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Dixon, N. E.

Publications and source records attributed to Dixon, N. E..

8 recordsLinked to original sources

Structural basis of the nucleotide incorporation cycle of bacterial DNA polymerase III

Bacterial DNA polymerase III (PolIII) is the primary replicative polymerase responsible for faithful genome duplication, yet high-resolution structural snapshots of the enzyme during DNA synthesis and proofreading have remained elusive. Here we determine cryo-EM structures of the Escherichia coli PolIII core-clamp-DNA binary, ternary and proofreading complexes at 2.4-2.7 [A] resolution, revealing the structural basis of nucleotide selection, incorporation and proofreading. Binding of an incoming nucleotide expels the single-stranded template overhang from the polymerase central channel and induces a large rotation of the polymerase index finger, which closes around the incoming nucleotide to form a compact nascent base-pair-binding pocket. A conserved tyrosine on the finger stacks against the incoming nucleotide to impose stringent steric constraints that promote nucleotide selection, whereas a conserved histidine acts as a steric gate to exclude ribonucleotides. The proofreading structures capture key intermediates that reveal how PolIII transfers a mismatched primer terminus to the 3'-5' exonuclease active site and excises the misincorporated nucleotide while avoiding unnecessary degradation of correctly paired DNA. Together, these findings define the molecular mechanism by which the bacterial replicative polymerase couples rapid and processive DNA synthesis with exceptional replication fidelity.

biochemistry↗

Structural characterisation of the complete cycle of sliding clamp loading in Escherichia coli

Ring-shaped DNA sliding clamps are essential for DNA replication and genome maintenance. Clamps need to be opened or trapped open and chaperoned onto DNA by clamp loader complexes (CLCs). Detailed understanding of the mechanisms by which CLCs open and place clamps around DNA remains limited. Here, we present a series of six structures of the Escherichia coli CLC bound to an open or closed clamp on and off a primer-template DNA that represent all intermediates in the clamp loading process. We show that the ATP-bound CLC first binds to a clamp, then constricts to hold onto it. The CLC then expands to open the clamp with a gap large enough for double-stranded DNA to enter. Upon binding to DNA, the CLC constricts slightly, allowing ATP hydrolysis and clamp closing around DNA. Although both yeast and E. coli CLCs open clamps by crab claw-like motions, they do it by the CLC expanding in opposite directions. These structures provide critical high-resolution snapshots of clamp loading by the E. coli CLC, revealing how the molecular machine works.

biochemistry↗

Single-molecule visualization of stalled replication-fork rescue by the Escherichia coli Rep helicase

Genome duplication occurs while the template DNA is bound by numerous DNA-binding proteins. Each of these proteins act as potential roadblocks to the replication fork and can have deleterious effects on cells. In Escherichia coli, these roadblocks are displaced by the accessory helicase Rep, a DNA translocase and helicase that interacts with the replisome. The mechanistic details underlying the coordination with replication and roadblock removal by Rep remain poorly understood. Through real-time fluorescence imaging of the DNA produced by individual E. coli replisomes and the simultaneous visualization of fluorescently-labeled Rep, we show that Rep continually surveils elongating replisomes. We found that this association of Rep with the replisome is stochastic and occurs independently of whether the fork is stalled or not. Further, we visualize the efficient rescue of stalled replication forks by directly imaging individual Rep molecules as they remove a model protein roadblock, dCas9, from the template DNA. Using roadblocks of varying DNA-binding stabilities, we conclude that replication restart is the rate-limiting step of stalled replication rescue.

biochemistry↗

The E. coli helicase does not use ATP during replication.

The replisome is responsible for replication of DNA in all domains of life, with several of its individual enzyme components relying on hydrolysis of nucleoside triphosphates to provide energy for replisome function. Half a century of biochemical studies have demonstrated a dependence on ATP as an energy source for helicases to unwind duplex DNA during replication. Through single-molecule visualization of DNA replication by the Escherichia coli replisome, we demonstrate that the DnaB helicase does not rely on hydrolysis of ATP (or any ribo-NTPs) in the context of the elongating replisome. We establish that nucleotide incorporation by the leading-strand polymerase is the main motor driving the replication process. One Sentence SummaryPolymerases provide the energy for helicase-mediated DNA unwinding during E. coli DNA replication.

biochemistry↗

Mechanism of transcription modulation by the transcription-repair coupling factor

Elongation by RNA polymerase is dynamically modulated by accessory factors. The transcription-repair coupling factor (TRCF) recognizes distressed RNAPs and either rescues transcription or initiates transcription termination. Precisely how TRCFs choose to execute either outcome remains unclear. With Escherichia coli as a model, we used single-molecule assays to study dynamic modulation of elongation by Mfd, the bacterial TRCF. We found that nucleotide-bound Mfd converts the elongation complex (EC) into a catalytically poised state, presenting the EC with an opportunity to restart transcription. After long-lived residence in this catalytically poised state, ATP hydrolysis by Mfd remodels the EC through an irreversible process leading to loss of the RNA transcript. Further, biophysical studies revealed that the motor domain of Mfd binds and partially melts DNA containing a template strand overhang. The results explain pathway choice determining the fate of the EC and provide a molecular mechanism for transcription modulation by TRCF.

biophysics↗

Recycling of single-stranded DNA-binding protein by the bacterial replisome.

Single-stranded DNA-binding proteins (SSBs) support DNA replication by protecting single-stranded DNA from nucleolytic attack, preventing intra-strand pairing events, and playing many other regulatory roles within the replisome. Recent developments in single-molecule approaches have led to a revised picture of the replisome that is much more complex in how it retains or recycles protein components. Here we visualise how an in vitro reconstituted E. coli replisome recruits SSB by relying on two different molecular mechanisms. Not only does it recruit new SSB molecules from solution to coat newly formed single-stranded DNA on the lagging strand, but it also internally recycles SSB from one Okazaki fragment to the next. We show that this internal transfer mechanism is balanced against recruitment from solution in a manner that is concentration dependent. By visualising SSB dynamics in live cells, we show that both internal transfer and external exchange mechanisms are physiologically relevant.

biophysics↗

A Primase-Induced Conformational Switch Controls the Stability of the Bacterial Replisome

Recent studies of bacterial DNA replication have led to a picture of the replisome as an entity that freely exchanges DNA polymerases and displays intermittent coupling between the helicase and polymerase(s). Challenging the textbook model of the polymerase holoenzyme acting as a stable complex coordinating the replisome, these observations suggest a role of the helicase as the central organizing hub. We show here that the molecular origin of this newly-found plasticity lies in the >400-fold increase in strength of the interaction between the polymerase holoenzyme and the replicative helicase upon association of the primase with the replisome. By combining in vitro ensemble-averaged and single-molecule assays, we demonstrate that this conformational switch operates during replication and promotes recruitment of multiple holoenzymes at the fork. Our observations provide a molecular mechanism for polymerase exchange and offer a revised model for the replication reaction that emphasizes its stochasticity.

biochemistry↗

Nuclease dead Cas9 is a programmable roadblock for DNA replication

DNA replication occurs on chromosomal DNA while processes such as DNA repair, recombination and transcription continue. However, we have limited experimental tools to study the consequences of collisions between DNA-bound molecular machines. Here, we repurpose a catalytically inactivated Cas9 (dCas9) construct fused to the photo-stable dL5 protein fluoromodule as a novel, targetable protein-DNA roadblock for studying replication fork arrest at the single-molecule level in vitro as well as in vivo. We find that the specifically bound dCas9-guideRNA complex arrests viral, bacterial and eukaryotic replication forks in vitro.

biochemistry↗