Folia Microbiologica

, 49:247 | Cite as

Evolutionary relatedness between glycolytic enzymes most frequently occurring in genomes

  • A. Oslancová
  • Š. Janeček


More than 100 sequenced genomes were searched for genes coding for the enzymes involved in glycolysis in an effort to find the most frequently occurring ones. Triosephosphate isomerase (TIM), glyceraldehyde-3-phosphate dehydrogenase (GAPD), phosphoglycerate kinase (PGK) and enolase (ENOL) were found to be present in 90 investigated genomes all together. The final set consisted of 80 prokaryotic and 10 eukaryotic genomes. Of the 80 prokaryotic genomes, 73 were from Bacteria, 7 from Archaea. Two microbial genomes were also from Eucarya (yeasts). Eight genomes of nonmicrobial origin were included for comparison. The amino acid sequences of TIMs, GAPDs, PGKs and ENOLs were collected and aligned, and their individual as well as concatenated evolutionary trees were constructed and discussed. The trees clearly demonstrate a closer relatedness between Eucarya and Archaea (especially the concatenated tree) but they do not support the hypothesis that eukaryotic glycolytic enzymes should be closely related to their α-proteobacterial counterparts. Phylogenetic analyses further reveal that although the taxonomic groups (e.g., α-proteobacteria, γ-proteobacteria, firmicutes, actinobacteria,etc.) form their more or less compact clusters in the trees, the inter-clade relationships between the trees are not conserved at all. On the other hand, several examples of conservative relatedness separating some clades of the same taxonomic groups were observed,e.g., Buchnera along withWigglesworthia and the rest of γ-proteobacteria, or mycoplasmas and the rest of firmicutes. The results support the view that these glycolytic enzymes may have their own evolutionary history.


Enol Glycolytic Enzyme Borrelia Burgdorferi Neisseria Meningitidis Phosphoglycerate Kinase 
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.


