Skip to main content
SpringerLink
Log in

Comparative Analysis of the Ribosomal Componentsof the Hydrogenosome-Containing Protist, Trichomonas vaginalis

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The ribosomes of the amitochondriate but hydrogenosome-containing protist lineage, the trichomonads, have previously been reported to be prokaryotic or primitive eukaryotic, based on evidence that they have a 70S sedimentation coefficient and a small number of proteins, similar to prokaryotic ribosomes. In order to determine whether the components of the trichomonad ribosome indeed differ from those of typical eukaryotic ribosomes, the ribosome of a representative trichomonad, Trichomonas vaginalis, was characterized. The sedimentation coefficient of the T. vaginalis ribosome was smaller than that of Saccharomyces cerevisiae and larger than that of Escherichia coli. Based on two-dimensional PAGE analysis, the number of different ribosomal proteins was estimated to be approximately 80. This number is the same as those obtained for typical eukaryotes (approximately 80) but larger than that of E. coli (approximately 55). N-Terminal amino acid sequencing of 18 protein spots and the complete sequences of 4 ribosomal proteins as deduced from their genes revealed these sequences to display typical eukaryotic features. Phylogenetic analyses of the five ribosomal proteins currently available also clearly confirmed that the T. vaginalis sequences are positioned within a eukaryotic clade. Comparison of deduced secondary structure models of the small and large subunit rRNAs of T. vaginalis with those of other eukaryotes revealed that all helices commonly found in typical eukaryotes are present and conserved in T. vaginalis, while variable regions are shortened or lost. These lines of evidence demonstrate that the T. vaginalis ribosome has no prokaryotic or primitive eukaryotic features but is clearly a typical eukaryotic type.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • J Adachi M Hasegawa (1996) Computer science monographs, No. 28, MOLPHY version 2.3: programs for molecular phylogenetics based on maximum likelihood Institute of Statistical Mathematics Tokyo

    Google Scholar 

  • N Arisue T Hashimoto JA Lee DV Moore P Gordon CW Sensen T Gaasterland M Hasegawa M Müller (2002) ArticleTitleThe 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 Occurrence Handle1:CAS:528:DC%2BD38Xis1eqsrw%3D Occurrence Handle11908892

    CAS  PubMed  Google Scholar 

  • E Bapteste H Brinkmann JA Lee DV Moore CW Sensen P Gordon L Duruflé T Gaasterland P Lopez M Müller H Philippe (2002) ArticleTitleThe analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba Proc Natl Acad Sci USA 99 1414–1419 Occurrence Handle10.1073/pnas.032662799 Occurrence Handle1:CAS:528:DC%2BD38Xht1Cls7c%3D Occurrence Handle11830664

    Article  CAS  PubMed  Google Scholar 

  • T Cavalier-Smith (1987) ArticleTitleEukaryotes with no mitochondria Nature 326 332–333 Occurrence Handle10.1038/326332a0 Occurrence Handle1:STN:280:BiiC2s3pslE%3D Occurrence Handle3561476

    Article  CAS  PubMed  Google Scholar 

  • T Cavalier-Smith (1993) ArticleTitleKingdom protozoa and its 18 phyla Microbiol Rev 57 953–994 Occurrence Handle1:STN:280:ByuC3szps1M%3D Occurrence Handle8302218

    CAS  PubMed  Google Scholar 

  • T Cavalier-Smith (2002) ArticleTitleThe phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa Int J Sys Evol Microbiol 52 297–354 Occurrence Handle1:STN:280:DC%2BD387pvVekug%3D%3D

    CAS  Google Scholar 

  • JB Chaires G Kegeles (1977) ArticleTitleSucrose density gradient sedimentation of E. coli ribosomes Biophys Chem 7 173–178 Occurrence Handle10.1016/0301-4622(77)87019-1 Occurrence Handle1:CAS:528:DyaE1cXhvVWj Occurrence Handle334275

