Comparative analysis of the ribosomal components of the hydrogenosome-containing protist, Trichomonas vaginalis

Journal of Molecular Evolution

Volumn 59, Issue 1, 2004, Pages 59-71

  Arisue, Nobuko ^a,e   Maki, Yasushi ^b,f   Yoshida, Hideji ^b   Wada, Akira ^b   Sánchez, Lidya B ^c,g   Müller, Miklós ^c   Hashimoto, Tetsuo ^a,c,d  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b OSAKA MEDICAL COLLEGE   (Japan)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f NIIGATA UNIVERSITY   (Japan)

^g PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Ribosomal protein; Ribosome; rRNA; Sedimentation coefficient; Trichomonas vaginalis

Indexed keywords

RIBOSOME PROTEIN; RIBOSOME RNA;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; EUKARYOTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; RIBOSOME; SACCHAROMYCES CEREVISIAE; SEDIMENTATION; TRICHOMONAS VAGINALIS;

AMINO ACID SEQUENCE; ANIMALS; BASE PAIRING; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; DNA PRIMERS; DNA, RIBOSOMAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EVOLUTION, MOLECULAR; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; RIBOSOMAL PROTEINS; SEQUENCE ANALYSIS, DNA; TRICHOMONAS VAGINALIS;

ARCHEZOA; ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA; PROTISTA; PROTOZOA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; TRICHOMONADIDA; TRICHOMONAS VAGINALIS;

