title: Unique characteristics of the pyrrolysine system in the 7th order of methanogens: implications for the evolution of a genetic code expansion cassette.
abstract: Pyrrolysine (Pyl), the 22nd proteogenic amino acid, was restricted until recently to few organisms. Its translational use necessitates the presence of enzymes for synthesizing it from lysine, a dedicated amber stop codon suppressor tRNA, and a specific amino-acyl tRNA synthetase. The three genomes of the recently proposed Thermoplasmata-related 7th order of methanogens contain the complete genetic set for Pyl synthesis and its translational use. Here, we have analyzed the genomic features of the Pyl-coding system in these three genomes with those previously known from Bacteria and Archaea and analyzed the phylogeny of each component. This shows unique peculiarities, notably an amber tRNA(Pyl) with an imperfect anticodon stem and a shortened tRNA(Pyl) synthetase. Phylogenetic analysis indicates that a Pyl-coding system was present in the ancestor of the seventh order of methanogens and appears more closely related to Bacteria than to Methanosarcinaceae, suggesting the involvement of lateral gene transfer in the spreading of pyrrolysine between the two prokaryotic domains. We propose that the Pyl-coding system likely emerged once in Archaea, in a hydrogenotrophic and methanol-H2-dependent methylotrophic methanogen. The close relationship between methanogenesis and the Pyl system provides a possible example of expansion of a still evolving genetic code, shaped by metabolic requirements.
authors.affiliation: 1EA-4678 CIDAM, Clermont Université, Université d'Auvergne, Place Henri Dunant, 63001 Clermont-Ferrand, France ; Department of Microbiology and Alimentary Pharmabiotic Centre, University College Cork, Western Road, Cork, Ireland.
authors.forename: Guillaume
authors.initials: G
authors.lastname: Borrel
authors.affiliation: 1EA-4678 CIDAM, Clermont Université, Université d'Auvergne, Place Henri Dunant, 63001 Clermont-Ferrand, France.
authors.forename: Nadia
authors.initials: N
authors.lastname: Gaci
authors.affiliation: 1EA-4678 CIDAM, Clermont Université, Université d'Auvergne, Place Henri Dunant, 63001 Clermont-Ferrand, France.
authors.forename: Pierre
authors.initials: P
authors.lastname: Peyret
authors.affiliation: Department of Microbiology and Alimentary Pharmabiotic Centre, University College Cork, Western Road, Cork, Ireland.
authors.forename: Paul W
authors.initials: PW
authors.lastname: O'Toole
authors.affiliation: Institut Pasteur, Department of Microbiology, Unité de Biologie Moléculaire du Gène chez les Extrêmophiles, 28 rue du Dr. Roux, 75015 Paris, France.
authors.forename: Simonetta
authors.initials: S
authors.lastname: Gribaldo
authors.affiliation: 1EA-4678 CIDAM, Clermont Université, Université d'Auvergne, Place Henri Dunant, 63001 Clermont-Ferrand, France.
authors.forename: Jean-François
authors.identifier: 0000-0002-1559-2331
authors.initials: JF
authors.lastname: Brugère
mesh_terms: D000604:Amino Acyl-tRNA Synthetases / Q000235:genetics; D001419:Bacteria / Q000235:genetics; D053898:Biosynthetic Pathways / Q000235:genetics*; D019605:Euryarchaeota / Q000235:genetics*; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D005815:Genetic Code; D008239:Lysine / Q000031:analogs & derivatives* / Q000096:biosynthesis; D010802:Phylogeny; D012343:RNA, Transfer / Q000235:genetics; D017385:Sequence Homology
chemical_list: D012343:RNA, Transfer; D000604:Amino Acyl-tRNA Synthetases; C456839:pyrrolysine; D008239:Lysine