Synonymous codon usage variation among Giardia lamblia genes and isolates

Molecular Biology and Evolution

Volumn 16, Issue 11, 1999, Pages 1484-1495

  Lafay, Bénédicte ^a,b   Sharp, Paul M ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b STATION MARINE D ENDOUME   (France)

Author keywords

Codon usage; Diplomonads; GC36 variation; Giardia lamblia; Intraspecies heterogeneity; Translational selection

Indexed keywords

MEMBRANE ANTIGEN;

AMINO ACID ANALYSIS; AMINO ACID COMPOSITION; ARTICLE; EVOLUTION; GENE EXPRESSION; GENE ISOLATION; GENETIC VARIABILITY; GIARDIA LAMBLIA; NUCLEOTIDE SEQUENCE; UNINDEXED SEQUENCE;

GIARDIA LAMBLIA;

EID: 0032713107     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a026060     Document Type: Article

References (89)

1. ADAM, R. D. 1991. The biology of Giardia spp. Microbiol. Rev. 55:706-732.
2. ADAM, R. D., A. AGGARWAL, A. A. LAL, V. F. DE LA CRUZ, T. MCCUTCHAN, and T. E. NASH. 1988. Antigenic variation of a cystein-rich protein in Giardia lamblia. J. Exp. Med. 167:107-118.
3. ADAM, R. D., Y. M. YANG, and T. E. NASH. 1992. The Cysrich protein gene family of Giardia lamblia: loss of the CRP170 gene in an antigenic variant. Mol. Cell. Biol. 12: 1197-1201.
4. AGGARWAL, A., R. D. ADAM, and T. E. NASH. 1989. Characterization of a 33-kilodalton structural protein of Giardia lamblia and localization to the ventral disk. Infect. Immun. 57:1305-1310.
5. AKASHI, H. 1997. Codon usage bias evolution in Drosophila. Population genetics of mutation-selection drift. Gene 205: 269-278.
6. ALTSCHUL, S. F., T. L. MADDEN, A. A. SCHAFFER, J. ZHANG, Z. ZHANG, W. MILLER, and D. J. LIPMAN. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res. 25:3389-3402.
7. ANDERS, R. F., D. J. MCCOLL, and R. L. COPPEL. 1993. Molecular variation in Plasmodium falciparum: polymorphic antigens of asexual erythrocytic stages. Acta Trop. 53:239-253.
8. ANDREWS, R. H., M. ADAMS, P. F. L. BOREHAM, G. MAYRHOFER, and B. P. MELONI. 1989. Giardia intestinalis: electrophoretic evidence for a species complex. Int. J. Parasitol. 19:183-190.
9. BAKER, D. A., D. V. HOLBERTON, and J. MARSHALL. 1988. Sequence of a giardin subunit cDNA from Giardia lamblia. Nucleic Acids Res. 16:7177.
10. BARUCH, A. C., J. ISAAC-RENTON, and R. D. ADAM. 1996. The molecular epidemiology of Giardia lamblia: a sequence-based approach. J. Infect. Dis. 174:233-236.
11. BERNARDI, G., B. OLOFSSON, J. FILIPSKI, M. ZERIAL, J. SALINAS, G. CUNY, M. MEUNIER-ROTIVAL, and E RODIER. 1985. The mosaic genome of warm-blooded vertebrates. Science 228:953-958.
12. BOOTHROYD, J. C., A. WANG, D. A. CAMPBELL, and C. C. WANG. 1987. An unusually compact ribosomal DNA repeat in the protozoan Giardia lamblia. Nucleic Acids Res. 15: 4065-4084.
13. BRUDERER, T., P. PAPANASTASIOU, R. CASTRO, and P. KOHLER. 1993. Variant cysteine-rich surface proteins of Giardia isolates from human and animal sources. Infect. Immun. 61: 2937-3944.
14. BULMER, M. 1987. Coevolution of codon usage and transfer tRNA abundance. Nature 325:728-730.
15. _. 1990. The effect of context on synonymous codon usage in genes with low codon usage bias. Nucleic Acids Res. 18:2869-2873.
16. _. 1991. The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897-907.
17. CAVALIER-SMITH, T. 1987. Eukaryotes with no mitochondria. Nature 326:332-333.
18. CAZZULO, J. J., and A. C. FRASCH. 1992. SAPA/trans-sialidase and cruzipain: two antigens from Trypanosoma cruzi contain immunodominant but enzymatically inactive domains. FASEB J. 6:3259-3264.
19. CHAR, S., and M. J. G. FARTHING. 1992. Codon usage in Giardia lamblia. J. Protozool. 39:642-643.
20. CHEN, N., J. A. UPCROFT, and P. UPCROFT. 1995. A Giardia duodenalis gene encoding a protein with multiple repeats of a toxin homolog. Parasitology 111:423-431.
21. _. 1996. A new cysteine-rich protein-encoding gene family in Giardia duodenalis. Gene 169:33-38.