    Article  CAS  PubMed  Google Scholar 

  • D Chakrabarti JB Dame RR Gutell CA Yowell (1992) ArticleTitleCharacterization 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 Occurrence Handle10.1016/0166-6851(92)90037-K Occurrence Handle1:CAS:528:DyaK38XkvVCnt74%3D Occurrence Handle1625709

    Article  CAS  PubMed  Google Scholar 

  • WS Champney HS Chittum R Samuels (1992) ArticleTitleRibosomes from trichomonad protozoa have prokaryotic characteristics Int J Biochem 24 1125–1133 Occurrence Handle10.1016/0020-711X(92)90383-C Occurrence Handle1:CAS:528:DyaK38XksVChs7o%3D Occurrence Handle1397506

    Article  CAS  PubMed  Google Scholar 

  • X Chen R Wu (1997) ArticleTitleDirect amplification of unknown genes and fragments by uneven polymerase chein reaction Gene 185 195–199 Occurrence Handle10.1016/S0378-1119(96)00637-3 Occurrence Handle1:CAS:528:DyaK2sXktFSiuw%3D%3D Occurrence Handle9055815

    Article  CAS  PubMed  Google Scholar 

  • RT Cook RC Rock M Aikawa MJ Fournier SuffixJr (1971) ArticleTitleRibosomes of the malarial parasite, Plasmodium knowlesi. I. Isolation, activity and sedimentation velocity Comp Biochem Physiol B 39 897–911 Occurrence Handle10.1016/0305-0491(71)90113-1 Occurrence Handle1:CAS:528:DyaE3MXltVGjsrY%3D Occurrence Handle5002363

    Article  CAS  PubMed  Google Scholar 

  • P Rijk ParticleDe HS Gatehouse R Wachter ParticleDe (1998) ArticleTitleThe secondary structure of Nosema apis large subunit ribosomal RNA Biochim Biophys Acta 1442 326–328 Occurrence Handle9804982

    PubMed  Google Scholar 

  • P Rijk ParticleDe E Robbrecht S Hoog ParticleDe A Caers Y Peer ParticleVan de R Wachter ParticleDe (1999) ArticleTitleDatabase on the structure of large subunit ribosomal RNA Nucleic Acids Res 27 174–178 Occurrence Handle10.1093/nar/27.1.174 Occurrence Handle9847172

    Article  PubMed  Google Scholar 

  • M Dequard-Chablat E Coppin-Raynal M Picard-Bennoun JJ Madjar (1986) ArticleTitleAt least seven ribosomal proteins are involved in the control of translational accuracy in a eukaryotic organism J Mol Biol 190 167–175 Occurrence Handle1:CAS:528:DyaL28XltFWrsrY%3D Occurrence Handle3795267

    CAS  PubMed  Google Scholar 

  • LS Diamond (1957) ArticleTitleThe establishment of various Trichomonads of animals and man in axenic cultures J Parasitol 43 488–490 Occurrence Handle1:STN:280:CyeD3cnjsF0%3D

    CAS  Google Scholar 

  • TD Edlind J Li GS Visvesvara MH Vodkin GL McLaughlin SK Katiyar (1996) ArticleTitlePhylogenetic analysis of β-tubulin sequences from amitochondrial protozoa Mol Phylogenet Evol 5 359–367 Occurrence Handle10.1006/mpev.1996.0031 Occurrence Handle1:CAS:528:DyaK28XjtVCkurc%3D Occurrence Handle8728394

    Article  CAS  PubMed  Google Scholar 

  • TM Embley RP Hirt (1998) ArticleTitleEarly branching eukaryotes? Curr Opin Genet Dev 8 624–629 Occurrence Handle10.1016/S0959-437X(98)80029-4 Occurrence Handle1:CAS:528:DyaK1MXhs1yjtQ%3D%3D Occurrence Handle9914207

