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Title: A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

Abstract

The sulfur-containing nucleosides in transfer RNA (tRNAs) are present in all three domains of life; they have critical functions for accurate and efficient translation, such as tRNA structure stabilization and proper codon recognition. The tRNA modification enzymes ThiI (in bacteria and archaea) and Ncs6 (in archaea and eukaryotic cytosols) catalyze the formation of 4-thiouridine (s4U) and 2-thiouridine (s2U), respectively. The ThiI homologs were proposed to transfer sulfur via cysteine persulfide enzyme adducts, whereas the reaction mechanism of Ncs6 remains unknown. In this, we show that ThiI from the archaeon Methanococcus maripaludis contains a [3Fe-4S] cluster that is essential for its tRNA thiolation activity. Furthermore, the archaeal and eukaryotic Ncs6 homologs as well as phosphoseryl-tRNA (Sep-tRNA):Cys-tRNA synthase (SepCysS), which catalyzes the Sep-tRNA to Cys-tRNA conversion in methanogens, also possess a [3Fe-4S] cluster similar to the methanogenic archaeal ThiI. These results suggest that the diverse tRNA thiolation processes in archaea and eukaryotic cytosols share a common mechanism dependent on a [3Fe-4S] cluster for sulfur transfer.

Authors:
 [1];  [2];  [3];  [4];  [4];  [3];  [5];  [5]
+ Show Author Affiliations
  1. Louisiana State Univ., Baton Rouge, LA (United States). Dept. of Biological Sciences
  2. Yale Univ., New Haven, CT (United States). Dept. of Chemistry; Louisiana State Univ., Baton Rouge, LA (United States). Dept. of Biological Sciences
  3. Yale Univ., New Haven, CT (United States). Dept. of Chemistry
  4. Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry
  5. Yale Univ., New Haven, CT (United States). Dept. of Chemistry and Dept. of Molecular Biophysics and Biochemistry
Publication Date:
Research Org.:
Yale Univ., New Haven, CT (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1418599
Grant/Contract Number:  
FG02-05ER15646; MCB-1410079; GM22854; GM065313
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 45; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; iron-sulfur cluster; thionucleosides; tRNA modification; CTU1

Citation Formats

Liu, Yuchen, Vinyard, David J., Reesbeck, Megan E., Suzuki, Tateki, Manakongtreecheep, Kasidet, Holland, Patrick L., Brudvig, Gary W., and Söll, Dieter. A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes. United States: N. p., 2016. Web. doi:10.1073/pnas.1615732113.
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Liu, Yuchen, Vinyard, David J., Reesbeck, Megan E., Suzuki, Tateki, Manakongtreecheep, Kasidet, Holland, Patrick L., Brudvig, Gary W., & Söll, Dieter. A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes. United States. https://doi.org/10.1073/pnas.1615732113
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Liu, Yuchen, Vinyard, David J., Reesbeck, Megan E., Suzuki, Tateki, Manakongtreecheep, Kasidet, Holland, Patrick L., Brudvig, Gary W., and Söll, Dieter. Mon . "A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes". United States. https://doi.org/10.1073/pnas.1615732113. https://www.osti.gov/servlets/purl/1418599.
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@article{osti_1418599,
title = {A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes},
author = {Liu, Yuchen and Vinyard, David J. and Reesbeck, Megan E. and Suzuki, Tateki and Manakongtreecheep, Kasidet and Holland, Patrick L. and Brudvig, Gary W. and Söll, Dieter},
abstractNote = {The sulfur-containing nucleosides in transfer RNA (tRNAs) are present in all three domains of life; they have critical functions for accurate and efficient translation, such as tRNA structure stabilization and proper codon recognition. The tRNA modification enzymes ThiI (in bacteria and archaea) and Ncs6 (in archaea and eukaryotic cytosols) catalyze the formation of 4-thiouridine (s4U) and 2-thiouridine (s2U), respectively. The ThiI homologs were proposed to transfer sulfur via cysteine persulfide enzyme adducts, whereas the reaction mechanism of Ncs6 remains unknown. In this, we show that ThiI from the archaeon Methanococcus maripaludis contains a [3Fe-4S] cluster that is essential for its tRNA thiolation activity. Furthermore, the archaeal and eukaryotic Ncs6 homologs as well as phosphoseryl-tRNA (Sep-tRNA):Cys-tRNA synthase (SepCysS), which catalyzes the Sep-tRNA to Cys-tRNA conversion in methanogens, also possess a [3Fe-4S] cluster similar to the methanogenic archaeal ThiI. These results suggest that the diverse tRNA thiolation processes in archaea and eukaryotic cytosols share a common mechanism dependent on a [3Fe-4S] cluster for sulfur transfer.},
doi = {10.1073/pnas.1615732113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 45,
volume = 113,
place = {United States},
year = {Mon Oct 24 00:00:00 EDT 2016},
month = {Mon Oct 24 00:00:00 EDT 2016}
}
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https://doi.org/10.1073/pnas.1615732113
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