22. CHIAPELLO, H., F. LISACEK, M. CABOCHE, and A. HENAULT. 1998. Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene 209:GC1-GC38.
23. CLARK, C. G., and A. J. ROGER. 1995. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 92:6518-6521.
24. CLAYTON, C., J. FUERI, and M. MOWATT. 1991. The procyclic surface of protein of Trypanosoma brucei. Pp. 55-63 in C. C. WANG, ed. Molecular and immunological aspects of parasitism. American Association for the Advancement of Science, Washington, D.C.
25. COLLINS, J. F., and A. F. W. COULSON. 1990. Significance of protein sequence similarities. Pp. 474-487 in R. F. DOOLITTLE, ed. Molecular evolution: computer analysis of protein and nucleic acid sequences. Academic Press, San Diego.
26. DONG, H., L. NILSSON, and C. G. KURLAND. 1996. Co-variation of the tRNA abundance and codon usage in Escherichia coli at different growth rates. J. Mol. Biol. 260:649-663.
27. DROUIN, G., M. MONIZ DE SÁ, and M. ZUKER. 1995. The Giardia lamblia actin gene and the phylogeny of eukaryotes. J. Mol. Evol. 41:841-849.
28. EY, P. L., R. H. ANDREWS, and G. MAYRHOFER. 1993. Differentiation of major genotypes of Giardia intestinalis by polymerase chain reaction analysis of a gene encoding a trophozoite surface antigen. Parasitology 106:347-356.
29. EY, P. L., T. BRUDERER, C. WEHRLI, and P. KÖHLER. 1996. Comparison of genetic groups determined by molecular and immunological analyses of Giardia isolated from animals and humans in Switzerland and Australia. Parasitol. Res. 82:52-60.
30. EY, P. L., J. M. DARBY, R. H. ANDREWS, and G. MAYRHOFER. 1993. Giardia intestinalis: detection of major genotypes by restriction analysis of gene amplification products. Int. J. Parasitol. 23:591-600.
31. EY, P. L., K. KHANNA, R. H. ANDREWS, P. A. MANNING, and G. MAYRHOFER. 1992. Distinct genetic groups of Giardia intestinalis distinguished by restriction fragment length polymorphisms. J. Gen. Microbiol. 138:2629-2637.
32. EY, P. L., M. MANSOURI, J. V. KULDA, E. NOHÝNKOVÁ, P. T. MONIS, R. H. ANDREWS, and G. MAYRHOFER. 1997. Genetic analysis of Giardia from hoofed farm animals reveals artiodactyl-specific and potentially zoonotic genotypes. J. Eukaryot. Microbiol. 44:626-635.
33. EYRE-WALKER, A. C. 1991. An analysis of codon usage in mammals: selection or mutation bias? J. Mol. Evol. 33:442-449.
34. GERMOT, A., H. PHILIPPE, and H. LE GUYADER. 1996. Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc. Natl. Acad. Sci. USA 93: 14614-14617.
35. _. 1997. Evidence for loss of mitochondria in microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol. Biol. Parasitol. 87:159-168.
36. GILLIN, F. D., D. S. REINER, and J. M. MCCAFFERY. 1996. Cell biology of the primitive eukaryote Giardia lamblia. Annu. Rev. Microbiol. 50:679-705.
37. GOUY, M., C. GAUTIER, M. ATTIMONELLI, C. LANAVE, and G. DI PAOLA. 1985. ACNUC - a portable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. CABIOS 1:167-172.
38. GREENACRE, M. J. 1984. Theory and applications of correspondence analysis. Academic Press, London.
39. GUPTA, R. S., K. AITKEN, M. FALAH, and B. SINGH. 1994. Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 91:2895-2899.
40. HASHIMOTO, T., and M. HASEGAWA. 1996. Origin and early evolution of eukaryotes inferred from the amino acid sequences of translation elongation factors 1-alpha/Tu and 2/ G. Adv. Biophys. 32:73-120.
41. HASHIMOTO, T., Y. NAKAMURA, F. NAKAMURA, T. SHIRAKURA, J. ADACHI, N. GOTO, K.-I. OKAMOTO, and M. HASEGAWA. 1994. Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol. Biol. Evol. 11:65-71.
42. HASHIMOTO, T., L. B. SÁNCHEZ, T. SHIRAKURA, M. MÜLLER, and M. HASEGAWA. 1998. Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc. Natl. Acad. Sci. USA 95:6860-6865.
43. HOMAN, W. L., F. H. VAM ENCKEVORT, L. LIMPER, G. J. J. M. VAN EYS, G. J. SCHOONE, W. KASPRZAK, A. C. MAJEWSKA, and F. VAN KNAPEN. 1992. Comparison of Giardia isolates from different laboratories by isoenzyme analysis and DNA probes. Parasitol. Res. 78:316-323.