    Article  CAS  PubMed  Google Scholar 

  • TM Embley M Giezen Particlevan der DS Horner PL Dyal P Foster (2003) ArticleTitleHydrogenosomes and mitochondria are two forms of the same fundamental organelle Phil Trans R Soc Lond 358 191–201 Occurrence Handle10.1098/rstb.2002.1190 Occurrence Handle1:CAS:528:DC%2BD3sXktVWhs74%3D

    Article  CAS  Google Scholar 

  • J Felsenstein (2002) PHYLIP (phylogeny inference package). Version 3.6a. Distributed by the author University of Washington Seattle

    Google Scholar 

  • GH Fleming JE Boynton NW Gillham (1987) ArticleTitleCytoplasmic ribosomal proteins from Chlamydomonas reinhardtii: Characterization and immunological comparisons Mol Gen Genet 206 226–237 Occurrence Handle1:CAS:528:DyaL2sXhslamuro%3D Occurrence Handle3295482

    CAS  PubMed  Google Scholar 

  • A Germot H Philippe H Le Guyader (1997) ArticleTitleEvidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae Mol Biochem Parasitol 87 159–168 Occurrence Handle10.1016/S0166-6851(97)00064-9 Occurrence Handle1:CAS:528:DyaK2sXkvFalurY%3D Occurrence Handle9247927

    Article  CAS  PubMed  Google Scholar 

  • RR Gutell (1993) ArticleTitleCollection of small subunit (16S- and 16S-like) ribosomal RNA structures Nucleic Acids Res 21 3051–3054 Occurrence Handle1:CAS:528:DyaK3sXkvV2itL8%3D Occurrence Handle8332526

    CAS  PubMed  Google Scholar 

  • C Guthrie GR Fink (Eds) (1991) Methods in enzymology, Vol 194: Guide to yeast genetics and molecular biology Academic Press San Diego

    Google Scholar 

  • SJS Hardy CG Kurland P Voynow G Mora (1969) ArticleTitleExtraction of ribosomal proteins with acetic acid Biochemstry 8 2897–2905 Occurrence Handle1:CAS:528:DyaF1MXksFKksLs%3D

    CAS  Google Scholar 

  • RA Hartskeerl ARJ Schuitema R Wachter Particlede (1993) ArticleTitleSecondary structure of the small subunit ribosomal RNA sequence of the microsporidium Encephalitozoon cuniculi Nucleic Acids Res 21 1489 Occurrence Handle1:CAS:528:DyaK3sXit1ynsb8%3D Occurrence Handle8464742

    CAS  PubMed  Google Scholar 

  • T Hashimoto Y Nakamura T Kamaishi M Hasegawa (1997) ArticleTitleEarly evolution of eukaryotes inferred from protein phylogenies of translation elongation factors 1α and 2 Arch Protistenkd 48 287–295

    Google Scholar 

  • T Hashimoto LB Sanchéz T Shirakura M Müller M Hasegawa (1998) ArticleTitleSecondary absence of mitochondria in Giardia lamblia and Trichommonas vaginalis revealed by valyl-tRNA synthetase phylogeny Proc Natl Acad Sci USA 95 6868–6865

    Google Scholar 

  • K Henze DS Horner S Suguri DV Moore LB Sánchez M Müller TM Embley (2001) ArticleTitleUnique phylogenetic relationships of glucokinase and glucosephosphate isomerase of the amitochondriate eukaryotes Giardia intestinalis, Spironucleus barkhanus and Trichomonas vaginalis Gene 281 123–131 Occurrence Handle10.1016/S0378-1119(01)00773-9 Occurrence Handle1:CAS:528:DC%2BD3MXptFelsbw%3D Occurrence Handle11750134

    Article  CAS  PubMed  Google Scholar 

  • G Hinkle DD Leipe TA Nerad ML Sogin (1994) ArticleTitleThe unusually long small subunit ribosomal RNA of Phreatamoeba balamuthi Nucleic Acids Res 22 465–469 Occurrence Handle1:CAS:528:DyaK2cXitlOgur0%3D Occurrence Handle8127686

