Temperature-responsive in vitro RNA structurome of Yersinia pseudotuberculosis

Francesco Righetti, Aaron M. Nuss, Christian Twittenhoff, Sascha Beele, Kristina Urban, Sebastian Will, Stephan H. Bernhart, Peter F. Stadler, Petra Dersch, and Franz Narberhaus
PNAS published ahead of print June 13, 2016 https://doi.org/10.1073/pnas.1523004113

  1. Edited by Gisela Storz, National Institutes of Health, Bethesda, MD, and approved May 12, 2016 (received for review November 20, 2015)

Significance

The RNA structure is critical for RNA function in all domains of life. We determined the transcriptome-wide RNA structurome of Yersinia pseudotuberculosis, a food-borne pathogen, at three physiologically relevant temperatures. Our analysis shows that mRNAs tend to have a poorly structured ribosome binding site. Transcripts that deviate from this general principle are very good candidates as translational repressor elements, and we identified 16 RNA thermometers able to control gene expression in a temperature-dependent manner. Our analysis demonstrates the power of high-throughput RNA structure probing approaches to identify new sensory and regulatory RNA structures.

Abstract

RNA structures are fundamentally important for RNA function. Dynamic, condition-dependent structural changes are able to modulate gene expression as shown for riboswitches and RNA thermometers. By parallel analysis of RNA structures, we mapped the RNA structurome of Yersinia pseudotuberculosis at three different temperatures. This human pathogen is exquisitely responsive to host body temperature (37 °C), which induces a major metabolic transition. Our analysis profiles the structure of more than 1,750 RNAs at 25 °C, 37 °C, and 42 °C. Average mRNAs tend to be unstructured around the ribosome binding site. We searched for 5′-UTRs that are folded at low temperature and identified novel thermoresponsive RNA structures from diverse gene categories. The regulatory potential of 16 candidates was validated. In summary, we present a dynamic bacterial RNA structurome and find that the expression of virulence-relevant functions in Y. pseudotuberculosis and reprogramming of its metabolism in response to temperature is associated with a restructuring of numerous mRNAs.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: franz.narberhaus{at}rub.de.

  • Author contributions: F.R., A.M.N., P.D., and F.N. designed research; F.R., A.M.N., C.T., S.B., and K.U. performed research; F.R., A.M.N., C.T., S.W., S.H.B., P.F.S., P.D., and F.N. analyzed data; and F.R., S.W., P.F.S., P.D., and F.N. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited at the homepage of the Bioinformatics Institute at the University of Leipzig, www.bioinf.uni-leipzig.de/publications/supplements/16-001.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1523004113/-/DCSupplemental.

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RNA structures of Yersinia pseudotuberculosis
Francesco Righetti, Aaron M. Nuss, Christian Twittenhoff, Sascha Beele, Kristina Urban, Sebastian Will, Stephan H. Bernhart, Peter F. Stadler, Petra Dersch, Franz Narberhaus
Proceedings of the National Academy of Sciences Jun 2016, 201523004; DOI: 10.1073/pnas.1523004113
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