Skip to main content
Log in

Horizontal Gene Transfer in Aminoacyl-tRNA Synthetases Including Leucine-Specific Subtypes

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

Abstract

Aminoacyl-tRNA synthetases catalyze a fundamental reaction for the flow of genetic information from RNA to protein. Their presence in all organisms known today highlights their important role in the early evolution of life. We investigated the evolutionary history of aminoacyl-tRNA synthetases on the basis of sequence data from more than 200 Archaea, Bacteria, and Eukaryota. Phylogenetic profiles are in agreement with previous observations that many genes for aminoacyl-tRNA synthetases were transferred horizontally between species from all domains of life. We extended these findings by a detailed analysis of the history of leucyl-tRNA synthetases. Thereby, we identified a previously undetected case of horizontal gene transfer from Bacteria to Archaea based on phylogenetic profiles, trees, and networks. This means that, finally, the last subfamily of aminoacyl-tRNA synthetases has lost its exceptional position as the sole subfamily that is devoid of horizontal gene transfer. Furthermore, the leucyl-tRNA synthetase phylogenetic tree suggests a dichotomy of the archaeal/eukaryotic-cytosolic and bacterial/eukaryotic-mitochondrial proteins. We argue that the traditional division of life into Prokaryota (non-chimeric) and Eukaryota (chimeric) is favorable compared to Woese’s trichotomy into Archaea/Bacteria/Eukaryota.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  PubMed  CAS  Google Scholar 

  • Baldauf SL, Palmer JD, Doolittle WF (1996) The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. Proc Natl Acad Sci USA 93:7749–7754

    Article  PubMed  CAS  Google Scholar 

  • Berg P (1961) Specificity in protein synthesis. Annu Rev Biochem 30:293–322

    Article  CAS  Google Scholar 

  • Blair JE, Ikeo K, Gojobori T, Hedges SB (2002) The evolutionary position of nematodes. BMC Evol Biol 2:7

    Article  PubMed  Google Scholar 

  • Brinkmann H, Martin W (1996) Higher-plant chloroplast and cytosolic 3-phosphoglycerate kinases: a case of endosymbiotic gene replacement. Plant Mol Biol 30:65–75

    Article  PubMed  CAS  Google Scholar 

  • Brochier C, Bapteste E, Moreira D, Philippe H (2002) Eubacterial phylogeny based on translational apparatus proteins. Trends Genet 18:1–5

    Article  PubMed  CAS  Google Scholar 

  • Brown JR, Doolittle WF (1995) Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc Natl Acad Sci USA 92:2441–2445

    Article  PubMed  CAS  Google Scholar 

  • Brown JR, Robb FT, Weiss R, Doolittle WF (1997) Evidence for the early divergence of tryptophanyl- and tyrosyl-tRNA synthetases. J Mol Evol 45:9–16

    Article  PubMed  CAS  Google Scholar 

  • Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265

    Article  PubMed  CAS  Google Scholar 

  • Carter CW Jr (1993) Cognition, mechanism, and evolutionary relationships in aminoacyl–tRNA synthetases. Annu Rev Biochem 62:715–748

    Article  PubMed  CAS  Google Scholar 

  • Cusack S, Yaremchuk A, Tukalo M (2000) The 2 A crystal structure of leucyl-tRNA synthetase and its complex with a leucyl-adenylate analogue. EMBO J 19:2351–2361

    Article  PubMed  CAS  Google Scholar 

  • Doolittle RF, Handy J (1998) Evolutionary anomalies among the aminoacyl–tRNA synthetases. Curr Opin Genet Dev 8:630–636

    Article  PubMed  CAS  Google Scholar 

  • Farahi K, Pusch GD, Overbeek R, Whitman WB (2004) Detection of lateral gene transfer events in the prokaryotic tRNA synthetases by the ratios of evolutionary distances method. J Mol Evol 58:615–631

    Article  PubMed  CAS  Google Scholar 

  • Francklyn C, Perona JJ, Puetz J, Hou YM (2002) Aminoacyl-tRNA synthetases: versatile players in the changing theater of translation. RNA 8:1363–1372

    Article  PubMed  CAS  Google Scholar 

  • Fukunaga R, Yokoyama S (2005) Crystal structure of leucyl-tRNA synthetase from the archaeon Pyrococcus horikoshii reveals a novel editing domain orientation. J Mol Biol 346:57–71

    Article  PubMed  CAS  Google Scholar 

  • Gogarten JP, Kibak H, Dittrich P, et al. (1989) Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci USA 86:6661–6665

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS, Golding GB (1996) The origin of the eukaryotic cell. Trends Biochem Sci 21:166–171