    CAS  PubMed  Google Scholar 

  • RP Hirt JM Logsdon SuffixJr B Healy MW Dorey WF Doolittle TM Embley (1999) ArticleTitleMicrosporidia are related to Fungi: Evidence from the largest subunit of RNA polymerase II and other proteins Proc Natl Acad Sci USA 96 580–585 Occurrence Handle10.1073/pnas.96.2.580 Occurrence Handle1:CAS:528:DyaK1MXmtlClsQ%3D%3D Occurrence Handle9892676

    Article  CAS  PubMed  Google Scholar 

  • K Horie A Wada H Fukutome (1981) ArticleTitleConformational studies of Escherichia coli ribosomes with the use of acridine orange as a probe J Biochem 90 449–461 Occurrence Handle1:CAS:528:DyaL3MXltFSgur4%3D Occurrence Handle6170632

    CAS  PubMed  Google Scholar 

  • DS Horner TM Embley (2001) ArticleTitleChaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes Mol Biol Evol 18 1970–1975 Occurrence Handle1:CAS:528:DC%2BD3MXns1WhsrY%3D Occurrence Handle11557802

    CAS  PubMed  Google Scholar 

  • R Ishihara Y Hayashi (1968) ArticleTitleSome properties of ribosomes from the sporoplasm of Nosema bombycis J Invertebr Pathol 11 377–385 Occurrence Handle1:CAS:528:DyaF1MXhtVar

    CAS  Google Scholar 

  • M Iwabuchi H Ochiai (1969) ArticleTitleSedimentation properties of ribosomal particles in Dictyostelium discoideum Biochim Biophys Acta 190 211–213 Occurrence Handle10.1016/0005-2787(69)90170-1 Occurrence Handle1:CAS:528:DyaF1MXltF2ls74%3D Occurrence Handle5387784

    Article  CAS  PubMed  Google Scholar 

  • PJ Keeling WF Doolittle (1996) ArticleTitleAlpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family Mol Biol Evol 13 1297–1305 Occurrence Handle1:CAS:528:DyaK28XnsVWhsLc%3D Occurrence Handle8952074

    CAS  PubMed  Google Scholar 

  • PJ Keeling JD Palmer (2000) ArticleTitlePhylogeny: Parabasalian flagellates are ancient eukaryotes Nature 405 635–637 Occurrence Handle10.1038/35015167 Occurrence Handle1:CAS:528:DC%2BD3cXktlCju7Y%3D

    Article  CAS  Google Scholar 

  • PJ Keeling MA Luker JD Palmer (2000) ArticleTitleEvidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi Mol Biol Evol 17 23–31 Occurrence Handle1:CAS:528:DC%2BD3cXotF2qtw%3D%3D Occurrence Handle10666703

    CAS  PubMed  Google Scholar 

  • DB Keister (1983) ArticleTitleAxenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile Trans R Soc Trop Med Hyg 77 487–488 Occurrence Handle10.1016/0035-9203(83)90120-7 Occurrence Handle1:STN:280:BiuD2cnhtFc%3D Occurrence Handle6636276

    Article  CAS  PubMed  Google Scholar 

  • DD Leipe JH Gunderson TA Nerad ML Sogin (1993) ArticleTitleSmall subunit ribosomal RNA+ of Hexamita inflata and the quest of the first branch in the eukaryotic tree Mol Biochem Parasitol 59 41–48 Occurrence Handle10.1016/0166-6851(93)90005-I Occurrence Handle1:CAS:528:DyaK3sXksVGjs7w%3D Occurrence Handle8515782

    Article  CAS  PubMed  Google Scholar 

  • WH Mager RJ Planta JG Ballesta JC Lee K Mizuta K Suzuki JR Warner J Woolford (1997) ArticleTitleA new nomenclature for the cytoplasmic ribosomal proteins of Saccharomyces cerevisiae Nucleic Acids Res 25 4872–4875 Occurrence Handle10.1093/nar/25.24.4872 Occurrence Handle1:CAS:528:DyaK1cXntFyntA%3D%3D Occurrence Handle9396790

