Summary
The genes for four glycolytic enzymes ofTrypanosoma brucei have been analyzed. The proteins encoded by these genes show 38–57% identity with their counterparts in other organisms, whether pro- or eukaryotic. These data are consistent with a phylogenetic tree in which trypanosomes diverged very early from the main branch of the eukaryotic lineage. No definite conclusion can be drawn yet about the evolutionary origin of glycosomes, the microbodies of trypanosomes which contain most enzymes of the glycolytic pathway. A bias could be observed in the codon usage of the glycolytic genes and genes for other housekeeping proteins, indicating that trypanosomes may have selected a nucleotide sequence that enables efficient translation. However, the genes for variant surface glycoproteins (VSGs) do not show such a bias. This lack of preference for special codons is explained by the high evolutionary rate that could be observed for VSG genes.
Similar content being viewed by others
Abbreviations
- ALDO:
-
aldolase
- TIM:
-
triosephosphate isomerase
- GAPDH:
-
glyceraldehydephosphate dehydrogenase
- PGK:
-
phosphoglycerate kinase
- VSG:
-
variant surface glycoprotein
- ESAG:
-
expression site associate gene
References
Benne R (1985) Mitochondrial genes in trypanosomes. Trends Genet. 1:117–121
Bennetzen JL, Hall BD (1982) Codon selection in yeast. J Biol Chem 257:3026–3031
Bernards A, De Lange T, Michels PAM, Liu AYC, Huisman MJ, Borst P (1984a) Two modes of activation of a single surface antigen gene ofTrypanosoma brucei. Cell 36:163–170
Bernards A, Van Harten-Loosbroek N, Borst P (1984b) Modification of telomeric DNA inTrypanosoma brucei; a role in antigenic variation? Nucleic Acids Res 12:4153–4169
Bernards A, Kooter JM, Borst P (1985) Structure and transcription of a telomeric surface antigen gene ofTrypanosoma brucei. Mol Cell Biol 5:545–553
Bernards A, Van der Ploeg LHT, Gibson WC, Leegwater P, Eijgenraam F, De Lange T, Weijers P, Calafat J, Borst P (1986) Rapid change of the repertoire of variant surface glycoprotein genes in trypanosomes by gene duplication and deletion. J Mol Biol 190:1–10
Boothroyd JC, Paynter CA, Coleman SL, Cross GAM (1982) Complete nucleotide sequence of complementary DNA coding for a variant surface glycoprotein fromTrypanosoma brucei. J Mol Biol 157:547–556
Borst P (1986) How proteins get into microbodies (peroxisomes, glyoxysomes, glycosomes). Biochim Biophys Acta 866:179–203
Borst P, Cross GAM (1982) Molecular basis for trypanosome antigenic variation. Cell 29:291–303
Branlant G, Branlant C (1985) Nucleotide sequence of theEscherichia coli gap gene. Different evolutionary behavior of the NAD+-binding domain and of the catalytic domain of D-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 150:61–66
Caron F, Meyer F (1985) DoesParamecium primaurelia use a different genetic code in its macronucleus? Nature 314:185–188
Clayton C (1985) Structure and regulated expression of genes encoding fructose biphosphate aldolase inTrypanosoma brucei. EMBO J 4:2997–3003
Cornelissen AWCA, Johnson PJ, Kooter JM, van der Ploeg LHT, Borst P (1985) Two simultaneously active VSG gene transcription units in a singleTrypanosoma brucei variant. Cell 41:825–832
Cully DF, Ip HS, Cross GAM (1985) Coordinate transcription of variant surface glycoprotein genes and an expression site associated gene family inTrypanosoma brucei. Cell 42:173–182
Frasch ACC, Borst P, Van den Burg J (1982) Rapid evolution of genes coding for variant surface glycoproteins in trypanosomes. Gene 17:197–211
Gibson WC, Osinga KA, Michels PAM, Borst P (1985) Trypanosomes of subgenusTrypanozoon are diploid for housekeeping genes. Mol Biochem Parasitol 16:231–242
Grantham R (1980) Workings of the genetic code. Trends Biochem Sci 5:327–331
Grosjean H, Fiers W (1982) Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene 18:199–209
Helftenbein E (1985) Nucleotide sequence of a macronuclear DNA molecule coding for α-tubulin from the ciliateStylonychia lemnae. Special codon usage: TAA is not a translation termination codon. Nucleic Acids Res 13:415–433
Horowitz S, Gorovsky MA (1985) An unusual genetic code in nuclear genes ofTetrahymena. Proc Natl Acad Sci USA 82:2452–2455
Ikemura T (1981) Correlation between the abundance ofEscherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for theE. coli translational system. J Mol Biol 151:389–409
Ikemura T (1983) Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. J Mol Biol 158:573–597
