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Divergent rRNAs as regulators of gene expression at the ribosome level

Nature Microbiology volume 4, pages 515–526 (2019)Cite this article

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Abstract

It is generally assumed that each organism has evolved to possess a unique ribosomal RNA (rRNA) species optimal for its physiological needs. However, some organisms express divergent rRNAs, the functional roles of which remain unknown. Here, we show that ribosomes containing the most variable rRNAs, encoded by the rrnI operon (herein designated as I-ribosomes), direct the preferential translation of a subset of mRNAs in Vibrio vulnificus, enabling the rapid adaptation of bacteria to temperature and nutrient shifts. In addition, genetic and functional analyses of I-ribosomes and target mRNAs suggest that both I-ribosomal subunits are required for the preferential translation of specific mRNAs, the Shine–Dalgarno sequences of which do not play a critical role in I-ribosome binding. This study identifies genome-encoded divergent rRNAs as regulators of gene expression at the ribosome level, providing an additional level of regulation of gene expression in bacteria in response to environmental changes.

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Fig. 1: Identification of mRNAs with rrnI-dependent expression.
Fig. 2: rrnI-dependent expression of hspA.
Fig. 3: rrnI-dependent expression of tpiA and phenotypic changes in V. vulnificus.
Fig. 4: Effect of rrnI deletion on the virulence of V. vulnificus in mice.
Fig. 5: Identification of variable residues in I-rRNAs associated with rrnI-dependent expression of hspA mRNAs.
Fig. 6: Characterization of I-ribosome-mediated preferential mRNA selection.

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Data availability

Ribosome profiling and transcriptome data have been deposited into the Gene Expression Ominbus (GEO) and are available under identifier GSE111991. Proteome data have been deposited into PRIDE and are available via ProteomeXchange under identifier PXD009215.

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Acknowledgements

We thank K.-H. Lee, Y. Lee and S. N. Cohen for helpful comments. This research was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (grant no. 2018R1A5A1025077 and 2017R1A2B2011008 to K.L.; grant no. 2015R1A5A1008958 to J.B. and H.-K.C.; grant no. 2017R1D1A1B03032197 to W.S.; and grant no. 2018R1D1A1B07050434 to J.-H.Y.).

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  1. These authors contributed equally: Wooseok Song, Minju Joo, Ji-Hyun Yeom, Eunkyoung Shin and Minho Lee.

Authors and Affiliations

  1. Department of Life Science, Chung-Ang University, Seoul, Republic of Korea

    Wooseok Song, Minju Joo, Ji-Hyun Yeom, Minho Lee, Seong-il Eyun, Yoonsoo Hahn & Kangseok Lee

  2. School of Pharmacy, Chung-Ang University, Seoul, Republic of Korea

    Eunkyoung Shin, Hyung-Kyoon Choi & Jeehyeon Bae

  3. Department of Microbiology, Pusan National University, Busan, Republic of Korea

    Jihwan Hwang

  4. Center for Bioanalysis, Korea Research Institute of Standards and Science, Daejeon, Republic of Korea

    Yong-In Kim, Ramin Seo & J. Eugene Lee

  5. Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea

    Ramin Seo

  6. Department of Genetics, Stanford University, Stanford, CA, USA

    Christopher J. Moore

  7. Department of Microbiology, Catholic University of Daegu School of Medicine, Daegu, Republic of Korea

    Yong-Hak Kim

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Contributions

W.S., M.J., J.-H.Y., E.S., M.L., Y.-I.K. and R.S. performed the experiments. Y.H., H.-K.C., J.H., J.E.L., C.J.M., Y.-H.K., S.E., Y.H., J.B. and K.L. analysed and interpreted the data. W.S., M.J., J.-H.Y., E.S., M.L., J.B. and K.L. wrote and reviewed the manuscript. J.B. and K.L designed the study, developed the methodology and supervised the study. All authors discussed the results and commented on the manuscript.

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Correspondence to Jeehyeon Bae or Kangseok Lee.

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Supplementary Information

Supplementary Figures 1–13, Supplementary Table 1, Supplementary Tables 3–8, Supplementary Discussion, Supplementary References.

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Supplementary Table 2

List of genes obtained from ribosome profiling and transcriptome data.

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Song, W., Joo, M., Yeom, JH. et al. Divergent rRNAs as regulators of gene expression at the ribosome level. Nat Microbiol 4, 515–526 (2019). https://doi.org/10.1038/s41564-018-0341-1

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