Journal of Molecular Evolution

, Volume 58, Issue 2, pp 225–237

Molecular Evolution of hisB Genes

Article

Abstract

The sixth and eighth steps of histidine biosynthesis are catalyzed by an imidazole glycerol-phosphate (IGP) dehydratase (EC 4.2.1.19) and by a histidinol-phosphate (HOL-P) phosphatase (EC 3.1.3.15), respectively. In the enterobacteria, in Campylobacter jejuni and in Xylella/Xanthomonas the two activities are associated with a single bifunctional polypeptide encoded by hisB. On the other hand, in Archaea, Eucarya, and most Bacteria the two activities are encoded by two separate genes. In this work we report a comparative analysis of the amino acid sequence of all the available HisB proteins, which allowed us to depict a likely evolutionary pathway leading to the present-day bifunctional hisB gene. According to the model that we propose, the bifunctional hisB gene is the result of a fusion event between two independent cistrons joined by domain-shuffling. The fusion event occurred recently in evolution, very likely in the proteobacterial lineage after the separation of the γ- and the β-subdivisions. Data obtained in this work established that a paralogous duplication event of an ancestral DDDD phosphatase encoding gene originated both the HOL-P phosphatase moiety of the E. colihisB gene and the gmhB gene coding for a DDDD phosphatase, which is involved in the biosynthesis of a precursor of the inner core of the outer membrane lipopolysaccharides (LPS).

Keywords

gmhB hisN Evolution of metabolic pathways Gene fusion Gene duplication Patchwork hypothesis 

References

  1. 1.
    Alifano, P, Fani, R, Liò, P, Lazcano, A, Bazzicalupo, M, Carlomagno, MS, Bruni, CB 1996Histidine biosynthetic pathway and genes: Structure, regulation and evolution.Microbiol Rev604469PubMedGoogle Scholar
  2. 2.
    Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W, Lipman, DJ 1997Gapped BLAST and PSI-BLAST: A new generation of protein database search programs.Nucleic Acids Res2533893402PubMedGoogle Scholar
  3. 3.
    Aravind, L, Koonin, EV 1998Phosphoesterase domains associated with DNA polymerase of diverse origins.Nucleic Acids Res2637463752CrossRefPubMedGoogle Scholar
  4. 4.
    Brady, DR, Houston, LL 1973Some properties of the catalytic sites of imidazoleglycerolephosphate dehydratase-histidinol posphate phosphatase, a bifunctional enzyme from Salmonella typhimurium.J Biol Chem24825882592PubMedGoogle Scholar
  5. 5.
    Brilli, M, Lazcano, A, Liò, P, Fani, R 2002Structure and evolution of the histidine biosynthetic pathway.Orig Life Evol Biosph32488Google Scholar
  6. 6.
    Broach, JR 1981

    Genes of Saccharomyces cerevisiae.

    Strathern, JNJones, EWBroach, JR eds. The molecular biology of the yeast Saccharomyces: Life cycle and inheritance.Cold Spring HarborNY653727
    Google Scholar
  7. 7.
    Carlomagno, MS, Chiarotti, L, Alifano, P, Nappo, AG, Bruni, CB 1988Structure of the Salmonella typhimurium and Escherichia coli K-12 histidine operons.J Mol Biol203585606PubMedGoogle Scholar
  8. 8.
    Chumley, FG, Roth, JR 1981Genetic fusions that place the lactose genes under histidine operon control.J Mol Biol145697712PubMedGoogle Scholar
  9. 9.
    Clarke, PH 1974

    The evolution of enzymes for the utilization of novel substrates.

    Carlile, MJSkehel, JJ eds. Evolution in the microbial world.Cambridge University PressCambridge
    Google Scholar
  10. 10.
    Cole, JR, Chai, B, Marsh, TL, Farris, RJ, Wang, Q, Kulam, SA, Chandra, S, McGarrell, DM, Schmidt, TM, Garrity, GM, Tiedje, JM 2003The Ribosomal Database Project (RDP-II): Previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy.Nucleic Acids Res31442443CrossRefPubMedGoogle Scholar
  11. 11.
    Fani, R, Bazzicalupo, M, Damiani, G, Bianchi, A, Schipani, C, Sgaramella, V, Polsinelli, M 1989Cloning of the histidine genes of Azospirillum brasilense: Organization of the ABFH gene cluster and nucleotide sequence of the hisB gene.Mol Gen Genet216224229PubMedGoogle Scholar
  12. 12.
    Fani, R, Liò, P, Lazcano, A 1995Molecular evolution of the histidine biosynthetic pathway.J Mol Evol41760774PubMedGoogle Scholar
  13. 13.
    Fani, R, Mori, E, Tamburini, E, Lazcano, A 1998Evolution of the structure and chromosomal distribution of histidine biosynthetic genes.OLEB28555570CrossRefGoogle Scholar
  14. 14.
    Fink, GR 1964Gene-enzyme relations in histidine biosynthesis in yeast.Science146525527PubMedGoogle Scholar
  15. 15.
    Glaser, RD, Houston, LL 1974Subunit structure and photooxidation of yeast imidazoleglycerolphosphate dehydratase.Biochemistry1351455152PubMedGoogle Scholar
  16. 16.
    Hall, TA 1999BioEdit: A user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.Nucleic Acids Symp Ser419598Google Scholar
  17. 17.
    Jensen, RA 1976Enzyme recruitment in evolution of new function.Annu Rev Microbiol30409425CrossRefPubMedGoogle Scholar
  18. 18.
    Jensen, RA, Ahmad, S 1990Nested gene fusions as markers of phylogenetic branchpoints in prokaryotes.Trends Ecol Evol5219224CrossRefGoogle Scholar
  19. 19.
    Jürgens, C, Strom, A, Wegener, D, Hettwer, S, Wilmanns, M, Sterner, R 2000Directed evolution of a (βα)8-barrel enzyme to catalyze related reactions in two different metabolic pathways.Proc Natl Acad Sci USA9799259930CrossRefPubMedGoogle Scholar
  20. 20.
    Kimura, M 1980A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences.J Mol Evol16111120PubMedGoogle Scholar
  21. 21.
    Kneidinger, B, Marolda, C, Graninger, M, Zamyatina, A, McArthur, F, Kosma, P, Valvano, MA, Messner, P 2002Biosynthesis pathway of ADP-L-glycero-β-D-manno-heptose in Escherichia coli.J Bacteriol184363369CrossRefPubMedGoogle Scholar
  22. 22.
    Kumar, S, Tamura, K, Jacobsen, IB, Nei, M 2001MEGA2: Molecular evolutionary genetics analysis software.Bioinformatics1712441245PubMedGoogle Scholar
  23. 23.
    Lazcano, A, Miller, SL 1996The origin and early evolution of life: prebiotic chemistry, the pre-RNA world, and time.Cell85793798PubMedGoogle Scholar
  24. 24.
    Lazcano, A, Fox, GE, Oro’, J 1992

