The hyperthermophilic partners Nanoarchaeum and Ignicoccus stabilize their tRNA T-loops via different but structurally equivalent modifications.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
09 07 2020
Historique:
accepted: 06 05 2020
revised: 19 04 2020
received: 08 02 2020
pubmed: 28 5 2020
medline: 9 9 2020
entrez: 28 5 2020
Statut: ppublish

Résumé

The universal L-shaped tertiary structure of tRNAs is maintained with the help of nucleotide modifications within the D- and T-loops, and these modifications are most extensive within hyperthermophilic species. The obligate-commensal Nanoarchaeum equitans and its phylogenetically-distinct host Ignicoccus hospitalis grow physically coupled under identical hyperthermic conditions. We report here two fundamentally different routes by which these archaea modify the key conserved nucleotide U54 within their tRNA T-loops. In N. equitans, this nucleotide is methylated by the S-adenosylmethionine-dependent enzyme NEQ053 to form m5U54, and a recombinant version of this enzyme maintains specificity for U54 in Escherichia coli. In N. equitans, m5U54 is subsequently thiolated to form m5s2U54. In contrast, I. hospitalis isomerizes U54 to pseudouridine prior to methylating its N1-position and thiolating the O4-position of the nucleobase to form the previously uncharacterized nucleotide m1s4Ψ. The methyl and thiol groups in m1s4Ψ and m5s2U are presented within the T-loop in a spatially identical manner that stabilizes the 3'-endo-anti conformation of nucleotide-54, facilitating stacking onto adjacent nucleotides and reverse-Hoogsteen pairing with nucleotide m1A58. Thus, two distinct structurally-equivalent solutions have evolved independently and convergently to maintain the tertiary fold of tRNAs under extreme hyperthermic conditions.

Identifiants

pubmed: 32459340
pii: 5847778
doi: 10.1093/nar/gkaa411
pmc: PMC7337903
doi:

Substances chimiques

RNA, Transfer 9014-25-9
tRNA Methyltransferases EC 2.1.1.-
tRNA(uracil-5)-methyltransferase EC 2.1.1.35

