contopoulou R., Doudoroff M. Nucleic acid homologies in the genus Pseudomonas. Int J Syst Bacteriol 1973; 23:333–339
    [Google Scholar]
  34. Patel N., Pierson D.L., Jensen R.A. Dual enzymatic routes to L-tyrosine and L-phenylalanine via pretyrosine in Pseudomonas aeruginosa. J Biol Chem 1977; 252:5839–5846
    [Google Scholar]
  35. Smith M.W., Feng D.-F., Doolittle R.F. Evolution by acquisition: the case for horizontal gene transfers. Trends Biochem Sei 1992; 17:489–493
    [Google Scholar]
  36. Whitaker R.J., Byng G.S., Gherna R.L., Jensen R.A. Comparative allostery of 3-deoxy-D-öröz/«o-heptulosonate-7-phos-phate synthase as an indicator of taxonomic relatedness in pseudomonad genera. J Bacteriol 1981a; 145:752–759
    [Google Scholar]
  37. Whitaker R.J., Byng G.S., Gherna R.L., Jensen R.A. Diverse enzymological patterns of phenylalanine biosynthesis in pseudomonads are conserved in parallel with deoxyribonucleic acid homology groupings. J Bacteriol 1981b; 147:526–534
    [Google Scholar]
  38. Willems A., Gillis M., & De Ley J. Transfer of Rhodocyclus gelatinosas to Rubrivivax gelatinosas gen comb, nov., and phylogenetic relationships with Eeptothrix, Sphaerotilus natans, Pseudomonas saccharophila and Alcaligenes latus. Int J Syst Bacteriol 1991; 41:65–73
    [Google Scholar]
  39. Woese C.R. Bacterial evolution. Microbiol Rev 1987; 51:221–271
    [Google Scholar]
  40. Woese C.R., Blanz P., Hahn C.M. What isn’t a pseudomonad: the importance of nomenclature in bacterial classification. Syst Appl Microbiol 1984; 5:179–195
    [Google Scholar]
  41. Xia T., Jensen R.A. A single cyclohexadienyl dehydrogenase specifies the prephenate dehydrogenase and arogenate dehydrogenase components of the dual pathways to L-tyrosine in Pseudomonas aeruginosa. J Biol Chem 1990; 265:20033–20036
    [Google Scholar]
  42. Xia T., Song J., Zhao G., Aldrich H., Jensen R.A. The aroQ-encoded monofunctional chorismate mutase (CM-F) protein is a periplasmic enzyme in Erwinia herbicola. J Bacteriol 1993; 175:4729–4737
    [Google Scholar]
  43. Zamir L.O., Tiberio R., Fiske M., Berry A., Jensen R.A. Enzymatic and non-enzymatic dehydration reactions of l-arogenate. Biochemistry 1985; 24:1607–1612
    [Google Scholar]
  44. Zhao G., Xia T., Aldrich H., Jensen R.A. Cyclo-hexadienyl dehydratase from Pseudomonas aeruginosa is a peri-plasmic protein. J Gen Microbiol 1993a; 139:807–813
    [Google Scholar]
  45. Zhao G., Xia T., Ingram L., Jensen R.A. An allosterically insensitive type of cyclohexadienyl dehydrogenase from Zymomonas mobilis. Eur J Biochem 1993b; 212:157–165
    [Google Scholar]
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