A trailing ribosome speeds up RNA polymerase at the expense of transcript fidelity via force and allostery

Wee, Liang M.; Tong, Alexander B.; Ariza, Alfredo Jose Florez; Cañari-Chumpitaz, Cristhian; Grob, Patricia; Nogales, Eva; Bustamante, Carlos

doi:10.1016/j.cell.2023.02.008

Cited by 26 publications

(25 citation statements)

References 194 publications

(188 reference statements)

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“…In a recent study, the trailing ribosome is shown to increase the speed of RNAP. 37 From these results, it appears that the difference in the transcript elongation rates of E. coli and M. tuberculosis RNAP is not as much as the difference in their growth rates (μ), which differ by 44-fold (M. tuberculosis μ = 0.039 and E. coli μ = 1.730). 38−40 Thus, at first glance, the correlation between transcription elongation and growth rates seems to be less significant.…”

Section: ■ Discussionmentioning

confidence: 87%

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Comparison of Transcription Elongation Rates of Three RNA Polymerases in Real Time

Tare,

Bhowmick,

Katagi

et al. 2023

ACS Omega

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RNA polymerases (RNAPs) across the bacterial kingdom have retained a conserved structure and function. In spite of the remarkable similarity of the enzyme in different bacteria, a wide variation is found in the promoter–polymerase interaction, transcription initiation, and termination. However, the transcription elongation was considered to be a monotonic process, although the rate of elongation could vary in different bacteria. Such variations in RNAP elongation rates could be important to fine-tune the transcription, which in turn would influence cellular metabolism and growth rates. Here, we describe a quantitative study to measure the transcription rates for the RNAPs from three bacteria, namely, Mycobacterium tuberculosis , Mycobacterium smegmatis , and Escherichia coli , which exhibit different growth kinetics. The RNA synthesis rates of the RNAPs were calculated from the real-time elongation kinetic profile using surface plasmon resonance through a computational flux flow model. The computational model revealed the modular process of elongation, with different rate profiles for the three RNAPs. Notably, the transcription elongation rates of these RNAPs followed the trend in the growth rates of these bacteria.

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Section: ■ Discussionmentioning

confidence: 87%

“…Notably, the in vivo elongation rates will be influenced by various elongation factors that facilitate pause or relieve the pause. In a recent study, the trailing ribosome is shown to increase the speed of RNAP …”

Section: Discussionmentioning

confidence: 94%

Comparison of Transcription Elongation Rates of Three RNA Polymerases in Real Time

Tare,

Bhowmick,

Katagi

et al. 2023

ACS Omega

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“…Beyond their application in chromatin studies, single-molecule manipulation techniques have also been extensively employed to explore the dynamics of various molecular motors. These include RNA polymerase, , ribosome, DNA helicase, and DNA topoisomerase . This broad application spectrum underscores the versatility and significance of single-molecule manipulation in understanding complex biological processes.…”

Section: Nucleosome Assembly and Chiralitymentioning

confidence: 99%

Nucleosome Dynamics Derived at the Single-Molecule Level Bridges Its Structures and Functions

Chen,

Li,

2024

JACS Au

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Nucleosome, the building block of chromatin, plays pivotal roles in all DNA-related processes. While cryogenic-electron microscopy (cryo-EM) has significantly advanced our understanding of nucleosome structures, the emerging field of single-molecule force spectroscopy is illuminating their dynamic properties. This technique is crucial for revealing how nucleosome behavior is influenced by chaperones, remodelers, histone variants, and posttranslational modifications, particularly in their folding and unfolding mechanisms under tension. Such insights are vital for deciphering the complex interplay in nucleosome assembly and structural regulation, highlighting the nucleosome's versatility in response to DNA activities. In this Perspective, we aim to consolidate the latest advancements in nucleosome dynamics, with a special focus on the revelations brought forth by single-molecule manipulation. Our objective is to highlight the insights gained from studying nucleosome dynamics through this innovative approach, emphasizing the transformative impact of single-molecule manipulation techniques in the field of chromatin research.

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“…For example, the (Wang et al, 2020); 6ZTO, 6ZTM, 6ZTJ (Webster et al, 2020); 6AWB, 6AWC (Demo et al, 2017); 5MY1-available PDB deposition is of EC and 30S subunit only (Kohler et al, 2017) likely through physical pushing (Proshkin et al, 2010;Stevenson-Jones et al, 2020). More recent biochemical and single-molecule analyses showed that a coupled ribosome can increase transcription processivity, though at the expense of fidelity of RNA synthesis, through mechanical and allosteric means (Wee et al, 2023). These findings are corroborated by in vivo observations that the ribosome appears to assist the progression of EC inhibited by carbon starvation, while average rates of transcription are reduced when translation is inhibited under nitrogen-limiting conditions (Iyer et al, 2018).…”

Section: Thecl a Ss I C Sofc T Tmentioning

confidence: 99%

Transcription–translation coupling: Recent advances and future perspectives

Woodgate

Zenkin

2023

Molecular Microbiology

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The flow of genetic information from the chromosome to protein in all living organisms consists of two steps: (1) copying information coded in DNA into an mRNA intermediate via transcription by RNA polymerase, followed by (2) translation of this mRNA into a polypeptide by the ribosome. Unlike eukaryotes, where transcription and translation are separated by a nuclear envelope, in bacterial cells, these two processes occur within the same compartment. This means that a pioneering ribosome starts translation on nascent mRNA that is still being actively transcribed by RNA polymerase. This tethering via mRNA is referred to as ‘coupling’ of transcription and translation (CTT). CTT raises many questions regarding physical interactions and potential mutual regulation between these large (ribosome is ~2.5 MDa and RNA polymerase is 0.5 MDa) and powerful molecular machines. Accordingly, we will discuss some recently discovered structural and functional aspects of CTT.

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A trailing ribosome speeds up RNA polymerase at the expense of transcript fidelity via force and allostery

Cited by 26 publications

References 194 publications

Comparison of Transcription Elongation Rates of Three RNA Polymerases in Real Time

Comparison of Transcription Elongation Rates of Three RNA Polymerases in Real Time

Nucleosome Dynamics Derived at the Single-Molecule Level Bridges Its Structures and Functions

Transcription–translation coupling: Recent advances and future perspectives

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