    Life before DNA: The origin and evolution of early Archean cells.

    Mortlock, RP eds. The evolution of metabolic function.CRC PressBoca Raton FL237339
    Google Scholar
  25. 25.
    Le Coq, D, Fillinger, S, Aymerich, S 1999Histidinol phosphate phosphatase, catalyzing the penultimate step of the histidine biosynthesis pathway, is encoded by ytvP (hisJ) in Bacillus subtilis.J Bacteriol18132773280PubMedGoogle Scholar
  26. 26.
    Limauro, D, Avitabile, A, Cappellano, C, Puglia, AM, Bruni, CB 1990Cloning and characterization of the histidine biosynthetic gene cluster of Streptomyces coelicolor A3(2)Gene903141CrossRefPubMedGoogle Scholar
  27. 27.
    Loper, JC 1961Enzyme complementation in mixed extracts of mutants from the Salmonella histidine B locus.Proc Natl Acad Sci USA471440l450PubMedGoogle Scholar
  28. 28.
    Malone, RE, Kim, S, Bullard, SA, Lundquist, S, Hutchings-Crow, L, Cramton, S, Lutfiyya, L, Lee, J 1994Analysis of a recombination hotspot for gene conversion occurring at the HIS2 gene of Saccharomyces cerevisiae.Genetics137518PubMedGoogle Scholar
  29. 29.
    Morales, AC, Nozawa, SR, Thedei, Jr G, Maccheroni, Jr W, Rossi, A 2000Properties of a constitutive alkaline phosphatase from strain 74A of the mold Neurospora crassa.Braz J Med Biol Res33905912PubMedGoogle Scholar
  30. 30.
    Mortlock, RP, Gallo, MA 1992

    Experiments in the evolution of gatabolic pathways using modern bacteria.

    Mortlock, RP eds. The evolution of metabolic functions.CRC PressBoca Raton, FL113
    Google Scholar
  31. 31.
    Nei, M, Kumar, S 2000Molecular evolution and phylogenetics.Oxford University PressNew YorkGoogle Scholar
  32. 32.
    Peretò, J, Fani, R, Leguina, JI, Lazcano, A 1998

    Enzyme evolution and the development of metabolic pathways.

    Cornish-Bowden, A eds. New beer in an old bottle: Eduard Buchner and the growth of biochemical knowledge.Universitat de ValenciaValencia173198
    Google Scholar
  33. 33.
    Shigenobu, S, Watanabe, H, Hattori, M, Sakaki, Y, Ishikawa, H 2000Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp.APS. Nature4078186CrossRefGoogle Scholar
  34. 34.
    Thaller, MC, Schippa, S, Rossolini, GM 1998Conserved sequence motifs among bacterial, eukaryotic, and archaeal phosphatases that define a new phosphohydrolase superfamily.Protein Sci716471652PubMedGoogle Scholar
  35. 35.
    Thompson, JD, Higgins, DG, Gibson, TJ 1994CLUSTALW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight-matrix choice.Nucleic Acids Res2246734680PubMedGoogle Scholar
  36. 36.
    Vance, JR, Wilson, TE 2001Uncoupling of 3’-phosphatase and 5’-kinase functions in budding yeast.J Biol Chem2761507315081CrossRefPubMedGoogle Scholar
  37. 37.
    Winkler, ME 1987

    Biosynthesis of histidine.

    Neidhardt, FCIngraham, JLLow, KBMagasanik, BSchaechter, MHumbarger, HD eds. Escherichia coli and Salmonella typhimurium: Cellular and molecular biology.ASM PressWashington, DC395411
    Google Scholar
  38. 38.
    Ycas, M 1974On the earlier states of the biochemical system.J Theor Biol44145160PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 2004

Authors and Affiliations

  1. 1.Dipartimento di Biologia Animale e GeneticaVia Romana 17-19, 1-50125, FirenzeItaly

Personalised recommendations