Kimmel BE, Samson S, Wu J, Hirschberg R, Yarbrough LR (1985) Tubulin genes of the African trypanosomeTrypanosoma brucei rhodesiense: nucleotide sequence of a 3.7-kb fragment containing genes for alpha and beta tubulins. Gene 35:237–248
Labuda D, Grosjean H, Striker G, Porschke D (1982) Codon: anticodon and anticodon: anticodon interaction. Evaluation of equilibrium and kinetic parameters of complexes involving a G:U wobble. Biochim Biophys Acta 698:230–236
Massamba NN, Williams RO (1984) Distinction of African trypanosome species using nucleic acid hybridization. Parasitology 88:55–65
McLaughlin PJ, Dayhoff MO (1973) Eukaryote evolution: a view based on cytochrome c sequence data. J Mol Evol 2:99–116
Michels PAM, Poliszczak A, Osinga KA, Misset O, Van Beeumen J, Wierenga RK, Borst P, Opperdoes FR (1986) Two tandemly-linked identical genes code for the glycosomal glyceraldehyde-phosphate dehydrogenase inTrypanosoma brucei. EMBO J 5:1049–1056
Michiels F, Matthyssens G, Kronenberger P, Pays E, Dero B, Van Assel S, Darville M, Cravador A, Steinert M, Hamers R (1983) Gene activation and re-expression of aTrypanosoma brucei variant surface glycoprotein. EMBO J 2:1185–1192
Misset O, Bos OJM, Opperdoes FR (1986) Glycolytic enzymes ofTrypanosoma brucei: simultaneous purification, intraglycosomal concentrations and physical properties. Eur J Biochem 157:441–453
Opperdoes FR (1984) Localization of the initial steps in alkoxyphospholipid biosynthesis in glycosomes (microbodies) ofTrypanosoma brucei. FEBS Lett 169:35–39
Opperdoes FR (1985) Biochemical peculiarities of trypanosomes, African and South American. Br Med Bull 41:130–136
Opperdoes FR, Baudhuin P, Coppens I, De Roe C, Edwards SW, Weijers PJ, Misset O (1984) Purification, morphometric analysis and characterization of the glycosomes (microbodies) of the protozoan hemoflagellateTrypanosoma brucei. J Cell Biol 98:1178–1184
Opperdoes FR, Borst P (1977) Localization of nine glycolytic enzymes in a microbody-like organelle inTrypanosoma brucei: the glycosome. FEBS Lett 80:360–364
Osinga KA, Swinkels BW, Gibson WC, Borst P, Veeneman GH, Van Boom JH, Michels PAM, Opperdoes FR (1985) Topogenesis of microbody enzymes: a sequence comparison of the genes for the glycosomal (microbody) and cytosolic phosphoglycerate kinases ofTrypanosoma brucei. EMBO J 4:3811–3817
Paindavoine P, Pays P, Laurent M, Geltmeyer Y, Le Ray D, Mechlitz D, Steinert M (1986) The use of DNA hybridization and numerical taxonomy in determining relationships betweenTrypanosoma brucei stocks and subspecies. Parasitology 92:31–50
Pays E, Dekerck P, Van Assel S, Babiker EE, Le Ray D, Van Meirvenne N, Steinert M (1983a) Comparative analysis of aTrypanosoma brucei gambiense antigen gene family and its potential use in epidemiology of sleeping sickness. Mol Biochem Parasitol 7:63–74
Pays E, Delauw MF, Van Assel S, Laurent M, Vervoort T (1983b) Modifications of aTrypanosoma brucei brucei antigen gene repertoire by different DNA recombinational mechanisms. Cell 35:721–731
Pays E, Delauw MF, Laurent M, Steinert M (1984) Possible DNA modification in GC dinucleotides ofTrypanosoma brucei telomeric sequences; relationship with antigen gene transcription. Nucleic Acids Res 12:5235–5247
Pettigrew GW (1972) The amino acid sequence of cytochrome c from a protozoanCrithidia oncopelti. FEBS Lett 22:64–66
Preer JR Jr, Preer LB, Rudman BM, Barnett AJ (1985) Deviation from the universal code shown by the gene for surface protein 51A inParamecium. Nature 314:188–190
Rice-Ficht AC, Chen KK, Donelson JE (1982) Point mutations during generation of expression-linked extra copy of trypanosome surface glycoprotein gene. Nature 298:676–679
Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83:1383–1387
Swinkels BW, Gibson WC, Osinga KA, Kramer R, Veeneman GH, Van Boom JH, Borst P (1986) Characterization of the gene for the microbody (glycosomal) triosephosphate isomerase ofTrypanosoma brucei. EMBO J 5:1291–1298
Tschudi C, Young AS, Ruben L, Patton CL, Richards FF (1985) Calmodulin genes in trypanosomes are tandemly repeated and produce multiple mRNAs with a common 5′ leader sequence. Proc Natl Acad Sci USA 82:3998–4002
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Michels, P.A.M. Evolutionary aspects of trypanosomes: Analysis of genes. J Mol Evol 24, 45–52 (1986). https://doi.org/10.1007/BF02099950
Issue Date:
DOI: https://doi.org/10.1007/BF02099950