Origins of Life and Evolution of Biospheres

, Volume 41, Issue 6, pp 621–632 | Cite as

Molecular Evolution of Aminoacyl tRNA Synthetase Proteins in the Early History of Life

Article

Abstract

Aminoacyl-tRNA synthetases (aaRS) consist of several families of functionally conserved proteins essential for translation and protein synthesis. Like nearly all components of the translation machinery, most aaRS families are universally distributed across cellular life, being inherited from the time of the Last Universal Common Ancestor (LUCA). However, unlike the rest of the translation machinery, aaRS have undergone numerous ancient horizontal gene transfers, with several independent events detected between domains, and some possibly involving lineages diverging before the time of LUCA. These transfers reveal the complexity of molecular evolution at this early time, and the chimeric nature of genomes within cells that gave rise to the major domains. Additionally, given the role of these protein families in defining the amino acids used for protein synthesis, sequence reconstruction of their pre-LUCA ancestors can reveal the evolutionary processes at work in the origin of the genetic code. In particular, sequence reconstructions of the paralog ancestors of isoleucyl- and valyl- RS provide strong empirical evidence that at least for this divergence, the genetic code did not co-evolve with the aaRSs; rather, both amino acids were already part of the genetic code before their cognate aaRSs diverged from their common ancestor. The implications of this observation for the early evolution of RNA-directed protein biosynthesis are discussed.