    Article  PubMed  CAS  Google Scholar 

  • Huson DH (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73

    Article  PubMed  CAS  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267

    Article  PubMed  CAS  Google Scholar 

  • Hutter H, Vogel BE, Plenefisch JD, Norris CR, Proenca RB, Spieth J, Guo C, Mastwal S, Zhu X, Scheel J, Hedgecock EM (2000) Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science 287:989–994

    Article  PubMed  CAS  Google Scholar 

  • Itoh T, Martin W, Nei M (2002) Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci USA 99:12944–12948

    Article  PubMed  CAS  Google Scholar 

  • Iwabe N, Kuma K, Hasegawa M, Osawa S, Miyata T (1989) Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci USA 86:9355–9359

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ, Doolittle WF (1997) Evidence that eukaryotic triosephosphate isomerase is of alpha-proteobacterial origin. Proc Natl Acad Sci USA 94:1270–1275

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245

    Article  PubMed  CAS  Google Scholar 

  • Lake JA, Rivera MC (2004) Deriving the genomic tree of life in the presence of horizontal gene transfer: conditioned reconstruction. Mol Biol Evol 21:681–690

    Article  PubMed  CAS  Google Scholar 

  • Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New Haven, CT

    Google Scholar 

  • Martin W, Brinkmann H, Savonna C, Cerff R (1993) Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90:8692–8696

    Article  PubMed  CAS  Google Scholar 

  • Mayr E (1998) Two empires or three? Proc Natl Acad Sci USA 95:9720–9723

    Article  PubMed  CAS  Google Scholar 

  • O’Donoghue P, Luthey-Schulten Z (2003) On the evolution of structure in aminoacyl-tRNA synthetases. Microbiol Mol Biol Rev 67:550–573

    Article  PubMed  CAS  Google Scholar 

  • Rivera MC, Jain R, Moore JE, Lake JA (1998) Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci USA 95:6239–6244

    Article  PubMed  CAS  Google Scholar 

  • Rivera MC, Lake JA (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257:74–76

    Article  PubMed  CAS  Google Scholar 

  • Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:255–274

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  PubMed  CAS  Google Scholar 

  • Schneller JM, Schneller C, Martin R, Stahl AJ (1976) Nuclear origin of specific yeast mitochondrial aminoacyl–tRNA synthetases. Nucleic Acids Res 3:1151–1165

    PubMed  CAS  Google Scholar 

  • Shiba K, Motegi H, Schimmel P (1997) Maintaining genetic code through adaptations of tRNA synthetases to taxonomic domains. Trends Biochem Sci 22:453–457

    Article  PubMed  CAS  Google Scholar 

  • Snel B, Bork P, Huynen MA (2002) The identification of functional modules from the genomic association of genes. Proc Natl Acad Sci USA 99:5890–5895

    Article  PubMed  CAS  Google Scholar 

  • Szymanski M, Deniziak M, Barciszewski J (2000) The new aspects of aminoacyl-tRNA synthetases. Acta Biochim Pol 47:821–834

    PubMed  CAS  Google Scholar 

  • Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Olsen GJ, Ibba M, Soll D (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Mol Biol Rev 64:202–236

    Article  PubMed  CAS  Google Scholar 

  • Wolf YI, Aravind L, Grishin NV, Koonin EV (1999) Evolution of aminoacyl-tRNA synthetases—analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res 9:689–710

    PubMed  CAS  Google Scholar 

  • Wolf YI, Rogozin IB, Grishin NV, Tatusov RL, Koonin EV (2001) Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evol Biol 1:8

    Article  PubMed  CAS  Google Scholar 

  • Zdobnov EM, von Mering C, Letunic I, Torrents D, Suyama M, Copley RR, Christophides GK, Thomasova D, Holt RA, Subramanian GM, Mueller HM, Dimopoulos G, Law JH, Wells MA, Birney E, Charlab R, Halpern AL, Kokoza E, Kraft CL, Lai Z, Lewis S, Louis C, Barillas-Mury C, Nusskern D, Rubin GM, Salzberg SL, Sutton GG, Topalis P, Wides R, Wincker P, Yandell M, Collins FH, Ribeiro J, Gelbart WM, Kafatos FC, Bork P (2002) Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298:149–159

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Hannes Luz and Thomas Meinel for discussions and helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eike Staub.

Additional information

[Reviewing Editor: Dr. Yves Van de Peer]

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dohm, J.C., Vingron, M. & Staub, E. Horizontal Gene Transfer in Aminoacyl-tRNA Synthetases Including Leucine-Specific Subtypes. J Mol Evol 63, 437–447 (2006). https://doi.org/10.1007/s00239-005-0094-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-005-0094-3

Keywords

Navigation