Table of Contents Author Guidelines Submit a Manuscript
Corrigendum

A corrigendum for this article has been published. To view the corrigendum, please click here.

Archaea
Volume 2014, Article ID 374146, 11 pages
http://dx.doi.org/10.1155/2014/374146
Research Article

Unique Characteristics of the Pyrrolysine System in the 7th Order of Methanogens: Implications for the Evolution of a Genetic Code Expansion Cassette

11EA-4678 CIDAM, Clermont Université, Université d’Auvergne, Place Henri Dunant, 63001 Clermont-Ferrand, France
2Department of Microbiology and Alimentary Pharmabiotic Centre, University College Cork, Western Road, Cork, Ireland
3Institut Pasteur, Department of Microbiology, Unité de Biologie Moléculaire du Gène chez les Extrêmophiles, 28 rue du Dr. Roux, 75015 Paris, France

Received 30 August 2013; Accepted 19 October 2013; Published 27 January 2014

Academic Editor: Kyung Mo Kim

Copyright © 2014 Guillaume Borrel et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. P. Lothrop, M. P. Torres, and S. M. Fuchs, “Deciphering post-translational modification codes,” FEBS Letters, vol. 587, pp. 1247–1257, 2013. View at Google Scholar
  2. F. Wold, “In vivo chemical modification of proteins (post-translational modification),” Annual Review of Biochemistry, vol. 50, pp. 783–814, 1981. View at Google Scholar · View at Scopus
  3. A. Bock and T. C. Stadtman, “Selenocysteine, a highly specific component of certain enzymes, is incorporated by a UGA-directed co-translational mechanism,” BioFactors, vol. 1, no. 3, pp. 245–250, 1988. View at Google Scholar · View at Scopus
  4. T. C. Stadtman, “Selenocysteine,” Annual Review of Biochemistry, vol. 65, pp. 83–100, 1996. View at Google Scholar · View at Scopus
  5. M. Ibba and D. Söll, “Genetic code: introducing pyrrolysine,” Current Biology, vol. 12, no. 13, pp. R464–R466, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Srinivasan, C. M. James, and J. A. Krzycki, “Pyrrolysine encoded by UAG in archaea: charging of a UAG-decoding specialized tRNA,” Science, vol. 296, no. 5572, pp. 1459–1462, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Bock, K. Forchhammer, J. Heider et al., “Selenocysteine: the 21st amino acid,” Molecular Microbiology, vol. 5, no. 3, pp. 515–520, 1991. View at Google Scholar · View at Scopus
  8. Y. Zhang, H. Romero, G. Salinas, and V. N. Gladyshev, “Dynamic evolution of selenocysteine utilization in bacteria: a balance between selenoprotein loss and evolution of selenocysteine from redox active cysteine residues,” Genome Biology, vol. 7, no. 10, article R94, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Rother, A. Resch, R. Wilting, and A. Böck, “Selenoprotein synthesis in archaea,” BioFactors, vol. 14, no. 1–4, pp. 75–83, 2001. View at Google Scholar · View at Scopus
  10. T. Stock and M. Rother, “Selenoproteins in Archaea and Gram-positive bacteria,” Biochimica et Biophysica Acta, vol. 1790, no. 11, pp. 1520–1532, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. M. A. Gaston, R. Jiang, and J. A. Krzycki, “Functional context, biosynthesis, and genetic encoding of pyrrolysine,” Current Opinion in Microbiology, vol. 14, no. 3, pp. 342–349, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Rother and J. A. Krzycki, “Selenocysteine, pyrrolysine, and the unique energy metabolism of methanogenic archaea,” Archaea, vol. 2010, Article ID 453642, 14 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. M. A. Gaston, L. Zhang, K. B. Green-Church, and J. A. Krzycki, “The complete biosynthesis of the genetically encoded amino acid pyrrolysine from lysine,” Nature, vol. 471, no. 7340, pp. 647–650, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. D. G. Longstaff, R. C. Larue, J. E. Faust et al., “A natural genetic code expansion cassette enables transmissible biosynthesis and genetic encoding of pyrrolysine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 3, pp. 1021–1026, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. J. A. Krzycki, “The path of lysine to pyrrolysine,” Current Opinion in Chemical Biology, vol. 17, no. 4, pp. 619–625, 2013. View at Google Scholar
