title: Biosynthesis of wyosine derivatives in tRNA: an ancient and highly diverse pathway in Archaea.
abstract: Wyosine (imG) and its derivatives such as wybutosine (yW) are found at position 37 of phenylalanine-specific transfer RNA (tRNA(Phe)), 3' adjacent to the anticodon in Eucarya and Archaea. In Saccharomyces cerevisiae, formation of yW requires five enzymes acting in a strictly sequential order: Trm5, Tyw1, Tyw2, Tyw3, and Tyw4. Archaea contain wyosine derivatives, but their diversity is greater than in eukaryotes and the corresponding biosynthesis pathways still unknown. To identify these pathways, we analyzed the phylogenetic distribution of homologues of the yeast wybutosine biosynthesis proteins in 62 archaeal genomes and proposed a scenario for the origin and evolution of wyosine derivatives biosynthesis in Archaea that was partly experimentally validated. The key observations were 1) that four of the five wybutosine biosynthetic enzymes are ancient and may have been present in the last common ancestor of Archaea and Eucarya, 2) that the variations in the distribution pattern of biosynthesis enzymes reflect the diversity of the wyosine derivatives found in different Archaea. We also identified 7-aminocarboxypropyl-demethylwyosine (yW-86) and its N4-methyl derivative (yW-72) as final products in tRNAs of several Archaea when these were previously thought to be only intermediates of the eukaryotic pathway. We confirmed that isowyosine (imG2) and 7-methylwyosine (mimG) are two archaeal-specific guanosine-37 derivatives found in tRNA of both Euryarchaeota and Crenarchaeota. Finally, we proposed that the duplication of the trm5 gene in some Archaea led to a change in function from N1 methylation of guanosine to C7 methylation of 4-demethylwyosine (imG-14).
authors.affiliation: Department of Microbiology and Cell Science, University of Florida, FL, USA. vcrecy@ufl.edu
authors.forename: Valérie
authors.initials: V
authors.lastname: de Crécy-Lagard
authors.forename: Céline
authors.initials: C
authors.lastname: Brochier-Armanet
authors.forename: Jaunius
authors.initials: J
authors.lastname: Urbonavicius
authors.forename: Bernard
authors.initials: B
authors.lastname: Fernandez
authors.forename: Gabriela
authors.initials: G
authors.lastname: Phillips
authors.forename: Benjamin
authors.initials: B
authors.lastname: Lyons
authors.forename: Akiko
authors.initials: A
authors.lastname: Noma
authors.forename: Sophie
authors.initials: S
authors.lastname: Alvarez
authors.forename: Louis
authors.initials: L
authors.lastname: Droogmans
authors.forename: Jean
authors.initials: J
authors.lastname: Armengaud
authors.forename: Henri
authors.initials: H
authors.lastname: Grosjean
mesh_terms: D001105:Archaea / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D002853:Chromatography, Liquid; D006151:Guanosine / Q000031:analogs & derivatives* / Q000737:chemistry / Q000378:metabolism; D013058:Mass Spectrometry; D010802:Phylogeny; D012343:RNA, Transfer / Q000378:metabolism*; D015398:Signal Transduction / Q000502:physiology*
chemical_list: D006151:Guanosine; C012100:wyosine; D012343:RNA, Transfer
references.citation: EMBO J. 1987 Feb;6(2):477-83
references.pmid: 3556165
references.citation: Nucleic Acids Res. 2009 May;37(9):2910-25
references.pmid: 19287006
references.citation: J Bacteriol. 1991 May;173(10):3138-48
references.pmid: 1708763
references.citation: Biochim Biophys Acta. 1990 Aug 27;1050(1-3):267-73
references.pmid: 2207154
references.citation: Nucleosides Nucleotides Nucleic Acids. 2004;23(1-2):41-50
references.pmid: 15043135
references.citation: Biochim Biophys Acta. 1971 Jun 30;240(2):163-9
references.pmid: 4327043
references.citation: J Biochem. 1974 May;75(5):1169-72
references.pmid: 4472218
references.citation: J Chromatogr. 1982 Jul 9;230(2):297-308
references.pmid: 7050138
references.citation: Nucleic Acids Res. 2005 Oct 07;33(17):5691-702
references.pmid: 16214803
