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Presence of a Bacterial-Like Citrate Synthase Gene in Tetrahymena thermophila: Recent Lateral Gene Transfers (LGT) or Multiple Gene Losses Subsequent to a Single Ancient LGT?

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Abstract

Citrate synthase is the initial enzyme in the tricarboxylic acid cycle of mitochondria. In plants and fungi, it is the second isozyme in the glyoxylate cycle of peroxisomes (or glyoxysomes), and it is also present in bacteria. Some of the biochemical reactions in the glyoxylate cycle of the ciliated protozoan Tetrahymena pyriformis depend upon mitochondrial enzymes, as T. pyriformis lacks some glyoxysome-specific enzymes. Here we demonstrate a new citrate synthase gene from Tetrahymena thermophila that is different from the mitochondrial counterpart. A potential peroxysome-targeted signal was detected in the N-terminus, suggesting the localization of the enzyme in peroxysomes. Phylogenetic analysis placed the Tetrahymena sequence in a clade consisting of a few sequences from eukaryotes such as cellular slime molds and two land plants, near a green sulfur bacterium and many proteobacteria as a sister group but not in a mitochondrial clade. Southern blot analysis revealed that this type of gene was absent from distantly related ciliates and other species of Tetrahymena except for the closest species, T. mallaccensis. The scattered presence of the bacterial-like genes among distantly related eukaryotes suggests three alternative interpretations of acquisition of the novel glyoxysomal citrate synthase gene via lateral gene transfer (LGT). (1) Some eukaryotes independently acquired the gene from a common bacterium or closely related bacteria via LGT. (2) A hypothetical eukaryote once acquired the gene, which was thereafter independently transferred from the eukaryote to other eukaryotes. (3) A single event of LGT (or duplication) occurred in a certain common ancestor of eukaryotes, followed by multiple losses in many eukaryotic lineages during the subsequent evolution. Considering the monophyly of the bacterial-like eukaryotic citrate synthase genes, the first model is somewhat unlikely, even though it is not impossible. The second and third models can rationally explain the present observation, so these models are discused in some detail.

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References

  1. SF Altshul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 5 3389–3402 Occurrence Handle10.1093/nar/25.17.3389

    Article  Google Scholar 

  2. JO Andersson AM Sjogren LA Davis TM Embley AJ Roger (2003) ArticleTitlePhylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 21 94–104 Occurrence Handle10.1016/S0960-9822(03)00003-4

    Article  Google Scholar 

  3. JM Archibald MB Rogers M Toop K Ishida PJ Keeling (2003) ArticleTitleLateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci USA 100 7678–7683 Occurrence Handle10.1073/pnas.1230951100 Occurrence Handle1:CAS:528:DC%2BD3sXlt1Wqsrs%3D Occurrence Handle12777624

    Article  CAS  PubMed  Google Scholar 

  4. D Bhattacharya T Helmchen C Bibeau M Melkonian (1995) ArticleTitleComparisons of nuclear-encoded small-subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. Mol Biol Evol 12 415–420 Occurrence Handle1:CAS:528:DyaK2MXltF2ntb0%3D Occurrence Handle7739383

    CAS  PubMed  Google Scholar 

  5. F Bushman (2002) Lateral DNA transfer: Mechanisms and consequences. Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  6. WF Doolittle (1998) ArticleTitleYou are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14 307–311 Occurrence Handle10.1016/S0168-9525(98)01494-2 Occurrence Handle1:CAS:528:DyaK1cXlsValsbk%3D Occurrence Handle9724962

    Article  CAS  PubMed  Google Scholar 

  7. AWC Einerhand TM Voorn-Brouwer R Erdmann W-H Kunau HF Tabak (1991) ArticleTitleRegulation of transcription of the gene coding for peroxisomal 3-oxoacyl-CoA thiolase of Saccharomyces cerevisiae. Eur J Biochem 200 113–122 Occurrence Handle1:CAS:528:DyaK3MXltVOhuro%3D Occurrence Handle1715273

    CAS  PubMed  Google Scholar 

  8. JE Ellis R Williams D Cole R Cammack D Lloyd (1993) ArticleTitleElectron transport components of the parasitic protozoon Giardia lamblia. FEBS Lett 5 196–200 Occurrence Handle10.1016/0014-5793(93)81072-8