EID: 3042806889     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Adachi J, Hasegawa M (1996) Computer science monographs, No. 28, MOLPHY version 2.3: programs for molecular phylogenetics based on maximum likelihood. Institute of Statistical Mathematics, Tokyo
2. Arisue N, Hashimoto T, Lee JA, Moore DV, Gordon P, Sensen CW, Gaasterland T, Hasegawa M, Müller M (2002) The phylogenetic position of the pelobiont Mastigamoeba balamuthi based on sequences of rDNA and translation elongation factors EF-1α and EF-2. J Eukaryot Microbiol 49:1-10
3. Bapteste E, Brinkmann H, Lee JA, Moore DV, Sensen CW, Gordon P, Duruflé L, Gaasterland T, Lopez P, Müller M, Philippe H (2002) The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc Natl Acad Sci USA 99:1414-1419
4. Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature 326:332-333
5. Cavalier-Smith T (1993) Kingdom protozoa and its 18 phyla. Microbiol Rev 57:953-994
6. Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Sys Evol Microbiol 52:297-354
7. Chaires JB, Kegeles G (1977) Sucrose density gradient sedimentation of E. coli ribosomes. Biophys Chem 7:173-178
8. Chakrabarti D, Dame JB, Gutell RR, Yowell , CA (1992) Characterization of the rDNA unit and sequence analysis of the small subunit rRNA and 5.8S rRNA genes from Tritrichomonas foetus. Mol Biochem Parasitol 52:75-83
9. Champney WS, Chittum HS, Samuels R (1992) Ribosomes from trichomonad protozoa have prokaryotic characteristics. Int J Biochem 24:1125-1133
10. Chen X, Wu R (1997) Direct amplification of unknown genes and fragments by uneven polymerase chein reaction. Gene 185:195-199
11. Cook RT, Rock RC, Aikawa M, Fournier MJ Jr (1971) Ribosomes of the malarial parasite, Plasmodium knowlesi. I. Isolation, activity and sedimentation velocity. Comp Biochem Physiol B 39:897-911
12. DeRijk P, Gatehouse HS, DeWachter R (1998) The secondary structure of Nosema apis large subunit ribosomal RNA. Biochim Biophys Acta 1442:326-328
13. DeRijk P, Robbrecht E, DeHoog S, Caers A, Van de Peer Y, DeWachter R (1999) Database on the structure of large subunit ribosomal RNA. Nucleic Acids Res 27:174-178
14. Dequard-Chablat M, Coppin-Raynal E, Picard-Bennoun M, Madjar JJ (1986) At least seven ribosomal proteins are involved in the control of translational accuracy in a eukaryotic organism. J Mol Biol 190:167-175
15. Diamond LS (1957) The establishment of various Trichomonads of animals and man in axenic cultures. J Parasitol 43:488-490
16. Edlind TD, Li J, Visvesvara GS, Vodkin MH, McLaughlin GL, Katiyar SK (1996) Phylogenetic analysis of β-tubulin sequences from amitochondrial protozoa. Mol Phylogenet Evol 5:359-367
17. Embley TM, Hirt RP (1998) Early branching eukaryotes? Curr Opin Genet Dev 8:624-629
18. Embley TM, van der Giezen M, Horner DS, Dyal PL, Foster P (2003) Hydrogenosomes and mitochondria are two forms of the same fundamental organelle. Phil Trans R Soc Lond 358:191-201
19. Felsenstein J (2002) PHYLIP (phylogeny inference package). Version 3.6a. Distributed by the author. University of Washington, Seattle
20. Fleming GH, Boynton JE, Gillham NW (1987) Cytoplasmic ribosomal proteins from Chlamydomonas reinhardtii: Characterization and immunological comparisons. Mol Gen Genet 206:226-237
21. Germot A, Philippe H, Le Guyader H (1997) Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol Biochem Parasitol 87:159-168
22. Gutell RR (1993) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res 21:3051-3054
23. Guthrie C, Fink GR (eds) (1991) Methods in enzymology, Vol 194: Guide to yeast genetics and molecular biology. Academic Press, San Diego
24. Hardy SJS, Kurland CG, Voynow P, Mora G (1969) Extraction of ribosomal proteins with acetic acid. Biochemstry 8:2897-2905
25. Hartskeerl RA, Schuitema ARJ, de Wachter R (1993) Secondary structure of the small subunit ribosomal RNA sequence of the microsporidium Encephalitozoon cuniculi. Nucleic Acids Res 21:1489
26. Hashimoto T, Nakamura Y, Kamaishi T, Hasegawa M (1997) Early evolution of eukaryotes inferred from protein phylogenies of translation elongation factors 1α and 2. Arch Protistenkd 48:287-295
27. Hashimoto T, Sanchéz LB, Shirakura T, Müller M, Hasegawa M (1998) Secondary absence of mitochondria in Giardia lamblia and Trichommonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci USA 95:6868-6865
28. Henze K, Horner DS, Suguri S, Moore DV, Sánchez LB, Müller M, Embley TM (2001) Unique phylogenetic relationships of glucokinase and glucosephosphate isomerase of the amitochondriate eukaryotes Giardia intestinalis, Spironucleus barkhanus and Trichomonas vaginalis. Gene 281:123-131
29. Hinkle G, Leipe DD, Nerad TA, Sogin ML (1994) The unusually long small subunit ribosomal RNA of Phreatamoeba balamuthi. Nucleic Acids Res 22:465-469
30. Hirt RP, Logsdon JM Jr, Healy B, Dorey MW, Doolittle WF, Embley TM (1999) Microsporidia are related to Fungi: Evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci USA 96:580-585
31. Horie K, Wada A, Fukutome H (1981) Conformational studies of Escherichia coli ribosomes with the use of acridine orange as a probe. J Biochem 90:449-461
32. Horner DS, Embley TM (2001) Chaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes. Mol Biol Evol 18:1970-1975
33. Ishihara R, Hayashi Y (1968) Some properties of ribosomes from the sporoplasm of Nosema bombycis. J Invertebr Pathol 11:377-385
34. Iwabuchi M, Ochiai H (1969) Sedimentation properties of ribosomal particles in Dictyostelium discoideum. Biochim Biophys Acta 190:211-213
35. Keeling PJ, Doolittle WF (1996) Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol Biol Evol 13:1297-1305
36. Keeling PJ, Palmer JD (2000) Phylogeny: Parabasalian flagellates are ancient eukaryotes. Nature 405:635-637
37. Keeling PJ, Luker MA, Palmer JD (2000) Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol Biol Evol 17:23-31
38. Keister DB (1983) Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77:487-488
39. + of Hexamita inflata and the quest of the first branch in the eukaryotic tree. Mol Biochem Parasitol 59:41-48