references.citation: Mol Biol Evol. 2000 Apr;17(4):540-52
references.pmid: 10742046
references.citation: Nucleic Acids Res. 2001 Nov 15;29(22):4699-706
references.pmid: 11713320
references.citation: EMBO J. 2006 May 17;25(10):2142-54
references.pmid: 16642040
references.citation: J Biol Chem. 2005 Nov 11;280(45):37616-22
references.pmid: 16162496
references.citation: Proc Natl Acad Sci U S A. 1967 Mar;57(3):751-8
references.pmid: 16591527
references.citation: Bioorg Chem. 2004 Apr;32(2):82-91
references.pmid: 14990307
references.citation: Acta Crystallogr D Biol Crystallogr. 2007 Oct;63(Pt 10):1059-68
references.pmid: 17881823
references.citation: Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9188-93
references.pmid: 8799176
references.citation: Nucleic Acids Symp Ser. 2000;(44):267-8
references.pmid: 12903371
references.citation: J Bacteriol. 2003 Sep;185(18):5483-90
references.pmid: 12949100
references.citation: J Mol Biol. 2004 Jun 11;339(4):707-19
references.pmid: 15165845
references.citation: BMC Evol Biol. 2004 Jun 28;4:18
references.pmid: 15222900
references.citation: Nucleic Acids Res. 1987 Jan 26;15(2):683-93
references.pmid: 3103099
references.citation: Biochemistry. 1973 Jan 16;12(2):188-93
references.pmid: 4566585
references.citation: Nucleic Acids Res. 2009 Jan;37(Database issue):D159-62
references.pmid: 18957446
references.citation: Bioinformatics. 1999 Apr;15(4):305-8
references.pmid: 10320398
references.citation: Trends Biochem Sci. 1998 Nov;23(11):444-7
references.pmid: 9852764
references.citation: Methods Mol Biol. 2004;265:357-91
references.pmid: 15103084
references.citation: Eur J Biochem. 1968 Sep 24;5(4):546-55
references.pmid: 5698615
references.citation: Nat Struct Mol Biol. 2009 Oct;16(10):1109-15
references.pmid: 19749755
references.citation: Curr Opin Chem Biol. 2003 Apr;7(2):238-51
references.pmid: 12714058
references.citation: Biochim Biophys Acta. 1968 Oct 29;166(3):714-7
references.pmid: 5722700
references.citation: J Bacteriol. 2008 Dec;190(24):7876-84
references.pmid: 18931107
references.citation: Mol Biol Evol. 2007 Aug;24(8):1752-60
references.pmid: 17504772
references.citation: Nat Rev Microbiol. 2008 Mar;6(3):245-52
references.pmid: 18274537
references.citation: Biochem Biophys Res Commun. 2005 Aug 26;334(2):433-40
references.pmid: 16005430
references.citation: FASEB J. 2000 Nov;14(14):2365-8
references.pmid: 11053259
references.citation: EMBO J. 2001 Jan 15;20(1-2):231-9
references.pmid: 11226173
references.citation: Nucleic Acids Res. 1993 Nov 11;21(22):5264-72
references.pmid: 8255784
references.citation: Mol Gen Genet. 1982;188(3):440-6
references.pmid: 6298573
references.citation: Bioinformatics. 2003 Aug 12;19(12):1572-4
references.pmid: 12912839
references.citation: Proteins. 2008 Sep;72(4):1274-89
references.pmid: 18384044
references.citation: Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
references.pmid: 9254694
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15616-21
references.pmid: 19717466
references.citation: Nucleic Acids Res. 1990 Aug 25;18(16):4779-82
references.pmid: 2395642
references.citation: Microbiology (Reading). 2001 Apr;147(Pt 4):959-964
references.pmid: 11283291
references.citation: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references.pmid: 15034147
references.citation: Nucleic Acids Res. 1985 Apr 11;13(7):2443-9
references.pmid: 4000960
references.citation: Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20356-61
references.pmid: 19073919
references.citation: J Biol Chem. 1984 Aug 10;259(15):9461-71
references.pmid: 6746655
references.citation: Methods Enzymol. 1990;193:796-824
references.pmid: 1706064
references.citation: J Mol Biol. 2007 Oct 5;372(5):1204-14
references.pmid: 17727881
references.citation: Biochemistry. 1976 Feb 24;15(4):898-904
references.pmid: 942858
references.citation: Nature. 2002 May 2;417(6884):63-7
references.pmid: 11986665