    Article  CAS  PubMed  Google Scholar 

  • AG McArthur HG Morrison JE Nixon NQ Passamaneck U Kim G Hinkle MK Crocker ME Holder R Farr CI Reich GE Olsen SB Aley RD Adam FD Gillin ML Sogin (2000) ArticleTitleThe Giardia genome project database FEMS Microbiol Lett 189 271–273 Occurrence Handle10.1016/S0378-1097(00)00299-8 Occurrence Handle1:CAS:528:DC%2BD3cXltlWhsbw%3D Occurrence Handle10930750

    Article  CAS  PubMed  Google Scholar 

  • S Michel RR Traut JC Lee (1983) ArticleTitleYeast ribosomal proteins: Electrophoretic analysis in four two-dimensional gel systems—Correlation of nomenclatures Mol Gen Genet 191 251–256 Occurrence Handle1:CAS:528:DyaL3sXltlGrsLs%3D

    CAS  Google Scholar 

  • K Mizumoto K Iwasaki M Tanaka Y Kaziro (1974) ArticleTitleStudies on polypeptide elongation factor 2 from pig liver. I. Purification and properties J Biochem 75 104–1056

    Google Scholar 

  • M Müller (1988) ArticleTitleEnergy metabolism of protozoa without mitochondria Annu Rev Microbiol 42 465–488 Occurrence Handle10.1146/annurev.mi.42.100188.002341 Occurrence Handle3059999

    Article  PubMed  Google Scholar 

  • M Müller (1993) ArticleTitleThe hydrogenosome J Gen Microbiol 139 2879–2889 Occurrence Handle8126416

    PubMed  Google Scholar 

  • JM Neefs Y Peer ParticleVan de P Rijk ParticleDe S Chapelle R Wachter ParticleDe (1993) ArticleTitleCompilation of small ribosomal subunit RNA structures Nucleic Acids Res 21 3025–3049 Occurrence Handle1:CAS:528:DyaK3sXkvV2itL4%3D Occurrence Handle8332525

    CAS  PubMed  Google Scholar 

  • P Nieuwenhuysen J Clauwaert (1981) ArticleTitlePhysicochemical characterization of ribosomal particles from the eukaryote Anemia J Biol Chem 256 9626–9632 Occurrence Handle1:CAS:528:DyaL3MXlsVGktrk%3D Occurrence Handle7026555

    CAS  PubMed  Google Scholar 

  • Y Oka H Hayashi N Hayashi M Furuya Y Ito M Yagyu H Osaki (1973) ArticleTitleComparative studies on the isolation of ribosomes in Trichomonas foetus Jpn J Parasitol 22 193–198 Occurrence Handle1:CAS:528:DyaE2cXhsVaktrw%3D

    CAS  Google Scholar 

  • VB Patel CC Cunningham RR Hantgan (2001) ArticleTitlePhysiochemical properties of rat liver mitochondrial ribosomes J Biol Chem 276 6739–6746 Occurrence Handle10.1074/jbc.M005781200 Occurrence Handle1:CAS:528:DC%2BD3MXhslSgsr8%3D Occurrence Handle11106644

    Article  CAS  PubMed  Google Scholar 

  • B Petridou M Cuny MF Guerin F Hayes (1983) ArticleTitleRibosomal 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 Occurrence Handle1:CAS:528:DyaL3sXlsFCisL0%3D Occurrence Handle6617641

    CAS  PubMed  Google Scholar 

  • E Peyretaillade C Biderre P Peyret F Duffieux G Metenier M Gouy B Michot CP Vivares (1998) ArticleTitleMicrosporidian 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 Occurrence Handle10.1093/nar/26.15.3513 Occurrence Handle1:CAS:528:DyaK1cXltlKqtrw%3D Occurrence Handle9671812

