Structural basis of transcription-translation coupling

Wang, Chengyuan; Molodtsov, Vadim; Firlar, Emre; Kaelber, Jason T.; Blaha, Gregor; Su, Min; Ebright, Richard H.

doi:10.1101/2020.03.01.972380

Cited by 27 publications

(51 citation statements)

References 50 publications

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“…3 , Supplemental Discussion ). It remains possible that the accelerated speed in B. subtilis is driven by differences in the RNAP pause signals 26 or other components of the RNAP 10 , 11 ( Extended Data Fig. 4 , Supplementary Discussion ).…”

Section: Rnap Outpaces Pioneering Ribosomementioning

confidence: 99%

Functionally uncoupled transcription–translation in Bacillus subtilis

Johnson

Lalanne

Peters

et al. 2020

Nature

137

104

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Coupled transcription and translation is considered a defining feature of bacterial gene expression 1 , 2 . The pioneering ribosome can both physically associate and kinetically coordinate with the RNA polymerase (RNAP) 3 - 11 , forming a signal-integration hub for co-transcriptional regulation that includes translation-based attenuation 12 , 13 and RNA quality control 2 . However, whether transcription-translation coupling – together with its broad functional consequences – is indeed a fundamental characteristic outside the well-studied Escherichia coli remains unresolved. 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 a diminished role of Rho-dependent transcription termination, as well as the prevalence of mRNA leaders that utilize riboswitches and RNA-binding proteins. More broadly, we identified widespread genomic signatures of runaway transcription in distinct phyla across the bacterial domain of life. Our results demonstrate 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.

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Section: Rnap Outpaces Pioneering Ribosomementioning

confidence: 99%

Functionally uncoupled transcription–translation in Bacillus subtilis

Johnson

Lalanne

Peters

et al. 2020

Nature

137

104

View full text Add to dashboard Cite

show abstract

“…While our manuscript was under review, two preprints have been published reporting several structures of coupled complexes from E. coli ( Wang et al., 2020 ; Webster et al., 2020 ). Overall, the structures indicate that there are indeed various types of transcription:translation coupling modes, both direct and indirect coupling.…”

Section: Discussionmentioning

confidence: 99%

“…For example, the structure of the collided complex (see above [ Kohler et al., 2017 ]) was confirmed, but this coupling mode may be relevant only under certain conditions or when the RNA spacer is very short. In NusG-coupled complexes ( Wang et al., 2020 ; Webster et al., 2020 ) NusG bridges RNAP and ribosome with NusG-NTD contacting the RNAP at the expected binding site ( Kang et al., 2018 ) and NusG-CTD interacting with S10. This is similar to what was found for the binary NusG-CTD:S10 system ( Burmann et al., 2012 ) and is in agreement with our data.…”

Section: Discussionmentioning

confidence: 99%

“…As compared with the collided complex, RNAP is significantly rotated relative to the ribosome, but, interestingly, no stable contacts between RNAP and ribosome were observable ( Webster et al., 2020 ). However, more coupling modes are possible, emphasizing the complexity of the interplay between transcription and translation ( Wang et al., 2020 ; Webster et al., 2020 ).…”

Section: Discussionmentioning

confidence: 99%

“…Coupling may synchronize transcription and translation; in particular, the leading ribosome may “push” RNAP to overcome transcriptional pauses while RNAP could “pull” the ribosome to prevent/escape translational pausing ( Wang et al., 2020 ). In NusG-coupled complexes the small transcription factor may serve as cushion, conferring the system the flexibility necessary to keep transcription and translation synchronized, even if these processes are regulated differently or occur at different rates.…”

Section: Discussionmentioning

confidence: 99%

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Escherichia coli NusG Links the Lead Ribosome with the Transcription Elongation Complex

et al. 2020

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Summary It has been known for more than 50 years that transcription and translation are physically coupled in bacteria, but whether or not this coupling may be mediated by the two-domain protein N-utilization substance (Nus) G in Escherichia coli is still heavily debated. Here, we combine integrative structural biology and functional analyses to provide conclusive evidence that NusG can physically link transcription with translation by contacting both RNA polymerase and the ribosome. We present a cryo-electron microscopy structure of a NusG:70S ribosome complex and nuclear magnetic resonance spectroscopy data revealing simultaneous binding of NusG to RNAP and the intact 70S ribosome, providing the first direct structural evidence for NusG-mediated coupling. Furthermore, in vivo reporter assays show that recruitment of NusG occurs late in transcription and strongly depends on translation. Thus, our data suggest that coupling occurs initially via direct RNAP:ribosome contacts and is then mediated by NusG.

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Quantitative analysis of asynchronous transcription-translation and transcription processivity in Bacillus subtilis under various growth conditions

Zhu

Han

et al. 2021

iScience

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Tight coordination between transcription and translation has long been recognized as the hallmark of gene expression in bacteria. In Escherichia coli cells, disruption of the transcription-translation coordination leads to the loss of transcription processivity via triggering Rho-mediated premature transcription termination. Here we quantitatively characterize the transcription and translation kinetics in Gram-positive model bacterium Bacillus subtilis. We found that the speed of transcription elongation is much faster than that of translation elongation in B. subtilis under various growth conditions. Moreover, a Rho-independent loss of transcription processivity occurs constitutively in several genes/operons but is not subject to translational control. When the transcription elongation is decelerated under poor nutrients, low temperature, or nucleotide depletion, the loss of transcription processivity is strongly enhanced, suggesting that its degree is modulated by the speed of transcription elongation. Our study reveals distinct design principles of gene expression in E. coli and B. subtilis.

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Structural basis of transcription-translation coupling

Cited by 27 publications

References 50 publications

Functionally uncoupled transcription–translation in Bacillus subtilis

Functionally uncoupled transcription–translation in Bacillus subtilis

Escherichia coli NusG Links the Lead Ribosome with the Transcription Elongation Complex

Quantitative analysis of asynchronous transcription-translation and transcription processivity in Bacillus subtilis under various growth conditions

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