40. Mager WH, Planta RJ, Ballesta JG, Lee JC, Mizuta K, Suzuki K, Warner JR, Woolford J (1997) A new nomenclature for the cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Nucleic Acids Res 25:4872-4875
41. McArthur AG, Morrison HG, Nixon JE, Passamaneck NQ, Kim U, Hinkle G, Crocker MK, Holder ME, Farr R, Reich CI, Olsen GE, Aley SB, Adam RD, Gillin FD, Sogin ML (2000) The Giardia genome project database. FEMS Microbiol Lett 189:271-273
42. Michel S, Traut RR, Lee JC (1983) Yeast ribosomal proteins: Electrophoretic analysis in four two-dimensional gel systems - Correlation of nomenclatures. Mol Gen Genet 191:251-256
43. Mizumoto K, Iwasaki K, Tanaka M, Kaziro Y (1974) Studies on polypeptide elongation factor 2 from pig liver. I. Purification and properties. J Biochem 75:104-1056
44. Müller M (1988) Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol 42:465-488
45. Müller M (1993) The hydrogenosome. J Gen Microbiol 139:2879-2889
46. Neefs JM, Van de Peer Y, DeRijk P, Chapelle S, DeWachter R (1993) Compilation of small ribosomal subunit RNA structures. Nucleic Acids Res 21:3025-3049
47. Nieuwenhuysen P, Clauwaert J (1981) Physicochemical characterization of ribosomal particles from the eukaryote Anemia. J Biol Chem 256:9626-9632
48. Oka Y, Hayashi H, Hayashi N, Furuya M, Ito Y, Yagyu M, Osaki H (1973) Comparative studies on the isolation of ribosomes in Trichomonas foetus. Jpn J Parasitol 22:193-198 (in Japanese with an English abstract)
49. Patel VB, Cunningham CC, Hantgan RR (2001) Physiochemical properties of rat liver mitochondrial ribosomes. J Biol Chem 276:6739-6746
50. Petridou B, Cuny M, Guerin MF, Hayes F (1983) Ribosomal subunits and ribosomal proteins of Tetrahymena thermophila. Effect of the presence of iodoacetamide during ribosome extraction on the properties of the subunits. Eur J Biochem 135:425-434
51. Peyretaillade E, Biderre C, Peyret P, Duffieux F, Metenier G, Gouy M, Michot B, Vivares CP (1998) Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res 26:3513-3520
52. Philippe H, Laurent J (1998) How good are deep phylogenetic trees? Curr Opin Genet Dev 8:616-623
53. Philippe H, Lopez P, Brinkmann H, Budin K, Germot A, Laurent J, Moreira D, Müller M, Le Guyader H (2000) Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc R Soc Lond B Biol Sci 267:1213-1221
54. Ramagopal S, Ennis HL (1980) Studies on ribosomal proteins in the cellular slime mold Dictyostelium discoideum. Resolution, nomenclature and molecular weights of proteins in the 40-S and 60-S ribosomal subunits. Nucleic Acids Res 25:4872-4875
55. Roger AJ (1999) Reconstructing early events in eukaryotic evolution. Am Nat 154:S146-S163
56. Roger AJ, Morrison HG, Sogin ML (1999) Primary structure and phylogenetic relationships of a malate dehydrogenase gene from Giardia lamblia. J Mol Evol 48:750-755
57. Rotte C, Henze K, Müller M, Martin W (2000) Origins of hydrogenosomes and mitochondria. Curr Opin Microbiol 3:481-486
58. Sambrook J, Fritch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
59. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114-1116
60. Shirakura T, Maki Y, Yoshida H, Arisue N, Wada A, Sánchez LB, Nakamura F, Müller M, Hashimoto T (2001) Characterization of the ribosomal proteins of the amitochondriate protist, Giardia lamblia. Mol Biochem Parasitol 112:153-156
61. Sogin ML, Silberman JD (1998) Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int J Parasitol 28:11-20
62. Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA (1989) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75-77
63. Tovar J, Leon-Avila G, Sánchez LB, Sutak R, Tachezy J, van der Giezen M, Hernández M, Müller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron-sulfur protein maturation. Nature 426:172-176
64. Van de Peer Y, Ben Ali A, Meyer A (2000a) Microsporidia: Accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. Gene 246:1-8
65. Van de Peer Y, Baldauf SL, Doolittle WF, Meyer A (2000b) An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51:565-576
66. Van Keulen H, Gutell RR, Campbell SR, Erlandsen SL, Jarroll EL (1992) The nucleotide sequence of the entire ribosomal DNA operon and the structure of the large subunit rRNA of Giardia muris. J. Mol Evol 35:318-328
67. Vivarès VP, Gouy M, Thomarat F, Méténier G (2002) Functional and evolutionary analysis of a eukaryotic parasitic genome. Curr Opin Microbiol 5:499-505
68. Vossbrinck CR, Woose CR (1986) Eukaryotic ribosomes that lack a 5.8 RNA. Nature 320:287-288
69. Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrinck BA, Woese CR (1987) Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326:411-414
70. Wada A (1986a) Analysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. I. Detection of four new proteins. J Biochem 100:1583-1594
71. Wada A (1986b) Analysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. II. Detection of four new proteins. J Biochem 100:1595-1605
72. Williams BAP, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865-869
73. Wool IG, Chan YL, Gluck A (1995) Structure and evolution of mammalian ribosomal proteins. Biochem Cell Biol 73:933-947
74. Wu G, Hashimoto T (1999) Sequence analysis of genes encoding ribosomal proteins of amitochondriate protists: L1 of Trichomonas vaginalis and L29 of Giardia lamblia. Parasitol Int 48:135-134
75. Wuyts J, De Rijk P, Van de Peer Y, Winkelmans T, De Wachter R (2001) The European large subunit ribosomal RNA database. Nucleic Acids Res 29:175-177
76. Wuyts J, Van de Peer Y, Winkelmans T, De Wachter R (2002) The European database on small subunit ribosomal RNA. Nucleic Acids Res 30:183-185
77. Yang Z (1997) PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555-556
78. Zasloff M, Ochoa S (1971) A supernatant factor involved in initiation of complex formation with eukaryotic ribosomes. Proc Natl Acad Sci USA 65:3059-3063
79. Zuker M (1989) On finding all suboptimal foldings of an RNA molecules. Science 244:48-52