  16. F. Quitterer, P. Beck, A. Bacher, and M. Groll, “Structure and reaction mechanism of pyrrolysine synthase (PylD),” Angewandte Chemie International Edition, vol. 52, no. 27, pp. 7033–7037, 2013. View at Google Scholar
  17. K. Nozawa, P. O'Donoghue, S. Gundllapalli et al., “Pyrrolysyl-tRNA synthetase-tRNAPyl structure reveals the molecular basis of orthogonality,” Nature, vol. 457, no. 7233, pp. 1163–1167, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Polycarpo, A. Ambrogelly, A. Bérubé et al., “An aminoacyl-tRNA synthetase that specifically activates pyrrolysine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 34, pp. 12450–12454, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Théobald-Dietrich, M. Frugier, R. Giegé, and J. Rudinger-Thirion, “Atypical archaeal tRNA pyrrolysine transcript behaves towards EF-Tu as a typical elongator tRNA,” Nucleic Acids Research, vol. 32, no. 3, pp. 1091–1096, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Herring, A. Ambrogelly, C. R. Polycarpo, and D. Söll, “Recognition of pyrrolysine tRNA by the Desulfitobacterium hafniense pyrrolysyl-tRNA synthetase,” Nucleic Acids Research, vol. 35, no. 4, pp. 1270–1278, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. J. M. Kavran, S. Gundllapalli, P. O'Donoghue, M. Englert, D. Söll, and T. A. Steitz, “Structure of pyrrolysyl-tRNA synthetase, an archaeal enzyme for genetic code innovation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 27, pp. 11268–11273, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. M. Lee, R. Jiang, R. Jain, R. C. Larue, J. Krzycki, and M. K. Chan, “Structure of Desulfitobacterium hafniense PylSc, a pyrrolysyl-tRNA synthetase,” Biochemical and Biophysical Research Communications, vol. 374, no. 3, pp. 470–474, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Yanagisawa, R. Ishii, R. Fukunaga, T. Kobayashi, K. Sakamoto, and S. Yokoyama, “Crystallographic studies on multiple conformational states of active-site loops in pyrrolysyl-tRNA synthetase,” Journal of Molecular Biology, vol. 378, no. 3, pp. 634–652, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Yanagisawa, T. Sumida, R. Ishii, and S. Yokoyama, “A novel crystal form of pyrrolysyl-tRNA synthetase reveals the pre- and post-aminoacyl-tRNA synthesis conformational states of the adenylate and aminoacyl moieties and an asparagine residue in the catalytic site,” Acta Crystallographica D, vol. 69, pp. 5–15, 2013. View at Google Scholar
  25. L. Prat, I. U. Heinemann, H. R. Aerni, J. Rinehart, P. O’Donoghue, and D. Söll, “Carbon source-dependent expansion of the genetic code in bacteria,” Proceedings of the National Academy of Sciences, vol. 109, pp. 21070–21075, 2012. View at Google Scholar
  26. L. Paul, D. J. Ferguson Jr., and J. A. Krzycki, “The trimethylamine methyltransferase gene and multiple dimethylamine methyltransferase genes of Methanosarcina barkeri contain in-frame and read- through amber codons,” Journal of Bacteriology, vol. 182, no. 9, pp. 2520–2529, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. J. A. Soares, L. Zhang, R. L. Pitsch et al., “The residue mass of L-pyrrolysine in three distinct methylamine methyltransferases,” The Journal of Biological Chemistry, vol. 280, no. 44, pp. 36962–36969, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Mihajlovski, M. Alric, and J.-F. Brugère, “A putative new order of methanogenic Archaea inhabiting the human gut, as revealed by molecular analyses of the mcrA gene,” Research in Microbiology, vol. 159, no. 7-8, pp. 516–521, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Mihajlovski, J. Doré, F. Levenez, M. Alric, and J.-F. Brugère, “Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age-associated increase of the diversity,” Environmental Microbiology Reports, vol. 2, no. 2, pp. 272–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Iino, H. Tamaki, S. Tamazawa et al., “Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata,” Microbes and Environments, vol. 28, pp. 244–250, 2013. View at Google Scholar
