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Local-to-global signal transduction at the core of a Mn2+ sensing riboswitch

KC. Suddala, IR. Price, SS. Dandpat, M. Janeček, P. Kührová, J. Šponer, P. Banáš, A. Ke, NG. Walter,

. 2019 ; 10 (1) : 4304. [pub] 20190920

Language English Country Great Britain

Document type Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.

Persistent link   https://www.medvik.cz/link/bmc20005881

Grant support
P30 GM124165 NIGMS NIH HHS - United States
R01 GM118524 NIGMS NIH HHS - United States
R01 GM062357 NIGMS NIH HHS - United States
S10 RR029205 NCRR NIH HHS - United States
R35 GM118174 NIGMS NIH HHS - United States

The widespread Mn2+-sensing yybP-ykoY riboswitch controls the expression of bacterial Mn2+ homeostasis genes. Here, we first determine the crystal structure of the ligand-bound yybP-ykoY riboswitch aptamer from Xanthomonas oryzae at 2.96 Å resolution, revealing two conformations with docked four-way junction (4WJ) and incompletely coordinated metal ions. In >100 µs of MD simulations, we observe that loss of divalents from the core triggers local structural perturbations in the adjacent docking interface, laying the foundation for signal transduction to the regulatory switch helix. Using single-molecule FRET, we unveil a previously unobserved extended 4WJ conformation that samples transient docked states in the presence of Mg2+. Only upon adding sub-millimolar Mn2+, however, can the 4WJ dock stably, a feature lost upon mutation of an adenosine contacting Mn2+ in the core. These observations illuminate how subtly differing ligand preferences of competing metal ions become amplified by the coupling of local with global RNA dynamics.

References provided by Crossref.org

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$a The widespread Mn2+-sensing yybP-ykoY riboswitch controls the expression of bacterial Mn2+ homeostasis genes. Here, we first determine the crystal structure of the ligand-bound yybP-ykoY riboswitch aptamer from Xanthomonas oryzae at 2.96 Å resolution, revealing two conformations with docked four-way junction (4WJ) and incompletely coordinated metal ions. In >100 µs of MD simulations, we observe that loss of divalents from the core triggers local structural perturbations in the adjacent docking interface, laying the foundation for signal transduction to the regulatory switch helix. Using single-molecule FRET, we unveil a previously unobserved extended 4WJ conformation that samples transient docked states in the presence of Mg2+. Only upon adding sub-millimolar Mn2+, however, can the 4WJ dock stably, a feature lost upon mutation of an adenosine contacting Mn2+ in the core. These observations illuminate how subtly differing ligand preferences of competing metal ions become amplified by the coupling of local with global RNA dynamics.
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$a Price, Ian R $u Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14850, USA.
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$a Kührová, Petra $u Department of Physical Chemistry, Faculty of Science, Palacký University, tř. 17 listopadu 12, Olomouc, 771 46, Czech Republic. Regional Centre of Advanced Technologies and Materials, Faculty of Science, Palacký University, tř. 17 listopadu 12, Olomouc, 771 46, Czech Republic.
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$a Banáš, Pavel $u Institute of Biophysics of the Czech Academy of Sciences, Kralovopolská 135, Brno, 612 65, Czech Republic. Department of Physical Chemistry, Faculty of Science, Palacký University, tř. 17 listopadu 12, Olomouc, 771 46, Czech Republic. Regional Centre of Advanced Technologies and Materials, Faculty of Science, Palacký University, tř. 17 listopadu 12, Olomouc, 771 46, Czech Republic.
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$a Ke, Ailong $u Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14850, USA. ailong.ke@cornell.edu.
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$a Walter, Nils G $u Single Molecule Analysis Group and Center for RNA Biomedicine, Department of Chemistry, University of Michigan, Ann Arbor, MI, 48109, USA. nwalter@umich.edu.
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