44. IKEMURA, T. 1981. Correlation between the abundance of Escherichia 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 the E. coli translational system. J. Mol. Biol. 151:389-409.
45. KABNICK, K. S., and D. A. PEATTIE. 1990. In situ analyses reveal that the two nuclei of Giardia lamblia are equivalent. J. Cell Sci. 95:353-360.
46. KEELING, P. J., and W. F. DOOLITTLE. 1997. Widespread and ancient distribution of a noncanonical genetic code in diplomonads. Mol. Biol. Evol. 14:895-901.
47. LEIPE, D. D., J. H. GUNDERSON, T. A. NERAD, and M. L. SOGIN. 1993. Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch of the eukaryotic tree. Mol. Biochem. Parasitol. 59:41-48.
48. LI, W.-H. 1987. Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J. Mol. Evol. 24:337-345.
49. _. 1993. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36:96-99.
50. LI, W.-H., T. TANIMURA, and P. M. SHARP. 1987. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J. Mol. Evol. 25:330-342.
51. LLOYD, A. T., and P. M. SHARP. 1992. CODONS: a microcomputer program for codon usage analysis. J. Hered. 83:239-240.
52. MAYRHOFER, G., R. H. ANDREWS, P. L. EY, and N. B. CHILTON. 1995. Division of Giardia isolates from human into two genetically distinct assemblages by electrophoretic analysis of enzymes encoded at 27 loci and comparison with Giardia muris. Parasitology 111:11-17.
53. MONIS, P. T., R. H. ANDREWS, G. MAYRHOFER, J. MACKRILL, J. KULDA, J. L. ISAAC-RENTON, and P. L. EY. 1998. Novel lineages of Giardia intestinalis identified by genetic analysis of organisms isolated from dogs in Australia. Parasitology 116:7-9.
54. MONIS, P. T., G. MAYRHOFER, R. H. ANDREWS, W. L. HOMAN, L. LIMPER, and P. L. EY. 1996. Molecular genetic analysis of Giardia intestinalis isolates at the glutamate dehydrogenase locus. Parasitology 112:1-12.
55. MOWATT, M. R., B.-Y. T. NGUYEN, J. T. CONRAD, R. D. ADAM, and T. E. NASH. 1994. Size heterogeneity among antigenically related Giardia lamblia variant-specific surface proteins is due to differences in tandem repeat copy number. Infect. Immun. 62:1213-1218.
56. MURRAY, P. J., and T. W. SPITHILL. 1991. Variants of a Leishmania surface antigen derived from a multigenic family. J. Biol. Chem. 266:24477-24484.
57. MURTAGH, J. J., M. R. MOWATT, C.-M. LEE, F.-J. S. LEE, K. MISHIMA, T. E. NASH, J. Moss, and M. VAUGHAN. 1992. Guanine nucleotide-binding proteins in the intestinal parasite Giardia lamblia. J. Biol. Chem. 267:9654-9662.
58. NASH, T. E. 1992. Surface antigen variability and variation in Giardia lamblia. Parasitol. Today 8:229-234.
59. NASH, T. E., S. M. BANKS, D. W. ALLING, J. W. J. MERRITT, and J. T. CONRAD. 1990. Frequency of variant antigens in Giardia lamblia. Exp. Parasitol. 71:415-421.
60. NASH, T. E., T. MCCUTCHAN, D. KEISTER, J. B. DAME, J. D. CONRAD, and F. D. GILLIN. 1985. Restriction-endonuclease analysis of DNA from 15 Giardia isolates obtained from humans and animals. J. Infect. Dis. 59:1334-1340.
61. NUSSINOV, R. 1981. Eukaryotic dinucleotide preference rules and their implications for degenerate codon usage. J. Mol. Biol. 149:125-131.
62. _. 1984. Doublet frequencies in evolutionary distinct groups. Nucleic Acids Res. 12:1749-1763.
63. PEATTIE, D. A. 1990. The giardins of Giardia lamblia: genes and proteins with a promise. Parasitol. Today 6:52-56.
64. PEATTIE, D. A., R. A. ALONSO, A. HEIN, and J. P. CAULFIELD. 1989. Ultrastructural localization of giardins to the edges of disk microribbons of Giardia lamblia and the nucleotide and deduced protein sequence of alpha giardin. J. Cell Biol. 109:2323-2335.
65. POWELL, J. R., and E. N. MORIYAMA. 1997. Evolution of codon usage bias in Drosophila. Proc. Natl. Acad. Sci. USA 94: 7784-7790.
66. ROGER, A. J., C. G. CLARK, and W. F. DOOLITTLE. 1996. A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc. Natl. Acad. Sci. USA 93:14618-14622.