    Article  CAS  PubMed  Google Scholar 

  • H Philippe J Laurent (1998) ArticleTitleHow good are deep phylogenetic trees? Curr Opin Genet Dev 8 616–623 Occurrence Handle10.1016/S0959-437X(98)80028-2 Occurrence Handle1:CAS:528:DyaK1MXhs1yjtA%3D%3D Occurrence Handle9914208

    Article  CAS  PubMed  Google Scholar 

  • H Philippe P Lopez H Brinkmann K Budin A Germot J Laurent D Moreira M Müller H Le Guyader (2000) ArticleTitleEarly-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions Proc R Soc Lond B Biol Sci 267 1213–1221 Occurrence Handle10.1098/rspb.2000.1130 Occurrence Handle1:CAS:528:DC%2BD3cXlsFyqtLo%3D Occurrence Handle10902687

    Article  CAS  PubMed  Google Scholar 

  • S Ramagopal HL Ennis (1980) ArticleTitleStudies 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

    Google Scholar 

  • AJ Roger (1999) ArticleTitleReconstructing early events in eukaryotic evolution Am Nat 154 S146–S163 Occurrence Handle10.1086/303290 Occurrence Handle10527924

    Article  PubMed  Google Scholar 

  • AJ Roger HG Morrison ML Sogin (1999) ArticleTitlePrimary structure and phylogenetic relationships of a malate dehydrogenase gene from Giardia lamblia J Mol Evol 48 750–755 Occurrence Handle1:CAS:528:DyaK1MXkt1ynurY%3D Occurrence Handle10229579

    CAS  PubMed  Google Scholar 

  • C Rotte K Henze M Müller W Martin (2000) ArticleTitleOrigins of hydrogenosomes and mitochondria Curr Opin Microbiol 3 481–486 Occurrence Handle10.1016/S1369-5274(00)00126-0 Occurrence Handle1:CAS:528:DC%2BD3cXotVOitL0%3D Occurrence Handle11050446

    Article  CAS  PubMed  Google Scholar 

  • J Sambrook J EF Fritch T Maniatis (1989) Molecular cloning: A laboratory manual EditionNumber2 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  • H Shimodaira M Hasegawa (1999) ArticleTitleMultiple comparisons of log-likelihoods with applications to phylogenetic inference Mol Biol Evol 16 1114–1116 Occurrence Handle1:CAS:528:DyaK1MXltVyksrg%3D

    CAS  Google Scholar 

  • T Shirakura Y Maki H Yoshida N Arisue A Wada LB Sánchez F Nakamura M Müller T Hashimoto (2001) ArticleTitleCharacterization of the ribosomal proteins of the amitochondriate protist, Giardia lamblia Mol Biochem Parasitol 112 153–156 Occurrence Handle10.1016/S0166-6851(00)00356-X Occurrence Handle1:CAS:528:DC%2BD3MXps1Sjsw%3D%3D Occurrence Handle11166398

    Article  CAS  PubMed  Google Scholar 

  • ML Sogin JD Silberman (1998) ArticleTitleEvolution of the protists and protistan parasites from the perspective of molecular systematics Int J Parasitol 28 11–20 Occurrence Handle10.1016/S0020-7519(97)00181-1 Occurrence Handle1:STN:280:DyaK1c7mt1ymtA%3D%3D Occurrence Handle9504331

    Article  CAS  PubMed  Google Scholar 

  • ML Sogin JH Gunderson HJ Elwood RA Alonso DA Peattie (1989) ArticleTitlePhylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia Science 243 75–77 Occurrence Handle1:CAS:528:DyaL1MXhtFShurs%3D Occurrence Handle2911720

    CAS  PubMed  Google Scholar 

  • J Tovar G Leon-Avila LB Sánchez R Sutak J Tachezy M Giezen Particlevan der M Hernández M Müller JM Lucocq (2003) ArticleTitleMitochondrial remnant organelles of Giardia function in iron-sulfur protein maturation Nature 426 172–176 Occurrence Handle10.1038/nature01945 Occurrence Handle1:CAS:528:DC%2BD3sXovVKmtLw%3D Occurrence Handle14614504