Keywords

Aminoacyl-tRNA synthetase Paralog Genetic code LUCA Horizontal gene transfer 

References

  1. Andam CP, Gogarten JP (2011a) Biased gene transfer in microbial evolution.Google Scholar
  2. Andam CP, Gogarten JP (2011b) Biased gene transfer and its implications for the concept of lineage. Biol Direct 23:47CrossRefGoogle Scholar
  3. Andam CP, Williams D, Gogarten JP (2010) Biased gene transfer mimics patterns created through shared ancestry. Proc Natl Acad Sci USA 107:10679–10684PubMedCrossRefGoogle Scholar
  4. Andam CP, Fournier GP, Gogarten JP (2011) Multilevel populations and the evolution of antibiotic resistance through horizontal gene transfer. FEMS Microbiol Rev 35(5):756–767PubMedCrossRefGoogle Scholar
  5. Benner SA, Sassi SO, Gaucher EA (2007) Molecular paleoscience: systems biology from the past. Adv Enzymol Relat Areas Mol Biol 75:1–132PubMedGoogle Scholar
  6. Bilokapic S, Maier T, Ahel D, Gruic-Sovulj I, Söll D, Weygand-Durasevic I, Ban N (2006) Structure of the unusual seryl-tRNA synthetase reveals a distinct zinc-dependent mode of substrate recognition. EMBO J 25:2498–2509PubMedCrossRefGoogle Scholar
  7. Cusack S, Yaremchuk A, Tukalo M (2000) The 2 Å crystal structure of leucyl-tRNA synthetase and its complex with a leucyl-adenylate analogue. EMBO J 19(10):2351–2361PubMedCrossRefGoogle Scholar
  8. Dutheil J, Gaillard S, Bazin E, Glemin S, Ranwez V, Galtier N, Belkhir K (2006) Bio++: a set of C++ libraries for sequence analysis phylogenies, molecular evolution and population genetics. BMC Bioinforma 7:188CrossRefGoogle Scholar
  9. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113CrossRefGoogle Scholar
  10. Erives A (2011) A Model of Proto-Anti-Codon RNA Enzymes Requiring L:-Amino Acid Homochirality. J Mol Evol. Jul 22. [Epub ahead of print]Google Scholar
  11. Fischer JD, Holliday GL, Rahman SA, Thornton JM (2010) The structures and physiochemical properties of organic cofactors in biocatalysis. J Mol Biol 403(5):803–824PubMedCrossRefGoogle Scholar
  12. Fournier GP, Huang J, Gogarten JP (2009) Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life. Philos Trans R Soc Lond B Biol Sci 364:2229–2239PubMedCrossRefGoogle Scholar
  13. Fukai S, Nureki O, Sekine SI, Shimada A, Vassylyev DG, Yokoyama S (2003) Mechanism of molecular interactions for tRNA(Val) recognition by valyl-tRNA synthetase. RNA 9:100–111PubMedCrossRefGoogle Scholar
  14. Gogarten JP, Fournier GP, Zhaxybayeva O (2008) Gene Transfer and the Reconstruction of Life’s Early History from Genomic Data. Space Science Reviews 135:115–131CrossRefGoogle Scholar
  15. Grosjean H, Benne R (1998) Modification and Editing of RNA. ASM press, Washington DC, USAGoogle Scholar
  16. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Nucleic Acids Res 33:W557–W559CrossRefGoogle Scholar
  17. Hanson-Smith V, Kolaczkowski B, Thornton JW (2010) Robustness of ancestral sequence reconstruction to phylogenetic uncertainty. Mol Biol Evol 27(9):1988–1999PubMedCrossRefGoogle Scholar
  18. Ibba M, Celic I, Curnow A, Kim H, Pelaschier J, Tumbula D, Vothknecht U, Woese C, Söll D (1997) Aminoacyl-tRNA synthesis in Archaea. Nucleic Acids Symp Ser 37:305–306PubMedGoogle Scholar
  19. Ikeuchi Y, Kimura S, Numata T, Nakamura D, Yokogawa T, Ogata T, Wada T, Suzuki T, Suzuki T (2010) Agmatine-conjungated cytidine in a tRNA anticodon is essential for AUA decoding in archaea. Nat Chem Biol 6(4):277–282PubMedCrossRefGoogle Scholar
  20. Kim HS, Vothknecht UC, Hedderich R, Celic I, Söll D (1998) Sequence divergence of seryl-tRNA synthetases in archaea. J Bacteriol 180:6446–6449PubMedGoogle Scholar
  21. Knight RD, Freeland SJ, Landweber LF (1999) Selection, history and chemistry: the three faces of the genetic code. Trends Biochem Sci 24(6):241–247PubMedCrossRefGoogle Scholar
  22. Korencic D, Polycarpo C, Weygand-Durasevic I, Söll D (2004) Differential modes of transfer RNASer recognition in Methanosarcina barkeri. J Biol Chem 279:48780–48786PubMedCrossRefGoogle Scholar
  23. Krzycki JA (2004) Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases. Curr Opin Chem Biol 8(5):484–491PubMedCrossRefGoogle Scholar
  24. Nagel GM, Doolittle RF (1995) Phylogenetic analysis of the aminoacyl-tRNA synthetases. J Mol Evol 40(5):487–498PubMedCrossRefGoogle Scholar
  25. Newman EB, Magasanik B (1963) The relation of serine-glycine metabolism to the formation of single-carbon units. Biochim Biophys Acta 78:437–448PubMedCrossRefGoogle Scholar
  26. Schimmel P (2008) Development of tRNA synthetases and connection to genetic code and disease. Protein Sci 17:1643–1652PubMedCrossRefGoogle Scholar
  27. Srinivasan G, James CM, Krzycki JA (2002) Pyrrolysine encoded by UAG in Archaea: charging of a UAG-decoding specialized tRNA. Science 296:1459–1462PubMedCrossRefGoogle Scholar
  28. Suzuki A, Knaff DB (2005) Glutamate synthetase: structural, mechanistic and regulatory properties, and role in the amino acid metabolism. Photosynth Res 83(2):191–217PubMedCrossRefGoogle Scholar
  29. Suzuki T, Miyauchi K (2010) Discover and characterization of tRNAIle lysidine synthetase (TilS). FEBS Lett 584(2):272–277PubMedCrossRefGoogle Scholar
  30. White RH (2001) Biosynthesis of the methanogenic cofactors. Vitam Horm 61:299–337PubMedCrossRefGoogle Scholar
  31. Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids; cysteine and methionine. Photosynth Res 86(3):345–362PubMedCrossRefGoogle Scholar
  32. Woese CR, Olsen GJ, Ibba M, Söll D (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Molec Biol Rev 64:202–236CrossRefGoogle Scholar
  33. 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 9:689–710PubMedGoogle Scholar
  34. Xiao JF, Yu J (2007) A scenario on the stepwise evolution of the genetic code. Genomics Proteomics Bioinformatics 5(3–4):143–151PubMedCrossRefGoogle Scholar
  35. Yang Z (2007) PAML 4:phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591PubMedCrossRefGoogle Scholar
  36. Zhaxybayeva O, Gogarten JP (2004) Cladogenesis, coalescence and the evolution of the three domains of life. Trends Gen 20:182–18CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Biological EngineeringMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Department of Crop and Soil SciencesCornell UniversityIthacaUSA
  3. 3.Department of Molecular and Cell BiologyUniversity of ConnecticutStorrsUSA

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