A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism

doi:10.1111/j.1365-2958.2008.06208.x

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Wiley InterScience

Molecular Microbiology

Volume 68 Issue 4, Pages 918 - 932

Published Online: 20 Mar 2008

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A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism

Elizabeth E. Regulski, ¹ Ryan H. Moy, ² Zasha Weinberg, ¹ Jeffrey E. Barrick, ^2,3 ^† Zizhen Yao, ⁴ Walter L. Ruzzo ^4,5 and Ronald R. Breaker ^1,2,3 *

¹ Department of Molecular, Cellular and Developmental Biology, ² Department of Molecular Biophysics and Biochemistry and ³ Howard Hughes Medical Institute, Yale University, New Haven, CT 06520, USA. Departments of ⁴ Computer Science and Engineering and ⁵ Genome Sciences, University of Washington, Seattle, WA 98195, USA.

Correspondence to *E-mail ronald.breaker@yale.edu; Tel. (+1) 203 432 9389; Fax: Tel. (+1) 203 432 0753.

^† Present address: Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824-4320, USA.

Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

ABSTRACT

We have identified a highly conserved RNA motif located upstream of genes encoding molybdate transporters, molybdenum cofactor (Moco) biosynthesis enzymes, and proteins that utilize Moco as a coenzyme. Bioinformatics searches have identified 176 representatives in γ-Proteobacteria, δ-Proteobacteria, Clostridia, Actinobacteria, Deinococcus-Thermus species and DNAs from environmental samples. Using genetic assays, we demonstrate that a Moco RNA in Escherichia coli associated with the Moco biosynthetic operon controls gene expression in response to Moco production. In addition, we provide evidence indicating that this conserved RNA discriminates against closely related analogues of Moco. These results, together with extensive phylogenetic conservation and typical gene control structures near some examples, indicate that representatives of this structured RNA represent a novel class of riboswitches that sense Moco. Furthermore, we identify variants of this RNA that are likely to be triggered by the related tungsten cofactor (Tuco), which carries tungsten in place of molybdenum as the metal constituent.

Accepted 24 February, 2008.

DIGITAL OBJECT IDENTIFIER (DOI)

10.1111/j.1365-2958.2008.06208.x About DOI