    Article  CAS  PubMed  Google Scholar 

  • Y Peer ParticleVan de A Ben Ali A Meyer (2000a) ArticleTitleMicrosporidia: Accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi Gene 246 1–8 Occurrence Handle10.1016/S0378-1119(00)00063-9

    Article  Google Scholar 

  • Y Peer ParticleVan de SL Baldauf WF Doolittle A Meyer (2000b) ArticleTitleAn updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances J Mol Evol 51 565–576

    Google Scholar 

  • H Keulen ParticleVan RR Gutell SR Campbell SL Erlandsen EL Jarroll (1992) ArticleTitleThe 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 Occurrence Handle1404417

    PubMed  Google Scholar 

  • VP Vivarès M Gouy F Thomarat G Méténier (2002) ArticleTitleFunctional and evolutionary analysis of a eukaryotic parasitic genome Curr Opin Microbiol 5 499–505 Occurrence Handle10.1016/S1369-5274(02)00356-9 Occurrence Handle1:CAS:528:DC%2BD38Xnt1Ggu7w%3D Occurrence Handle12354558

    Article  CAS  PubMed  Google Scholar 

  • CR Vossbrinck CR Woose (1986) ArticleTitleEukaryotic ribosomes that lack a 5.8 RNA Nature 320 287–288 Occurrence Handle1:CAS:528:DyaL28XhsVCitLg%3D Occurrence Handle3083262

    CAS  PubMed  Google Scholar 

  • CR Vossbrinck JV Maddox S Friedman BA Debrunner-Vossbrinck CR Woese (1987) ArticleTitleRibosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes Nature 326 411–414 Occurrence Handle10.1038/326411a0 Occurrence Handle1:CAS:528:DyaL2sXktVWrsr4%3D Occurrence Handle3550472

    Article  CAS  PubMed  Google Scholar 

  • A Wada (1986a) ArticleTitleAnalysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. I. Detection of four new proteins J Biochem 100 1583–1594 Occurrence Handle1:CAS:528:DyaL2sXks1Ogtw%3D%3D

    CAS  Google Scholar 

  • A Wada (1986b) ArticleTitleAnalysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. II. Detection of four new proteins J Biochem 100 1595–1605 Occurrence Handle1:CAS:528:DyaL2sXivFSntA%3D%3D

    CAS  Google Scholar 

  • BAP Williams RP Hirt JM Lucocq TM Embley (2002) ArticleTitleA mitochondrial remnant in the microsporidian Trachipleistophora hominis Nature 418 865–869 Occurrence Handle10.1038/nature00949 Occurrence Handle1:CAS:528:DC%2BD38XmtlWlt7o%3D Occurrence Handle12192407

    Article  CAS  PubMed  Google Scholar 

  • IG Wool YL Chan A Gluck (1995) ArticleTitleStructure and evolution of mammalian ribosomal proteins Biochem Cell Biol 73 933–947 Occurrence Handle1:CAS:528:DyaK28Xit1Kks7o%3D Occurrence Handle8722009

    CAS  PubMed  Google Scholar 

  • G Wu T Hashimoto (1999) ArticleTitleSequence analysis of genes encoding ribosomal proteins of amitochondriate protists: L1 of Trichomonas vaginalis and L29 of Giardia lamblia Parasitol Int 48 135–134 Occurrence Handle10.1016/S1383-5769(99)00010-0 Occurrence Handle1:CAS:528:DyaK1MXltlylsr8%3D Occurrence Handle11269274

    Article  CAS  PubMed  Google Scholar 

  • J Wuyts P Rijk ParticleDe Y Peer ParticleVan de T Winkelmans R Wachter ParticleDe (2001) ArticleTitleThe European large subunit ribosomal RNA database Nucleic Acids Res 29 175–177 Occurrence Handle10.1093/nar/29.1.175 Occurrence Handle1:CAS:528:DC%2BD3MXjtlWmsro%3D Occurrence Handle11125083