  1. Antonyuk S.V., Eady R.R., Strange R.W., Hasnain S.S.: The structure of glyceraldehyde-3-phosphate dehydrogenase fromAlcaligenes xylosoxidans at 1.7 Å resolution.Acta Crystallogr. D59, 835–842 (2003).Google Scholar
  2. Bairoch A., Apweiler R.: The Swiss Prot protein sequence database and its supplement TrEMBL, in 2000.Nucl.Acids Res. 28, 45–48 (2000).PubMedCrossRefGoogle Scholar
  3. Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J., Rapp B.A., Wheeler D.L.: GenBank.Nucl.Acids Res. 28, 15–18 (2000).PubMedCrossRefGoogle Scholar
  4. Bernstein B.E., Williams D.M., Bressi J.C., Kuhn P., Gelb M.H., Blackburn G.M., Hol W.G.: A bisubstrate analog induces unexpected conformational changes in phosphoglycerate kinase fromTrypanosoma brucei.J.Mol.Biol. 279, 1137–1148 (1998).PubMedCrossRefGoogle Scholar
  5. Canback B., Andersson S.G., Kurland C.G.: The global phylogeny of glycolytic enzymes.Proc.Nat.Acad.Sci.USA 99, 6097–6102 (2002).PubMedCrossRefGoogle Scholar
  6. Cordwell S.J.: Microbial genomes and “missing enzymes”: redefining biochemical pathways.Arch.Microbiol. 172, 269–279 (1999).PubMedCrossRefGoogle Scholar
  7. Dandekar T., Schuster S., Snel B., Huynen M., Bork P.: Pathway alignment: application to the comparative analysis of glycolytic enzymes.Biochem.J. 343, 115–124 (1999).PubMedCrossRefGoogle Scholar
  8. Erlandsen H., Abola E.E., Stevens R.C.: Combining structural genomics and enzymology: completing the picture in metabolic pathways and enzyme active sites.Curr.Opin.Struct.Biol. 10, 719–730 (2000).PubMedCrossRefGoogle Scholar
  9. Felsenstein J.: Confidence limits on phylogenies: an approach using the bootstrap.Evolution 39, 783–791 (1985).CrossRefGoogle Scholar
  10. Figge R.M., Cerff R.: GAPDH gene diversity in spirochetes: a paradigm for genetic promiscuity.Mol.Biol.Evol. 18, 2240–2249 (2001).PubMedGoogle Scholar
  11. Fleming T., Littlechild J.: Sequence and structural comparison of thermophilic phosphoglycerate kinases with a mesophilic equivalent.Comp.Biochem.Physiol. A118, 439–451 (1997).CrossRefGoogle Scholar
  12. Fothergill-Gilmore L.A.: The evolution of glycolytic pathway.Trends Biochem.Sci. 11, 47–51 (1986).CrossRefGoogle Scholar
  13. Fothergill-Gilmore L.A., Michels P.A.M.: Evolution of glycolysis.Progr.Biophys.Mol.Biol. 59, 105–235 (1993).CrossRefGoogle Scholar
  14. Galperin M.Y., Koonin E.V.: Functional genomics and enzyme evolution. Homologous and analogous enzymes encoded in microbial genomes.Genetica 106, 159–170 (1999).PubMedCrossRefGoogle Scholar
  15. Gebbia J.A., Backenson P.B., Coleman J.L., Anda P., Benach J.L.: Glycolytic enzyme operon ofBorrelia burgdorferi: characterization and evolutionary implications.Gene 188, 221–228 (1997).PubMedCrossRefGoogle Scholar
  16. Gogarten J.P., Olendzenski L., Hilario E., Simon C., Holsinger K.E.: Dating the cenancester of organisms.Science 274, 1750–1751 (1996).PubMedCrossRefGoogle Scholar
  17. Hannaert V., Brinkmann H., Nowitzki U., Lef J.A., Albert M.A., Sensen C.W., Gaasterland T., Muller M., Michels P., Martin W.: Enolase fromTrypanosoma brucei, from the amitochondriate protistMastigamoeba balamuthi, and from the chloroplast and cytosol ofEuglena gracilis: pieces in the evolutionary puzzle of the eukaryotic glycolytic pathway.Mol.Biol.Evol. 17, 989–1000 (2000).PubMedGoogle Scholar
  18. Henrissat B., Deleury E., Coutinho P.M.: Glycogen metabolism loss: a common marker of parasitic behavior in bacteria?Trends Genet. 18, 437–440 (2002).PubMedCrossRefGoogle Scholar
  19. Huynen M.A., Dandekar T., Bork P.: Variation and evolution of the citric-acid cycle: a genomic perspective.Trends Microbiol. 7, 281–291 (1999).PubMedCrossRefGoogle Scholar
  20. Isupov M.N., Fleming T.M., Dalby A.R., Crowhurst G.S., Bourne P.C., Littlechild J.A.: Crystal structure of the glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic archaeonSulfolobus solfataricus.J.Mol.Biol. 291, 651–660 (1999).PubMedCrossRefGoogle Scholar
  21. Keeling P.J., Doolittle W.F.: Evidence that eukaryotic triosephosphate isomerase is of α-proteobacterial origin.Proc.Nat.Acad.Sci.USA 94, 1270–1275 (1997).PubMedCrossRefGoogle Scholar
  22. Klenk H.P., Clayton R.A., Tomb J.F., White O., Nelson K.E., Ketchum K.A., Dodson R.J., Gwinn M., Hickey E.K., Peterson J.D., Richardson D.L., Kerlavage A.R., Graham D.E., Kyrpides N.C., Fleischmann R.D., Quackenbush J., Lee N.H., Sutton G.G., Gill S., Kirkness E.F., Dougherty B.A., McKenney K., Adams M.D., Loftus B., Peterson S., Reich C.I., McNeil L.K., Badger J.H., Glodek A., Zhou L., Overbeek R., Gocayne J.D., Weidman J.F., McDonald L., Utterback T., Cotton M.D., Spriggs T., Artiach P., Kaine B.P., Sykes S.M., Sadow P.W., D’Andrea K.P., Bowman C., Fujii C., Garland S.A., Mason T.M., Olsen G.J., Fraser C.M., Smith H.O., Woese C.R., Venter J.C.: The complete genome sequence of the hyperthermophilic, sulfate-reducing archaeonArchaeoglobus fulgidus.Nature 390, 364–370 (1997).PubMedCrossRefGoogle Scholar
