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Title: Structural analysis of a class III preQ1 riboswitch reveals an aptamer distant from a ribosome-binding site regulated by fast dynamics

Abstract

PreQ1-III riboswitches are newly identified RNA elements that control bacterial genes in response to preQ1 (7-aminomethyl-7-deazaguanine), a precursor to the essential hypermodified tRNA base queuosine. Although numerous riboswitches fold as H-type or HLout-type pseudoknots that integrate ligand-binding and regulatory sequences within a single folded domain, the preQ1-III riboswitch aptamer forms a HLout-type pseudoknot that does not appear to incorporate its ribosome-binding site (RBS). To understand how this unusual organization confers function, in this paper we determined the crystal structure of the class III preQ1 riboswitch from Faecalibacterium prausnitzii at 2.75 Å resolution. PreQ1 binds tightly (KD,app 6.5 ± 0.5 nM) between helices P1 and P2 of a three-way helical junction wherein the third helix, P4, projects orthogonally from the ligand-binding pocket, exposing its stem-loop to base pair with the 3' RBS. Biochemical analysis, computational modeling, and single-molecule FRET imaging demonstrated that preQ1 enhances P4 reorientation toward P1–P2, promoting a partially nested, H-type pseudoknot in which the RBS undergoes rapid docking (kdock ~0.6 s-1) and undocking (kundock ~1.1 s-1). Finally, discovery of such dynamic conformational switching provides insight into how a riboswitch with bipartite architecture uses dynamics to modulate expression platform accessibility, thus expanding the known repertoire of gene control strategiesmore » used by regulatory RNAs.« less

Authors:
 [1];  [2];  [1];  [3];  [1];  [1];  [1];  [3];  [2];  [1]
+ Show Author Affiliations
  1. Univ. of Rochester School of Medicine and Dentistry, Rochester, NY (United States)
  2. Univ. of Michigan, Ann Arbor, MI (United States)
  3. Univ. of California, Irvine, CA (United States)
Publication Date:
Research Org.:
Univ. of Rochester School of Medicine and Dentistry, Rochester, NY (United States)
Sponsoring Org.:
USDOE; National Inst. of Health (NIH) (United States)
OSTI Identifier:
1349644
Grant/Contract Number:  
GM063162; RR026501; GM062357; GM076485; GM103393; RR001209
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 27; 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; preQ1 riboswitch; gene regulation; crystal structure; single-molecule FRET; molecular dynamics

Citation Formats

Liberman, Joseph A., Suddala, Krishna C., Aytenfisu, Asaminew, Chan, Dalen, Belashov, Ivan A., Salim, Mohammad, Mathews, David H., Spitale, Robert C., Walter, Nils G., and Wedekind, Joseph E. Structural analysis of a class III preQ1 riboswitch reveals an aptamer distant from a ribosome-binding site regulated by fast dynamics. United States: N. p., 2015. Web. doi:10.1073/pnas.1503955112.
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Liberman, Joseph A., Suddala, Krishna C., Aytenfisu, Asaminew, Chan, Dalen, Belashov, Ivan A., Salim, Mohammad, Mathews, David H., Spitale, Robert C., Walter, Nils G., & Wedekind, Joseph E. Structural analysis of a class III preQ1 riboswitch reveals an aptamer distant from a ribosome-binding site regulated by fast dynamics. United States. https://doi.org/10.1073/pnas.1503955112
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Liberman, Joseph A., Suddala, Krishna C., Aytenfisu, Asaminew, Chan, Dalen, Belashov, Ivan A., Salim, Mohammad, Mathews, David H., Spitale, Robert C., Walter, Nils G., and Wedekind, Joseph E. Tue . "Structural analysis of a class III preQ1 riboswitch reveals an aptamer distant from a ribosome-binding site regulated by fast dynamics". United States. https://doi.org/10.1073/pnas.1503955112. https://www.osti.gov/servlets/purl/1349644.
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@article{osti_1349644,
title = {Structural analysis of a class III preQ1 riboswitch reveals an aptamer distant from a ribosome-binding site regulated by fast dynamics},
author = {Liberman, Joseph A. and Suddala, Krishna C. and Aytenfisu, Asaminew and Chan, Dalen and Belashov, Ivan A. and Salim, Mohammad and Mathews, David H. and Spitale, Robert C. and Walter, Nils G. and Wedekind, Joseph E.},
abstractNote = {PreQ1-III riboswitches are newly identified RNA elements that control bacterial genes in response to preQ1 (7-aminomethyl-7-deazaguanine), a precursor to the essential hypermodified tRNA base queuosine. Although numerous riboswitches fold as H-type or HLout-type pseudoknots that integrate ligand-binding and regulatory sequences within a single folded domain, the preQ1-III riboswitch aptamer forms a HLout-type pseudoknot that does not appear to incorporate its ribosome-binding site (RBS). To understand how this unusual organization confers function, in this paper we determined the crystal structure of the class III preQ1 riboswitch from Faecalibacterium prausnitzii at 2.75 Å resolution. PreQ1 binds tightly (KD,app 6.5 ± 0.5 nM) between helices P1 and P2 of a three-way helical junction wherein the third helix, P4, projects orthogonally from the ligand-binding pocket, exposing its stem-loop to base pair with the 3' RBS. Biochemical analysis, computational modeling, and single-molecule FRET imaging demonstrated that preQ1 enhances P4 reorientation toward P1–P2, promoting a partially nested, H-type pseudoknot in which the RBS undergoes rapid docking (kdock ~0.6 s-1) and undocking (kundock ~1.1 s-1). Finally, discovery of such dynamic conformational switching provides insight into how a riboswitch with bipartite architecture uses dynamics to modulate expression platform accessibility, thus expanding the known repertoire of gene control strategies used by regulatory RNAs.},
doi = {10.1073/pnas.1503955112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 27,
volume = 112,
place = {United States},
year = {Tue Jun 23 00:00:00 EDT 2015},
month = {Tue Jun 23 00:00:00 EDT 2015}
}
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https://doi.org/10.1073/pnas.1503955112
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