Operon mRNAs are organized into ORF-centric structures that predict translation efficiency
- University of California, San Francisco, United States
- Howard Hughes Medical Institute, University of California, San Francisco, United States
- Massachusetts Institute of Technology, United States
Abstract
Bacterial mRNAs are organized into operons consisting of discrete open reading frames (ORFs) in a single polycistronic mRNA. Individual ORFs on the mRNA are differentially translated, with rates varying as much as 100-fold. The signals controlling differential translation are poorly understood. Our genome-wide mRNA secondary structure analysis indicated that operonic mRNAs are comprised of ORF-wide units of secondary structure that vary across ORF boundaries such that adjacent ORFs on the same mRNA molecule are structurally distinct. ORF translation rate is strongly correlated with its mRNA structure in vivo, and correlation persists, albeit in a reduced form, with its structure when translation is inhibited and with that of in vitro refolded mRNA. These data suggests that intrinsic ORF mRNA structure encodes a rough blueprint for translation efficiency. This structure is then amplified by translation, in a self-reinforcing loop, to provide the structure that ultimately specifies the translation of each ORF.
Data availability
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Operon mRNAs are organized into ORF-centric structures that predict translation efficiencyPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE77617).
Article and author information
Author details
Jonathan S Weissman
Funding
Howard Hughes Medical Institute
- Jonathan S Weissman
National Institutes of Health
- David H Burkhardt
- Yan Zhang
- Carol A Gross
Helen Hay Whitney Foundation
- Gene-Wei Li
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Rachel Green, Johns Hopkins School of Medicine, United States
Version history
- Received: October 3, 2016
- Accepted: January 27, 2017
- Accepted Manuscript published: January 31, 2017 (version 1)
- Version of Record published: February 20, 2017 (version 2)
Copyright
© 2017, Burkhardt et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Operon mRNAs are organized into ORF-centric structures that predict translation efficiency
eLife 6:e22037.
https://doi.org/10.7554/eLife.22037
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