67. ROGER, A. J., S. G. SVARD, J. TOVAR, C. G. CLARK, M. W. SMITH, F. D. GILLIN, and M. L. SOGIN. 1998. A mitochondrial-like chaperonin 60 in Giardia lamblia: evidence that diplomomads once harbored an endosymbiont related to the progenitor of mitochondria. Proc. Natl. Acad. Sci. USA 95: 229-234.
68. SABEUR, G., G. MACAYA, F. KADI, and G. BERNARDI. 1993. The isochore patterns of mammalian genomes and their phylogenetic implications. J. Mol. Evol. 37:93-108.
69. SHARP, P. M. 1991. Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J. Mol. Evol. 33:23-33.
70. SHARP, P. M., M. AVEROF, A. T. LLOYD, G. MATASSI, and J. F. PEDEN. 1995. DNA sequence evolution: the sounds of silence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 349:241-247.
71. SHARP, P. M., and K. M. DEVINE. 1989. Codon usage and gene expression in Dictyostelium discoideum: highly expressed genes do 'prefer' optimal codons. Nucleic Acids Res. 17: 5029-5039.
72. SHARP, P. M., and W.-H. LI. 1986a. Codon usage in regulatory genes in Escherichia coli does not reflect selection for "rare" codons. Nucleic Acids Res. 14:7737-7749.
73. _. 1986b. An evolutionary perspective on synonymous codon usage in unicellular organisms. J. Mol. Evol. 24:28-38.
74. _. 1989. On the rate of DNA sequence evolution in Drosophila. J. Mol. Evol. 28:398-402.
75. SHARP, P. M., M. STENICO, J. F. PEDEN, and A. T. LLOYD. 1993. Codon usage: mutational bias, translational selection, or both? Biochem. Soc. Trans. 21:835-841.
76. SHIELDS, D. C. 1990. Switches in species-specific codon preferences: the influence of mutation biases. J. Mol. Evol. 31: 71-80.
77. SHIELDS, D. C., P. M. SHARP, D. G. HIGGINS, and F. WRIGHT. 1988. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol. Biol. Evol. 5:704-716.
78. SOGIN, M. L., J. H. GUNDERSON, H. J. ELWOOD, R. A. ALONSO, and D. A. PEATTIE. 1989. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75-77.
79. STANLEY, S. L. J., A. BECKER, C. KUNZ-JENKINS, L. FOSTER, and E. LI. 1990. Cloning and expression of a membrane antigen of Entamoeba histolytica possessing multiple tandem repeats. Proc. Natl. Acad. Sci. USA 87:4976-4980.
80. STENICO, M., A. T. LLOYD, and P. M. SHARP. 1994. Codon usage in Caenorhabditis elegans: delineation of translation selection and mutational biases. Nucleic Acids Res. 22: 2437-2446.
81. STILLER, J. W., and B. D. HALL. 1998. The origin of red algae: implications for plastid evolution. Proc. Natl. Acad. Sci. USA 94:4520-4525.
82. SWARBRICK, A., R. L. H. LIM, J. A. UPCROFT, and T. S. STEWART. 1997. Nucleotide variation in the cytidine triphosphate synthetase gene of Giardia duodenalis. J. Eukaryot. Microbiol. 44:531-534.
83. THOMPSON, R. C. A., J. A. REYNOLDSON, and A. J. LYMBERY. 1993. Giardia - from molecules to disease and beyond. Parasitol. Today 9:313-315.
84. UPCROFT, J. A., P. F. L. BOREHAM, R. W. CAMPBELL, R. W. SHEPHERD, and P. UPCROFT. 1995. Biological and genetic analysis of a longitudinal collection of Giardia samples derived from humans. Acta Trop. 60:35-46.
85. UPCROFT, J. A., A. HEALEY, R. MITCHELL, P. F. L. BOREHAM, and P. UPCROFT. 1990. Antigen expression from the ribosomal DNA repeat unit of Giardia intestinalis. Nucleic Acids Res. 18:7077-7081.
86. UPCROFT, P., N. CHEN, and J. A. UPCROFT. 1997. Telomeric organization of a variable and inducible toxin gene family in the ancient eukaryote Giardia duodenalis. Genome Res. 7:37-46.
87. VAN KEULEN, H., W. L. HOMAN, S. L. ERLANDSEN, and E. L. JARROLL. 1995. A three nucleotide signature sequence in small-subunit ribosomal RNA divides human Giardia in two different genotypes. J. Eukaryot. Microbiol. 42:392-394.
88. VANHAMME, L., and E. PAYS. 1995. Control of gene expession in trypanosomes. Microbiol. Rev. 59:223-240.
89. WRIGHT, F. 1990. The 'effective number of codons' used in a gene. Gene 87:23-29.