    Article  Google Scholar 

  9. Felsenstein J (2002) PHYLIP (phylogeny inference package) version 3.6. Distributed by the author.

  10. J Field B Rosenthal J Samuelson (2000) ArticleTitleEarly lateral transfer of genes encoding malic enzyme, acetyl-CoA synthetase and alcohol dehydrogenases from anaerobic prokaryotes to Entamoeba histolytica. Mol Microbiol 38 446–455 Occurrence Handle10.1046/j.1365-2958.2000.02143.x Occurrence Handle1:CAS:528:DC%2BD3cXovV2isr4%3D Occurrence Handle11069669

    Article  CAS  PubMed  Google Scholar 

  11. CR Flynn RT Mullen RN Trelease (1998) ArticleTitleMutation analyses of type 2 peroxisomal targeting signal that is capable of directing oligomeric protein import into tobacco BY-2 glyoxysomes. Plant J 16 709–720 Occurrence Handle10.1046/j.1365-313X.1998.00344.x Occurrence Handle1:CAS:528:DyaK1MXotlKmtg%3D%3D Occurrence Handle10069077

    Article  CAS  PubMed  Google Scholar 

  12. C Gietl (1990) ArticleTitleGlyoxysomal malate dehydrogenase from watermelon is synthesized with an amino-terminal transit peptide. Proc Natl Acad Sci USA 87 5773–5777 Occurrence Handle1:CAS:528:DyaK3MXhsVOg Occurrence Handle2377615

    CAS  PubMed  Google Scholar 

  13. MW Gray (1993) ArticleTitleOrigin and evolution of organelle genomes. Curr Opin Genet 3 884–890 Occurrence Handle1:CAS:528:DyaK2cXitlOisrc%3D Occurrence Handle8118213

    CAS  PubMed  Google Scholar 

  14. DG Higgins JD Thompson TJ Gibson (1996) ArticleTitleUsing CLUSTAL for multiple sequences alignments. Methods Enzymol 266 383–402 Occurrence Handle1:CAS:528:DyaK28Xltl2nt7w%3D Occurrence Handle8743695

    CAS  PubMed  Google Scholar 

  15. 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 

  16. A Kato M Hayashi H Mori M Nishimura (1995) ArticleTitleMolecular characterization of a glyoxysomal citrate synthase that is synthesized as a precursor of higher molecular mass in pumpkin. Plant Mol Biol 27 377–390 Occurrence Handle1:CAS:528:DyaK2MXkt1Kgs7k%3D Occurrence Handle7888626

    CAS  PubMed  Google Scholar 

  17. PJ Keeling JD Palmer (2001) ArticleTitleLateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase. Proc Natl Acad Sci USA 11 10745–10750 Occurrence Handle10.1073/pnas.191337098

    Article  Google Scholar 

  18. K Kitamura Y Nishimura N Kubotera Y Higuchi M Yamaguchi (2002) ArticleTitleTransient activation of the microl homeobox gene family in the sea urchin (Hemicentrotus pulcherrimus) micromere. Dev Genes Evol 212 1–10 Occurrence Handle10.1007/s00427-001-0202-3 Occurrence Handle1:CAS:528:DC%2BD38XhsFSjtbc%3D Occurrence Handle11875651

    Article  CAS  PubMed  Google Scholar 

  19. W Koller H Kindl (1977) ArticleTitleGlyoxylate cycle enzymes of the glyoxysomal membrane from cucumber cotyledons. Arch Biochem Biophys 181 236–248 Occurrence Handle1:STN:280:CSiB38%2Fks1A%3D Occurrence Handle18106

    CAS  PubMed  Google Scholar 

  20. JG Lee SP Cho HS Lee CH Lee KS Bae PJ Maeng (2000) ArticleTitleIdentification of a cryptic N-terminal signal in Saccharomyces cerevisiae peroxisomal citrate synthase that functions in both peroxisomal and mitochondrial targeting. J Biochem (Tokyo) 128 1059–1072 Occurrence Handle1:CAS:528:DC%2BD3MXoslSlsA%3D%3D

    CAS  Google Scholar 

  21. AS Lewin V Hines GM Small (1990) ArticleTitleCitrate synthase encoded by the CIT2 gene of Saccharomyces cerevisiae is peroxisomal. Mol Cell Biol 10 1399–1405 Occurrence Handle1:CAS:528:DyaK3cXhslGgurg%3D Occurrence Handle2181273

