Two Old Dogs, One New Trick: A Review of RNA Polymerase and Ribosome Interactions during Transcription-Translation Coupling

Conn, Adam; Diggs, Stephen; Tam, Timothy K.; Blaha, Gregor

doi:10.3390/ijms20102595

Cited by 22 publications

(21 citation statements)

References 88 publications

(127 reference statements)

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“…How do the transcriptional and translational machineries intimately interact? Several recent publications have shed light on the molecular interactions that mediate the physical coupling of transcription and translation in E. coli , although their conclusions were not always in agreement (reviewed by Conn et al, 2019 ). CTT was initially proposed to be mediated by NusG.…”

Section: The Molecular Architecture Of Cttmentioning

confidence: 99%

Coupled Transcription-Translation in Prokaryotes: An Old Couple With New Surprises

Irastortza-Olaziregi

Amster‐Choder

2021

Front. Microbiol.

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Coupled transcription-translation (CTT) is a hallmark of prokaryotic gene expression. CTT occurs when ribosomes associate with and initiate translation of mRNAs whose transcription has not yet concluded, therefore forming “RNAP.mRNA.ribosome” complexes. CTT is a well-documented phenomenon that is involved in important gene regulation processes, such as attenuation and operon polarity. Despite the progress in our understanding of the cellular signals that coordinate CTT, certain aspects of its molecular architecture remain controversial. Additionally, new information on the spatial segregation between the transcriptional and the translational machineries in certain species, and on the capability of certain mRNAs to localize translation-independently, questions the unanimous occurrence of CTT. Furthermore, studies where transcription and translation were artificially uncoupled showed that transcription elongation can proceed in a translation-independent manner. Here, we review studies supporting the occurrence of CTT and findings questioning its extent, as well as discuss mechanisms that may explain both coupling and uncoupling, e.g., chromosome relocation and the involvement of cis- or trans-acting elements, such as small RNAs and RNA-binding proteins. These mechanisms impact RNA localization, stability, and translation. Understanding the two options by which genes can be expressed and their consequences should shed light on a new layer of control of bacterial transcripts fate.

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Section: The Molecular Architecture Of Cttmentioning

confidence: 99%

Coupled Transcription-Translation in Prokaryotes: An Old Couple With New Surprises

Irastortza-Olaziregi

Amster‐Choder

2021

Front. Microbiol.

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“…We next investigated how AZM alters gene expression in P. aeruginosa, since bacterial transcription and translation are coupled [55][56][57]. To understand the acute response of P. aeruginosa to AZM, planktonic cultures were treated with the antibiotic for a short duration (20 minutes).…”

Section: The Effects Of Azm On P Aeruginosa Gene Expressionmentioning

confidence: 99%

“…Translation efficiency is also positively correlated with tRNA levels [108]. Since bacterial transcription is co-translational [55][56][57]107], it is likely that increased levels of uncharged tRNAs that pair with certain rare codons impacts the transcription of genes enriched for codons that pair with them in P.…”

Section: The Effects Of Azm On P Aeruginosa Gene Expressionmentioning

confidence: 99%

“…Translation inhibition is hence thought to account for QS inhibition, which in turn inhibits biofilm formation and virulence gene expression by AZM in P. aeruginosa. Because transcription elongation and mRNA translation are spatio-temporally coupled in bacteria [55][56][57], the translation stalling caused by AZM could directly alter the production of full-length transcripts from QS genes and transcriptional regulators of the stress response. The extent of reduced transcriptional processivity due to AZM treatment remains an important unresolved question because methods used in previous studies lacked the resolution to differentiate between premature and full-length mRNA transcripts.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Quantitative mapping of mRNA 3’ ends inPseudomonas aeruginosareveals a pervasive role for premature 3’ end formation in response to azithromycin

Konikkat

Scribner

Eutsey

et al. 2020

Preprint

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P. aeruginosa produces serious chronic infections in hospitalized patients and immunocompromised individuals, including cystic fibrosis patients. The molecular mechanisms by which P. aeruginosa responds to antibiotics and other stresses to promote persistent infections may provide new avenues for therapeutic intervention. Azithromycin (AZM), an antibiotic frequently used in cystic fibrosis treatment, is thought to improve clinical outcomes through a number of mechanisms including impaired biofilm growth and QS. The mechanisms underlying the transcriptional response to AZM remain unclear. Here, we interrogated the P. aeruginosa transcriptional response to AZM using an improved genomewide approach to quantitate RNA 3'-ends (3pMap). We also identified hundreds of P.aeruginosa genes subject to premature transcription termination in their transcript leaders using 3pMap. AZM treatment of planktonic and biofilm cultures alters the expression of hundreds of genes, including those involved in QS, biofilm formation, and virulence.Strikingly, most genes downregulated by AZM in biofilms had increased levels of intragenic 3'-ends indicating premature transcription termination or pausing. Reciprocally, AZM reduced premature transcription termination in many upregulated genes. Most notably, reduced termination accompanied robust induction of obgE, a GTPase involved in persister formation in P. aeruginosa. Our results support a model in which AZM-induced premature transcription termination downregulates expression of central transcriptional regulators, which in turn both impairs QS and biofilm formation, and stress responses, while upregulating genes associated with persistence.

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“…Since the late 1960s it has been known that the rates of transcription and translation are synchronized in Escherichia coli (E. coli) so that mRNA is translated while being transcribed ( Das et al., 1967 ; Mehdi and Yudkin, 1967 ; Miller et al., 1970 ; Proshkin et al., 2010 ; Vogel and Jensen, 1994 , 1995 ). This process, called transcription:translation coupling, is possible due to the lack of a physical barrier between transcription and translation in bacteria (reviewed in Conn et al., 2019 ). Only recently, direct physical interactions between RNA polymerase (RNAP) and the ribosome have been demonstrated ( Demo et al., 2017 ; Fan et al., 2017 ; Kohler et al., 2017 ), consistent with earlier observations that transcriptional events may control translation activity and vice versa ( Proshkin et al., 2010 ).…”

Section: Introductionmentioning

confidence: 99%

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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Two Old Dogs, One New Trick: A Review of RNA Polymerase and Ribosome Interactions during Transcription-Translation Coupling

Cited by 22 publications

References 88 publications

Coupled Transcription-Translation in Prokaryotes: An Old Couple With New Surprises

Coupled Transcription-Translation in Prokaryotes: An Old Couple With New Surprises

Quantitative mapping of mRNA 3’ ends inPseudomonas aeruginosareveals a pervasive role for premature 3’ end formation in response to azithromycin

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

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