Dynamic RNA acetylation revealed by quantitative cross-evolutionary mapping

Aldema Sas-Chen, Justin M. Thomas, Donna Matzov, Masato Taoka, Kellie D. Nance, Ronit Nir, Keri M. Bryson, Ran Shachar, Geraldy L. S. Liman, Brett W. Burkhart, Supuni Thalalla Gamage, Yuko Nobe, Chloe A. Briney, Michaella J. Levy, Ryan T. Fuchs, G. Brett Robb, Jesse Hartmann, Sunny Sharma, Qishan Lin, Laurence Florens, Michael P. Washburn, Toshiaki Isobe, Thomas J. Santangelo, Moran Shalev-Benami (), Jordan L. Meier () and Schraga Schwartz ()
Additional contact information
Aldema Sas-Chen: Weizmann Institute of Science
Justin M. Thomas: National Institutes of Health
Donna Matzov: Weizmann Institute of Science
Masato Taoka: Tokyo Metropolitan University
Kellie D. Nance: National Institutes of Health
Ronit Nir: Weizmann Institute of Science
Keri M. Bryson: National Institutes of Health
Ran Shachar: Weizmann Institute of Science
Geraldy L. S. Liman: Colorado State University
Brett W. Burkhart: Colorado State University
Supuni Thalalla Gamage: National Institutes of Health
Yuko Nobe: Tokyo Metropolitan University
Chloe A. Briney: National Institutes of Health
Michaella J. Levy: Stowers Institute for Medical Research
Ryan T. Fuchs: New England Biolabs, Inc
G. Brett Robb: New England Biolabs, Inc
Jesse Hartmann: Weizmann Institute of Science
Sunny Sharma: Rutgers University
Qishan Lin: University at Albany
Laurence Florens: Stowers Institute for Medical Research
Michael P. Washburn: Stowers Institute for Medical Research
Toshiaki Isobe: Tokyo Metropolitan University
Thomas J. Santangelo: Colorado State University
Moran Shalev-Benami: Weizmann Institute of Science
Jordan L. Meier: National Institutes of Health
Schraga Schwartz: Weizmann Institute of Science

Nature, 2020, vol. 583, issue 7817, 638-643

Abstract: Abstract N4-acetylcytidine (ac4C) is an ancient and highly conserved RNA modification that is present on tRNA and rRNA and has recently been investigated in eukaryotic mRNA1–3. However, the distribution, dynamics and functions of cytidine acetylation have yet to be fully elucidated. Here we report ac4C-seq, a chemical genomic method for the transcriptome-wide quantitative mapping of ac4C at single-nucleotide resolution. In human and yeast mRNAs, ac4C sites are not detected but can be induced—at a conserved sequence motif—via the ectopic overexpression of eukaryotic acetyltransferase complexes. By contrast, cross-evolutionary profiling revealed unprecedented levels of ac4C across hundreds of residues in rRNA, tRNA, non-coding RNA and mRNA from hyperthermophilic archaea. Ac4C is markedly induced in response to increases in temperature, and acetyltransferase-deficient archaeal strains exhibit temperature-dependent growth defects. Visualization of wild-type and acetyltransferase-deficient archaeal ribosomes by cryo-electron microscopy provided structural insights into the temperature-dependent distribution of ac4C and its potential thermoadaptive role. Our studies quantitatively define the ac4C landscape, providing a technical and conceptual foundation for elucidating the role of this modification in biology and disease4–6.

Date: 2020
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DOI: 10.1038/s41586-020-2418-2

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