  31. K. Paul, J. O. Nonoh, L. Mikulski, and A. Brune, “‘Methanoplasmatales,’ Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens,” Applied and Environmental Microbiology, vol. 78, pp. 8245–8253, 2012. View at Google Scholar
  32. G. Borrel, P. W. O’Toole, P. Peyret, J. F. Brugère, and S. Gribaldo, “Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis,” Genome Biology and Evolution, vol. 5, pp. 1769–1780, 2013. View at Google Scholar
  33. G. Borrel, H. M. Harris, W. Tottey et al., “Genome sequence of, “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens,” Journal of Bacteriology, vol. 194, pp. 6944–6945, 2012. View at Google Scholar
  34. A. Gorlas, C. Robert, G. Gimenez, M. Drancourt, and D. Raoult, “Complete genome sequence of Methanomassiliicoccus luminyensis, the largest genome of a human-associated Archaea species,” Journal of Bacteriology, vol. 194, no. 17, p. 4745, 2012. View at Google Scholar
  35. B. Dridi, M. L. Fardeau, B. Ollivier, D. Raoult, and M. Drancourt, “Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces,” International Journal of Systematic and Evolutionary Microbiology, vol. 62, pp. 1902–1907, 2012. View at Google Scholar
  36. G. Borrel, H. M. Harris, N. Parisot et al., “Genome sequence of “Candidatus methanomassiliicoccus intestinalis” Issoire-Mx1, a third Thermoplasmatales-related methanogenic archaeon from human feces,” Genome Announcements, vol. 1, no. 4, Article ID e00453, 13 pages, 2013. View at Publisher · View at Google Scholar
  37. J. F. Brugère, G. Borrel, N. Gaci, W. Tottey, P. W. O. ’Toole, and C. Malpuech-Brugère, “Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease,” Gut Microbes, vol. 5, no. 1, 2013. View at Google Scholar
  38. M. Poulsen, C. Schwab, B. B. Jensen et al., “Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen,” Nature Communications, vol. 4, article 1428, 2013. View at Google Scholar
  39. R. K. Aziz, D. Bartels, A. Best et al., “The RAST server: rapid annotations using subsystems technology,” BMC Genomics, vol. 9, article 75, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Rutherford, J. Parkhill, J. Crook et al., “Artemis: sequence visualization and annotation,” Bioinformatics, vol. 16, no. 10, pp. 944–945, 2000. View at Google Scholar · View at Scopus
  41. S. F. Altschul, W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, “Basic local alignment search tool,” Journal of Molecular Biology, vol. 215, no. 3, pp. 403–410, 1990. View at Publisher · View at Google Scholar · View at Scopus
  42. M. A. Larkin, G. Blackshields, N. P. Brown et al., “Clustal W and clustal X version 2.0,” Bioinformatics, vol. 23, no. 21, pp. 2947–2948, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Notredame, D. G. Higgins, and J. Heringa, “T-coffee: a novel method for fast and accurate multiple sequence alignment,” Journal of Molecular Biology, vol. 302, no. 1, pp. 205–217, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. R. C. Edgar, “MUSCLE: multiple sequence alignment with high accuracy and high throughput,” Nucleic Acids Research, vol. 32, no. 5, pp. 1792–1797, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Wilm, D. G. Higgins, and C. Notredame, “R-Coffee: a method for multiple alignment of non-coding RNA,” Nucleic Acids Research, vol. 36, no. 9, article e52, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. A. R. Gruber, R. Lorenz, S. H. Bernhart, R. Neuböck, and I. L. Hofacker, “The Vienna RNA websuite,” Nucleic Acids Research, vol. 36, pp. W70–W74, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. J. S. Reuter and D. H. Mathews, “RNAstructure: software for RNA secondary structure prediction and analysis,” BMC Bioinformatics, vol. 11, article 129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Criscuolo and S. Gribaldo, “BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments,” BMC Evolutionary Biology, vol. 10, no. 1, article 210, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Guindon, J.-F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk, and O. Gascuel, “New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0,” Systematic Biology, vol. 59, no. 3, pp. 307–321, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Q. Le and O. Gascuel, “An improved general amino acid replacement matrix,” Molecular Biology and Evolution, vol. 25, no. 7, pp. 1307–1320, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. G. Jobb, A. von Haeseler, and K. Strimmer, “TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics,” BMC Evolutionary Biology, vol. 4, article 18, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. N. Lartillot, T. Lepage, and S. Blanquart, “PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating,” Bioinformatics, vol. 25, no. 17, pp. 2286–2288, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Yuan, P. O'Donoghue, A. Ambrogelly et al., “Distinct genetic code expansion strategies for selenocysteine and pyrrolysine are reflected in different aminoacyl-tRNA formation systems,” FEBS Letters, vol. 584, no. 2, pp. 342–349, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. I. L. Hofacker, “RNA secondary structure analysis using the Vienna RNA package,” Current Protocols in Bioinformatics, 2004, Chapter 12, Unit 12.2. View at Google Scholar · View at Scopus
  55. R. Jiang and J. A. Krzycki, “PylSn and the homologous N-terminal domain of pyrrolysyl-tRNA synthetase bind the tRNA that is essential for the genetic encoding of pyrrolysine,” The Journal of Biological Chemistry, vol. 287, pp. 32738–32746, 2012. View at Google Scholar
  56. E. M. Zdobnov and R. Apweiler, “InterProScan—an integration platform for the signature-recognition methods in InterPro,” Bioinformatics, vol. 17, no. 9, pp. 847–848, 2001. View at Google Scholar · View at Scopus
  57. M. J. Hohn, H.-S. Park, P. O'Donoghue, M. Schnitzbauer, and D. Söll, “Emergence of the universal genetic code imprinted in an RNA record,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 48, pp. 18095–18100, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Fournier, “Horizontal gene transfer and the evolution of methanogenic pathways,” Methods in Molecular Biology, vol. 532, pp. 163–179, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. G. P. Fournier, J. Huang, and J. Peter Gogarten, “Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life,” Philosophical Transactions of the Royal Society B, vol. 364, no. 1527, pp. 2229–2239, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. A. V. Lobanov, A. A. Turanov, D. L. Hatfield, and V. N. Gladyshev, “Dual functions of codons in the genetic code,” Critical Reviews in Biochemistry and Molecular Biology, vol. 45, no. 4, pp. 257–265, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. É. Bapteste, C. Brochier, and Y. Boucher, “Higher-level classification of the Archaea: evolution of methanogenesis and methanogens,” Archaea, vol. 1, no. 5, pp. 353–363, 2005. View at Google Scholar · View at Scopus
  62. S. Gribaldo and C. Brochier-Armanet, “The origin and evolution of Archaea: a state of the art,” Philosophical Transactions of the Royal Society B, vol. 361, no. 1470, pp. 1007–1022, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. J. T.-F. Wong, “Coevolutlon theory of genetic code at age thirty,” BioEssays, vol. 27, no. 4, pp. 416–425, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. D. G. Longstaff, S. K. Blight, L. Zhang, K. B. Green-Church, and J. A. Krzycki, “In vivo contextual requirements for UAG translation as pyrrolysine,” Molecular Microbiology, vol. 63, no. 1, pp. 229–241, 2007. View at Publisher · View at Google Scholar · View at Scopus