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6906-6918

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

Proc Natl Acad Sci U S A. 2008 May 13;105(19):6876-81
pubmed: 18451029
Science. 2006 Sep 29;313(5795):1935-42
pubmed: 16959973
Nucleic Acids Res. 2017 Feb 28;45(4):2007-2015
pubmed: 28204608
RNA. 2000 Jun;6(6):844-60
pubmed: 10864043
Proc Natl Acad Sci U S A. 2017 Jul 11;114(28):7355-7360
pubmed: 28655838
J Biol Chem. 2006 Jan 27;281(4):2104-13
pubmed: 16317006
Biochemistry. 1996 Sep 10;35(36):11652-9
pubmed: 8794745
Nucleic Acids Res. 2003 Aug 15;31(16):4738-46
pubmed: 12907714
Biomolecules. 2017 Apr 04;7(2):
pubmed: 28375166
Nucleic Acids Res. 1979 Apr;6(4):1571-81
pubmed: 377228
RNA. 2009 Feb;15(2):327-36
pubmed: 19144912
Biochemistry. 1985 Oct 8;24(21):5711-5
pubmed: 3853464
Eur J Biochem. 1988 Nov 15;177(3):467-75
pubmed: 2461858
FEBS Lett. 1974 Jul 1;43(1):59-63
pubmed: 4369142
RNA. 2012 Mar;18(3):421-33
pubmed: 22274953
BMC Bioinformatics. 2003 Sep 11;4:41
pubmed: 12969510
Methods Enzymol. 2007;425:3-20
pubmed: 17673077
J Bacteriol. 2003 Sep;185(18):5483-90
pubmed: 12949100
J Am Chem Soc. 2012 Dec 5;134(48):19739-45
pubmed: 23157377
J Biomol Struct Dyn. 1987 Dec;5(3):669-87
pubmed: 3078237
J Biol Chem. 2002 Oct 18;277(42):39128-35
pubmed: 12177072
Life (Basel). 2016 Jan 12;6(1):
pubmed: 26771646
RNA. 2011 Jan;17(1):45-53
pubmed: 21051506
J Bacteriol. 1991 May;173(10):3138-48
pubmed: 1708763
Nucleic Acids Res. 2009 Jan;37(Database issue):D159-62
pubmed: 18957446
Nature. 2013 Jul 25;499(7459):431-7
pubmed: 23851394
Biochemistry. 1970 Jul 7;9(14):2823-31
pubmed: 4918123
Biochemistry. 1994 Jun 28;33(25):7869-76
pubmed: 7516708
Nucleic Acids Res. 2018 Jan 4;46(D1):D303-D307
pubmed: 29106616
Biochemistry. 1983 Jan 4;22(1):98-102
pubmed: 6830766
Mol Microbiol. 2008 Jan;67(2):323-35
pubmed: 18069966
J Biol Chem. 1982 Apr 10;257(7):3589-92
pubmed: 7061499
Nucleic Acids Res. 2005 Jul 18;33(13):3955-64
pubmed: 16027442
IUBMB Life. 2019 Aug;71(8):1126-1140
pubmed: 30932315
Nucleic Acids Res. 2010 Oct;38(18):6206-18
pubmed: 20483913
Nucleic Acids Res. 2008 Sep;36(15):4929-40
pubmed: 18653523
J Bacteriol. 1980 Dec;144(3):991-8
pubmed: 6160144
J Biol. 2009;8(1):7
pubmed: 19216728
J Bacteriol. 2008 Mar;190(5):1743-50
pubmed: 18165302
Nucleic Acids Res. 2011 Nov;39(21):9368-75
pubmed: 21824914
RNA. 2000 Aug;6(8):1091-105
pubmed: 10943889
Methods Enzymol. 1988;164:481-9
pubmed: 2468070
Curr Opin Microbiol. 2011 Jun;14(3):335-41
pubmed: 21470902
J Biol Chem. 2006 May 19;281(20):14296-306
pubmed: 16547008
Nucleic Acids Res. 2004 Jan 22;32(2):465-76
pubmed: 14739239
J Mol Biol. 2008 Nov 14;383(3):641-51
pubmed: 18786544
Enzymes. 2017;41:1-50
pubmed: 28601219
Nucleic Acids Res. 1995 Nov 11;23(21):4312-9
pubmed: 7501451
Nucleic Acids Res. 2002 Apr 1;30(7):1427-64
pubmed: 11917006
J Biol Chem. 2002 Mar 15;277(11):8835-40
pubmed: 11779873
J Biol Chem. 2012 Dec 14;287(51):42480-94
pubmed: 23095745
RNA. 2004 Jun;10(6):907-13
pubmed: 15146074
Nucleic Acids Res. 2014 Jul;42(12):8073-82
pubmed: 24939895
Microorganisms. 2018 Oct 20;6(4):
pubmed: 30347855
Genome Biol. 2008;9(11):R158
pubmed: 19000309
Proc Natl Acad Sci U S A. 2017 May 9;114(19):4954-4959
pubmed: 28439027
Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12984-8
pubmed: 14566062
Biochem Biophys Res Commun. 1979 Nov 28;91(2):671-7
pubmed: 518660
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
PLoS Genet. 2014 May 08;10(5):e1004363
pubmed: 24809820
Methods Enzymol. 2007;425:103-19
pubmed: 17673080
Methods Enzymol. 2007;425:55-101
pubmed: 17673079
Proc Natl Acad Sci U S A. 1975 Feb;72(2):528-30
pubmed: 804695
Nature. 2002 May 2;417(6884):63-7
pubmed: 11986665

Auteurs

Simon Rose (S)

Department of Biochemistry & Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark.

Sylvie Auxilien (S)

Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France.

Jesper F Havelund (JF)

Department of Biochemistry & Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark.

Finn Kirpekar (F)

Department of Biochemistry & Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark.

Harald Huber (H)

Lehrstuhl für Mikrobiologie und Archaeenzentrum, Universität Regensburg, Universitätsstraße 31, D-93053 Regensburg, Germany.

Henri Grosjean (H)

Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France.

Stephen Douthwaite (S)

Department of Biochemistry & Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH