Convergent evolution in two bacterial replicative helicase loaders

Chase, Jillian; Jeruzalmi, David

doi:10.1016/j.tibs.2022.02.005

Cited by 8 publications

(19 citation statements)

References 117 publications

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“…The two genes coding for DciA and DnaC/I are unrelated and mutually exclusive in the bacterial genomes (Brézellec, Petit et al, 2017, Brézellec et al, 2016. However, like DnaC and the bacteriophage λ P helicase loader (Arias-Palomo et al, 2019, Chase et al, 2022, Chase et al, 2018, DciA interacts with the two-helix LH-DH module of DnaB. This "binding module", conserved in the bacterial replicative helicases, suggests a functional link between the different systems.…”

Section: Discussionmentioning

confidence: 99%

“…The LH-DH module is conserved in DnaB helicases (Chase et al, 2022). However, we have previously identified a residue in the DH helix that discriminates DciA helicases from DnaC/I helicases (respectively a serine and a glycine) (Marsin et al, 2021) (Figure 2A).…”

Section: Both Vcdcia and Ecdnac Loaders Target The Conserved Lh-dh Mo...mentioning

confidence: 96%

“…EcDnaC makes EcDnaB contacts through the first small α-helix (15 residues long) of its extended N-terminal domain (NTD). This helix interacts with the DnaB module composed of the "linker helix" (LH) of one DnaB protomer and of an antiparallel α-helix of the adjacent DnaB protomer, which we named "determinant helix" (DH) in a previous study (Marsin, Adam et al, 2021), and was named "docking helix" in a recent review comparing the convergent functional mechanisms of EcDnaC and bacteriophage λ P loaders (Chase, Berger et al, 2022). This forms a three α-helix bundle, which fixes the relative orientation of the two adjacent DnaB C-terminal domains (CTDs): the 6 DnaC thus latched onto the DnaB hexamer adopt a spiral configuration that causes a distortion in the helicase ring, resulting in its large opening as a means to allow single-strand DNA (ssDNA) to enter the helicase pore (Arias-Palomo et al, 2019, Nagata et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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The LH-DH module of the bacterial replicative helicases is the common binding site for DciA and other helicase loaders

Cargemel

Marsin

Noiray

et al. 2022

Preprint

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During the initiation step of bacterial genome replication, replicative helicases depend on specialized proteins for their loading onto oriC. DnaC and DnaI were the first loaders characterized. However, most bacteria do not contain any of these genes, which are domesticated phage elements that replaced the ancestral and unrelated loader gene dciA several times during evolution. To understand how DciA assists the loading of DnaB, we determined the crystal structure of the complex from Vibrio cholerae, in which two VcDciAs interact with a dimer of VcDnaB, without changing its canonical structure. Our data showed that the VcDciA binding site on VcDnaB is the conserved module formed by the linker helix LH of one monomer and the determinant helix DH of the second one. Interestingly, DnaC from Escherichia coli also targets this module onto EcDnaB. Thanks to their common target site, we showed that VcDciA and EcDnaC could be functionally interchanged in vitro, despite sharing no structural similarities. This is a milestone in understanding the mechanism employed by phage helicase loaders to hijack bacterial replicative helicases during evolution.

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Section: Discussionmentioning

confidence: 99%

Section: Both Vcdcia and Ecdnac Loaders Target The Conserved Lh-dh Mo...mentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

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The LH-DH module of the bacterial replicative helicases is the common binding site for DciA and other helicase loaders

Cargemel

Marsin

Noiray

et al. 2022

Preprint

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“…The copyright holder for this preprint (which this version posted May 5, 2022. ; https://doi.org/10.1101/2022.01. 24.477630 doi: bioRxiv preprint via domestication of related but distinct phage ATPase-containing genes (28)(29)(30)(31). DnaC and DnaI are both in the ATPases Associated with diverse cellular Activities (AAA+) ATPase family, and the ATPase activity of DnaC is required for its helicase loading function at the origin of replication (32,33).…”

Section: Introductionmentioning

confidence: 99%

DciA Helicase Operators Exhibit Diversity across Bacterial Phyla

et al. 2022

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“…In E. coli and B. subtilis, the loading of the replicative helicase is performed with the help of a helicase loader, termed DnaC in E. coli and DnaI in B. subtilis (4, [24][25][26][27]. dnaC and dnaI were acquired by E. coli and B. subtilis, respectively, 4 via domestication of related but distinct phage ATPase-containing genes (28)(29)(30)(31). DnaC and DnaI are both in the ATPases Associated with diverse cellular Activities (AAA+) ATPase family, and the ATPase activity of DnaC is required for its helicase loading function at the origin of replication (32,33).…”

Section: Introductionmentioning

confidence: 99%

DciA helicase operators exhibit diversity across bacterial phyla

Blaine¹,

Burke

Ravi

et al. 2022

Preprint

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A fundamental requirement for life is replication of an organism's DNA. Studies in Escherichia coli and Bacillus subtilis have set the paradigm for how DNA replication occurs in bacteria. During replication initiation in E. coli and B. subtilis, the replicative helicase is loaded onto the DNA at the origin of replication by an ATPase helicase loader. However, most bacteria do not encode homologs to the helicase loaders in E. coli and B. subtilis, raising the question of how helicase activity is facilitated in other bacteria during DNA replication initiation. Recent work has identified the DciA protein as a predicted helicase operator that may perform a function analogous to the helicase loaders in E. coli and B. subtilis. DciA proteins are defined by the presence of a DUF721 domain and are conserved in most bacteria. However, we find that the sequence conservation between DciA proteins across different phyla is very low. Therefore, to comprehensively define the DciA protein family, we took a computational evolutionary approach. These analyses identified diversity in sequence features and domain architectures amongst DciA homologs that were associated with specific phylogenetic lineages. The diversity of DciA proteins elucidated here represents the evolution of helicase operation in bacterial DNA replication, highlights the need for phyla-specific analyses of this fundamental biological process, and is an important example of how research in bacterial DNA replication is necessary in organisms beyond E. coli and B. subtilis.

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Convergent evolution in two bacterial replicative helicase loaders

Cited by 8 publications

References 117 publications

The LH-DH module of the bacterial replicative helicases is the common binding site for DciA and other helicase loaders

The LH-DH module of the bacterial replicative helicases is the common binding site for DciA and other helicase loaders

DciA Helicase Operators Exhibit Diversity across Bacterial Phyla

DciA helicase operators exhibit diversity across bacterial phyla

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