    Article  CAS  PubMed  Google Scholar 

  • J Wuyts Y Peer ParticleVan de T Winkelmans R Wachter ParticleDe (2002) ArticleTitleThe European database on small subunit ribosomal RNA Nucleic Acids Res 30 183–185 Occurrence Handle10.1093/nar/30.1.183 Occurrence Handle1:CAS:528:DC%2BD38Xht12ktbY%3D Occurrence Handle11752288

    Article  CAS  PubMed  Google Scholar 

  • Z Yang (1997) ArticleTitlePAML: A program package for phylogenetic analysis by maximum likelihood Comput Appl Biosci 13 555–556 Occurrence Handle1:CAS:528:DyaK2sXntlGnu7s%3D Occurrence Handle9367129

    CAS  PubMed  Google Scholar 

  • M Zasloff S Ochoa (1971) ArticleTitleA supernatant factor involved in initiation of complex formation with eukaryotic ribosomes Proc Natl Acad Sci USA 65 3059–3063

    Google Scholar 

  • M Zuker (1989) ArticleTitleOn finding all suboptimal foldings of an RNA molecules Science 244 48–52 Occurrence Handle1:CAS:528:DyaL1MXkt1SnsbY%3D Occurrence Handle2468181

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Work conducted at the Hayama laboratory in Japan was carried out under an ISM Cooperative Research Program (01ISMCRP-2047) and was supported by a grant from Japan Society for the Promotion of Science to T.H. (13640709). Work carried out at the Rockefeller University was supported by Grants MCB9615659 from the National Science Foundation and AI 11942 from the National Institutes of Health, U.S. Public Health Service, to M.M. Visits by T.H. to the New York laboratory and L.B.S. to the Hayama laboratory were supported by a U.S.–Japan Cooperative Research Project from the National Science Foundation and Japan Society for the Promotion of Science (INT-9726707). The authors would like to thank Dr. T. Uchiumi for providing information regarding the isolation of the ribosomes of Artemia salina and Drs. M. Hasegawa and H. Tokimatsu for helpful discussions.

Author information

Author notes

  1. Nobuko Arisue

    Present address: Department of Molecular Protozoology, Research Institute for Microbial Disease, Osaka University, Suita, Osaka, 565-0871, Japan

  2. Yasushi Maki

    Present address: Department of Biology, Faculty of Science, Niigata University, Niigata , 950-2181, Japan

  3. Lidya B. Sánchez

    Present address: Public Health Research Institute, Newark, NJ, 07103, USA

Authors and Affiliations

  1. Department of Biosystems Science, Graduate University for Advanced Studies (Sokendai), Hayama, Kanagawa, 240-0193, Japan

    Nobuko Arisue & Tetsuo Hashimoto

  2. Department of Physics, Osaka Medical College, Takatsuki, Osaka, 569-0084, Japan

    Yasushi Maki, Hideji Yoshida & Akira Wada

  3. The Rockefeller University, 1230 York Avenue, New York, NY, 10021, USA

    Lidya B. Sánchez, Miklós Müller & Tetsuo Hashimoto

  4. Institute of Biological Sciences, University of Tsukuba, Tsukuba, 305-8572, Japan

    Tetsuo Hashimoto

Authors
  1. Nobuko Arisue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasushi Maki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hideji Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akira Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lidya B. Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Miklós Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tetsuo Hashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tetsuo Hashimoto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arisue, N., Maki, Y., Yoshida, H. et al. Comparative Analysis of the Ribosomal Componentsof the Hydrogenosome-Containing Protist, Trichomonas vaginalis . J Mol Evol 59, 59–71 (2004). https://doi.org/10.1007/s00239-004-2604-0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-2604-0

Keywords

Search

Navigation