DciA is an ancestral replicative helicase operator essential for bacterial replication initiation

Brézellec, Pierre; Vallet-Gély, Isabelle; Possoz, Christophe; Quevillon‐Chéruel, Sophie; Ferat, Jean-Luc

doi:10.1038/ncomms13271

Cited by 35 publications

(68 citation statements)

References 22 publications

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“…In this regard, a bacteriophage clamp loader system would seem to act in a manner akin to ORC,Cdc6 during MCM2-7 loading. By contrast, the DnaI family of replicative helicase loaders, which are close evolutionary cousins of DnaC, has been reported to assemble helicase protomers around DNA (Soultanas, 2002;Velten et al, 2003), thereby acting through a distinct type of ''ring-maker'' mechanism (Davey and O'Donnell, 2003); the mechanism of helicase deposition by a third class of loader, DciA, is unknown (Bré zellec et al, 2016). Although we expect that the molecular approach by which DnaC and DnaI loaders engage their client helicases will be analogous, sequence alignments between the NTDs of these two loader families reveal little similarity ( Figure S7).…”

Section: Mechanistic Insights Into Ring-loading Reactionsmentioning

confidence: 99%

Physical Basis for the Loading of a Bacterial Replicative Helicase onto DNA

et al. 2019

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In cells, dedicated AAA+ ATPases deposit hexameric, ring-shaped helicases onto DNA to initiate chromosomal replication. To better understand the mechanisms by which helicase loading can occur, we used cryo-EM to determine sub-4-Å -resolution structures of the E. coli DnaB,DnaC helicase,loader complex with nucleotide in pre-and post-DNA engagement states. In the absence of DNA, six DnaC protomers latch onto and crack open a DnaB hexamer using an extended N-terminal domain, stabilizing this conformation through nucleotide-dependent ATPase interactions. Upon binding DNA, DnaC hydrolyzes ATP, allowing DnaB to isomerize into a topologically closed, pre-translocation state competent to bind primase. Our data show how DnaC opens the DnaB ring and represses the helicase prior to DNA binding and how DnaC ATPase activity is reciprocally regulated by DnaB and DNA. Comparative analyses reveal how the helicase loading mechanism of DnaC parallels and diverges from homologous AAA+ systems involved in DNA replication and transposition.Supplemental Information includes seven figures and six videos and can be found with this article online at https://doi.

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Section: Mechanistic Insights Into Ring-loading Reactionsmentioning

confidence: 99%

Physical Basis for the Loading of a Bacterial Replicative Helicase onto DNA

et al. 2019

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“…In Helicobacter pylori, the only replication restart protein identified is PriA (reviewed in reference 61). Like all bacteria that lack homologues of the E. coli DnaC and B. subtilis DnaI helicase loaders, H. pylori encodes a protein called DciA, which represents a third class of helicase loader (62). Replication restart proteins have been characterized genetically and biochemically in several bacterial species.…”

Section: Replication Restart In Bacteria Other Than E Colimentioning

confidence: 99%

Replication Restart in Bacteria

Michel

Sandler²

2017

J Bacteriol

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In bacteria, replication forks assembled at a replication origin travel to the terminus, often a few megabases away. They may encounter obstacles that trigger replisome disassembly, rendering replication restart from abandoned forks crucial for cell viability. During the past 25 years, the genes that encode replication restart proteins have been identified and genetically characterized. In parallel, the enzymes were purified and analyzed in vitro, where they can catalyze replication initiation in a sequence-independent manner from fork-like DNA structures. This work also revealed a close link between replication and homologous recombination, as replication restart from recombination intermediates is an essential step of DNA double-strand break repair in bacteria and, conversely, arrested replication forks can be acted upon by recombination proteins and converted into various recombination substrates. In this review, we summarize this intense period of research that led to the characterization of the ubiquitous replication restart protein PriA and its partners, to the definition of several replication restart pathways in vivo, and to the description of tight links between replication and homologous recombination, responsible for the importance of replication restart in the maintenance of genome stability.KEYWORDS DNA replication, homologous recombination R eplication of a circular bacterial chromosome normally initiates at a unique origin. For bidirectional DNA replication, two replication forks are established that replicate the DNA in opposite directions until they meet in the terminus region. Replication fork progression involves the coordinated action of two complexes, the primosome to open the DNA duplex and synthesize primers and the replisome to catalyze the concerted DNA synthesis of both DNA strands. The two DNA strands at the replication fork are antiparallel, and DNA synthesis occurs only in the 5=-to-3= direction. Therefore, to synthesize both strands in a concerted and semiconservative fashion, one strand is synthesized mainly continuously (the leading strand) and the other is synthesized discontinuously (the lagging strand). The fragments generated on the discontinuous strand are 1 to 2 kb in length and are called Okazaki fragments (OF). In Escherichia coli, the primosome is composed of the DnaB helicase that opens the parental strands and the DnaG primase that interacts transiently with DnaB and synthesizes the RNA primers at the onset of each OF synthesis. DnaB is a hexameric helicase that encircles singlestranded DNA (ssDNA) and translocates on the lagging-strand template in a 5=-to-3= direction. The DNA polymerase III holoenzyme (Pol III HE) synthesizes both nascent DNA strands, and its action is stimulated by interactions with DnaB and with the ssDNA binding protein (SSB) that covers the lagging-strand template (1).The first committed step in the assembly of a replication fork is DnaB loading. In bacteria, two pathways for DnaB loading have been described, a sequence-specific, DnaA-dep...

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“…dciA was replaced in the bacterial domain multiple times by viral proteins, at least seven times by dnaC/I (Brezellec et al 2016) and potentially once or more by dopE . This suggests limited adjustments and likely requires the predomesticated gene to belong to a phage that employs the host replicative helicase for its own replication.…”

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confidence: 99%

Domestication of Lambda Phage Genes into a Putative Third Type of Replicative Helicase Matchmaker

Brézellec

Petit

Pasek

et al. 2017

Genome Biology and Evolution

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At the onset of the initiation of chromosome replication, bacterial replicative helicases are recruited and loaded on the DnaA-oriC nucleoprotein platform, assisted by proteins like DnaC/DnaI or DciA. Two orders of bacteria appear, however, to lack either of these factors, raising the question of the essentiality of these factors in bacteria. Through a phylogenomic approach, we identified a pair of genes that could have substituted for dciA. The two domesticated genes are specific of the dnaC/dnaI- and dciA-lacking organisms and apparently domesticated from lambdoid phage genes. They derive from λO and λP and were renamed dopC and dopE, respectively. DopE is expected to bring the replicative helicase to the bacterial origin of replication, while DopC might assist DopE in this function. The confirmation of the implication of DopCE in the handling of the replicative helicase at the onset of replication in these organisms would generalize to all bacteria and therefore to all living organisms the need for specific factors dedicated to this function.

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DciA is an ancestral replicative helicase operator essential for bacterial replication initiation

Cited by 35 publications

References 22 publications

Physical Basis for the Loading of a Bacterial Replicative Helicase onto DNA

Physical Basis for the Loading of a Bacterial Replicative Helicase onto DNA

Replication Restart in Bacteria

Domestication of Lambda Phage Genes into a Putative Third Type of Replicative Helicase Matchmaker

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