    CAS  PubMed  Google Scholar 

  22. W Martin B Stoebe V Goremykin S Hapsmann M Hasegawa KV Kowallik (1998) ArticleTitleGene transfer to the nucleus and the evolution of chloroplasts. Nature 393 162–165 Occurrence Handle1:CAS:528:DyaK1cXjt1ahsL0%3D Occurrence Handle11560168

    CAS  PubMed  Google Scholar 

  23. T Mita H Shiomi K Iwai (1966) ArticleTitleIsolation of nuclei from exponentially growing Tetrahymena pyriformis. Exp Cell Res 43 696–699 Occurrence Handle1:STN:280:CCiD1crns1U%3D Occurrence Handle5334455

    CAS  PubMed  Google Scholar 

  24. A Mukai H Endoh (1999) ArticleTitleNovel aberrant nuclear behavior in abortive conjugation of Tetrahymena thermophila: Joint selection of a meiotic product and macronucleus during nuclear selection. Genes Genet Syst 74 29–32 Occurrence Handle10.1266/ggs.74.29 Occurrence Handle1:STN:280:DC%2BD3c%2Fhs1yntA%3D%3D Occurrence Handle10549130

    Article  CAS  PubMed  Google Scholar 

  25. M Muller JF Hogg C De Duve (1968) ArticleTitleDistribution of tricarboxylic acid cycle enzymes and glyoxylate cycle enzymes between mitochondria and peroxisomes in Tetrahymena pyriformis. J Biol Chem 25 5385–5395

    Google Scholar 

  26. JE Nixon A Wang J Field HG Morrison AG McArthur ML Sogin BJ Loftus J Samuelson (2002) ArticleTitleEvidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryot Cell 1 181–190 Occurrence Handle10.1128/EC.1.2.181-190.2002 Occurrence Handle1:CAS:528:DC%2BD38XjtVOisL4%3D Occurrence Handle12455953

    Article  CAS  PubMed  Google Scholar 

  27. O Numata T Takemasa I Takagi M Hirono H Hirano J Chiba Y Watanabe (1991) ArticleTitle Tetrahymena 14-nm filament-forming protein has citrate synthase activity. Biochem Biophys Res Commun 31 1028–1034

    Google Scholar 

  28. S Ohno (1970) Evolution by gene duplication. Springer-Verlag Heidelberg–Berlin–New York

    Google Scholar 

  29. E Orias Y Lee M Wu J Quackenbush AJ Eisen ND Chilcorat PA Turkewitz (2002) ArticleTitleThe Tetrahymena Genome Project: Progress and prospects. Jpn J Protozool 35 IssueIDSuppl 77

    Google Scholar 

  30. JR Jr Preer LB Preer B Rudman A Barnett (1987) ArticleTitleMolecular biology of the genes for immobilization antigens in Paramecium. J Protozool 34 418–423 Occurrence Handle1:CAS:528:DyaL1cXht1yh Occurrence Handle3323480

    CAS  PubMed  Google Scholar 

  31. S Remington G Wiegand R Huber (1982) ArticleTitleCrystallographic refinement and atomic models of two different forms of citrate synthase at 2.7 and 1.7 Å resolution. J Mol Biol 15 111–152

    Google Scholar 

  32. AJ Roger SG Svard J Tover CG Clark MW Smith FD Gillin ML Sogin (1998) ArticleTitleA mitochondtial-like chaperonin 60 gene in Giardia lamblia: Evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci USA 95 229–234 Occurrence Handle1:CAS:528:DyaK1cXjtl2jtw%3D%3D Occurrence Handle9419358

    CAS  PubMed  Google Scholar 

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  1. Department of Biology, Faculty of Science, Kanazawa University, Kanazawa 920-1192, Japan

    Atsushi Mukai & Hiroshi Endoh

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  1. Atsushi Mukai
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  2. Hiroshi Endoh
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Correspondence to Atsushi Mukai.

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Mukai, A., Endoh, H. Presence of a Bacterial-Like Citrate Synthase Gene in Tetrahymena thermophila: Recent Lateral Gene Transfers (LGT) or Multiple Gene Losses Subsequent to a Single Ancient LGT? . J Mol Evol 58, 540–549 (2004). https://doi.org/10.1007/s00239-003-2576-5

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