  23. Kohlhoff M., Dahm A., Hensel R.: Tetrameric trioscphosphate isomerase from hyperthermophilic Archaea.FEBS Lett. 383, 245–250 (1996).PubMedCrossRefGoogle Scholar
  24. Kováčová A., Janeček Š.: Evolutionary relationships of glycolytic (β/α)8-barrel enzymes present in completely sequenced genomes.Biologia (Bratislava) 57, 283–288 (2002).Google Scholar
  25. Lebioda L., Stec B., Brewer J.M.: The structure of yeast enolase at 2.25-Å resolution. An 8-fold β+α-barrel with a novel ββαα (βα)6 topology.J.Biol.Chem. 264, 3685–3693 (1989).PubMedGoogle Scholar
  26. Lolis E., Alber T., Davenport R.C., Rose D., Hartman F.C., Petsko G.A.: Structure of yeast triosephosphate isomerase at 1.9-Å resolution.Biochemistry 29, 6609–6618 (1990).PubMedCrossRefGoogle Scholar
  27. Martin W., Müller M.: The hydrogen hypothesis for the first cukaryote.Nature 392, 37–41 (1998).PubMedCrossRefGoogle Scholar
  28. Muirhead H., Watson H.: Glycolytic enzymes: from hexose to pyruvate.Curr.Opin.Struct.Biol. 2, 870–876 (1992).CrossRefGoogle Scholar
  29. van der Oost J., Huynen M.A., Verhees C.H.: Molecular characterization of phosphoglycerate mutase in archaea.FEMS Microbiol.Lett. 212, 111–120 (2002).PubMedGoogle Scholar
  30. Page R.D.: TreeView: an application to display phylogenetic trees on personal computers.Comput.Applic.Biosci. 12, 357–358 (1996).Google Scholar
  31. Pujadas G., Palau J.: TIM barrel fold: structural, functional and evolutionary characteristics in natural and designed molecules.Biologia (Bratislava) 54, 231–254 (1999).Google Scholar
  32. Ronimus R.S., Morgan H.W.: Distribution and phylogenies of enzymes of the Embden-Meyerhof-Parnas pathway from archaea and hyperthermophilic bacteria support a gluconeogenic origin of metabolism.Archaea 1, 199–221 (2003).PubMedCrossRefGoogle Scholar
  33. Saiiou N., Nei M.: The neighbor-joining method: a new method for reconstructing phylogenetic trees.Mol.Biol.Evol. 4, 406–425 (1987).Google Scholar
  34. Schmidt S., Sunyaev S., Bork P., Dandekar T.: Metabolites: a helping hand for pathway evolution?Trends Biochem.Sci. 28, 336–341 (2003).PubMedCrossRefGoogle Scholar
  35. Schuler G.D., Epstein J.A., Ohkawa H., Kans J.A.: Entrez: molecular biology database and retrieval system.Meth.Enzymol. 266, 141–162 (1996).PubMedCrossRefGoogle Scholar
  36. Skarzynski T., Moody P.C., Wonacott A.J.: Structure of holo-glyceraldehyde-3-phosphate dehydrogenase fromBocillus stearothermophilus at 1.8 Å resolution.J.Mol.Biol. 193, 171–187 (1987).PubMedCrossRefGoogle Scholar
  37. Stec B., Lebioda L.: Refined structure of yeast apo-enolase at 2.25 å resolution.J.Mol.Biol. 211, 235–248 (1990).PubMedCrossRefGoogle Scholar
  38. Thompson J.D., Higgins D.G., Gibson T.J.: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment trough sequence weighting, position specific gap penalties and weight matrix choice.Nucl.Acids Res. 22, 4673–4680 (1994).PubMedCrossRefGoogle Scholar
  39. Tomb J.F., White O., Kerlavage A.R., Clayton R.A., Sutton G.G., Fleischmann R.D., Ketchum K.A., Klenk H.P., Gill S., Dougherty B.A., Nelson K., Quackenbush J., Zhou L., Kirkness E.F., Peterson S., Loftus B., Richardson D., Dodson R., Khalak H.G., Glodek A., McKenney K., Fitzegerald L.M., Lee N., Adams M.D., Hickey F.K., Berg D.E., Gocayne J.D., Utterback T.R., Peterson J.D., Kelley J.M., Cotton M.D., Weidman J.M., Fujii C., Bowman C., Watthey L., Wallin E., Hayes W.S., Borodovsky M., Karp P.D., Smith H.O., Fraser C.M., Venter J.C.: The complete genome sequence of the gastric pathogenHelicobacter pylori.Nature 388, 539–547 (1997).PubMedCrossRefGoogle Scholar
  40. Velanker S.S., Ray S.S., Gokhale R.S., Suma S., Balaram H., Balaram P., Murthy M.R.N.: Triosephosphate isomerase fromPlasmodium falciparum: the crystal structure provides insights into antimalarial drug design.Structure 5, 751–761 (1997).PubMedCrossRefGoogle Scholar
  41. Verhees C.H., Kengen S.W.M., Tuininga J.E., Schut G.J., Adams M.W.W., de Vos W.M., Van der Oost J.: The unique features of glycolytic pathways in Archaea.Biochem.J. 375, 231–246 (2003).PubMedCrossRefGoogle Scholar
  42. Watson H.C., Walker N.P., Shaw P.J., Bryant T.N., Wendell P.L., Fothergill L.A., Perkins R.E., Conroy S.C., Dobson M.J., Tuite M.F., Kingsman A.J., Kingsman S.M.: Sequence and structure of yeast phosphoglycerate kinase.EMBO J. 1, 1635–1640 (1982).PubMedGoogle Scholar
  43. Wedekind J.E., Poyner R.R., Reed G.H., Rayment I.: Chelation of serine-39 to Mg2+ latches a gate at the active site of enolase: structure of the bis(Mg2+) complex of yeast enolase and the intermediate, phosphonoacetohydroxamate, at 2.1 Å resolution.Biochemistry 33, 9333–9342 (1994).PubMedCrossRefGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic 2004

Authors and Affiliations

  1. 1.Institute of Molecular Biology, Center of Excellence for Molecular MedicineSlovak Academy of SciencesBratislavaStovakia

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