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Functionally uncoupled transcription–translation in Bacillus subtilis

Author

Listed:
  • Grace E. Johnson

    (Massachusetts Institute of Technology)

  • Jean-Benoît Lalanne

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Michelle L. Peters

    (Massachusetts Institute of Technology)

  • Gene-Wei Li

    (Massachusetts Institute of Technology)

Abstract

Tight coupling of transcription and translation is considered a defining feature of bacterial gene expression1,2. The pioneering ribosome can both physically associate and kinetically coordinate with RNA polymerase (RNAP)3–11, forming a signal-integration hub for co-transcriptional regulation that includes translation-based attenuation12,13 and RNA quality control2. However, it remains unclear whether transcription–translation coupling—together with its broad functional consequences—is indeed a fundamental characteristic of bacteria other than Escherichia coli. Here we show that RNAPs outpace pioneering ribosomes in the Gram-positive model bacterium Bacillus subtilis, and that this ‘runaway transcription’ creates alternative rules for both global RNA surveillance and translational control of nascent RNA. In particular, uncoupled RNAPs in B. subtilis explain the diminished role of Rho-dependent transcription termination, as well as the prevalence of mRNA leaders that use riboswitches and RNA-binding proteins. More broadly, we identified widespread genomic signatures of runaway transcription in distinct phyla across the bacterial domain. Our results show that coupled RNAP–ribosome movement is not a general hallmark of bacteria. Instead, translation-coupled transcription and runaway transcription constitute two principal modes of gene expression that determine genome-specific regulatory mechanisms in prokaryotes.

Suggested Citation

  • Grace E. Johnson & Jean-Benoît Lalanne & Michelle L. Peters & Gene-Wei Li, 2020. "Functionally uncoupled transcription–translation in Bacillus subtilis," Nature, Nature, vol. 585(7823), pages 124-128, September.
  • Handle: RePEc:nat:nature:v:585:y:2020:i:7823:d:10.1038_s41586-020-2638-5
    DOI: 10.1038/s41586-020-2638-5
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    Cited by:

    1. Yayun Zheng & Ruochen Chai & Tianmin Wang & Zeqi Xu & Yihui He & Ping Shen & Jintao Liu, 2024. "RNA polymerase stalling-derived genome instability underlies ribosomal antibiotic efficacy and resistance evolution," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Wenwen Yu & Ke Jin & Dandan Wang & Nankai Wang & Yangyang Li & Yanfeng Liu & Jianghua Li & Guocheng Du & Xueqin Lv & Jian Chen & Rodrigo Ledesma-Amaro & Long Liu, 2024. "De novo engineering of programmable and multi-functional biomolecular condensates for controlled biosynthesis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Manlu Zhu & Xiongfeng Dai, 2023. "Stringent response ensures the timely adaptation of bacterial growth to nutrient downshift," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Hualiang Pi & Andy Weiss & Clare L. Laut & Caroline M. Grunenwald & Hannah K. Lin & Xinjie I. Yi & Devin L. Stauff & Eric P. Skaar, 2022. "An RNA-binding protein acts as a major post-transcriptional modulator in Bacillus anthracis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Olga Iwańska & Przemysław Latoch & Natalia Kopik & Mariia Kovalenko & Małgorzata Lichocka & Remigiusz Serwa & Agata L. Starosta, 2024. "Translation in Bacillus subtilis is spatially and temporally coordinated during sporulation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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