The Extended “Two-Barrel” Polymerases Superfamily: Structure, Function and Evolution

Sauguet, Ludovic

doi:10.1016/j.jmb.2019.05.017

Cited by 30 publications

(31 citation statements)

References 98 publications

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“…In contrast with cellular transcriptases and ribosomes, which evolved by accretion of complexity from a conserved catalytic core, it is striking that DNA replication was reinvented several times during evolution and that no replicative DNAP family is universally conserved. Bacteria, Archaea, and Eukarya have evolved three distinct protein folds to replicate their genomes as follows: (i) the Polβ-like fold-found in bacterial Pol-III, (ii) the Klenow-like fold-found both in archaeal/eukaryotic B-family DNAPs and in bacterial Pol-I, and (iii) the two-barrel fold-the third structural class of DNAPs that was recently unveiled with the structure of archaeal PolD 17,43 . Although structurally divergent, all replicative DNAPs share unifying features.…”

Section: Discussionmentioning

confidence: 99%

Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA

et al. 2020

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Replicative DNA polymerases (DNAPs) have evolved the ability to copy the genome with high processivity and fidelity. In Eukarya and Archaea, the processivity of replicative DNAPs is greatly enhanced by its binding to the proliferative cell nuclear antigen (PCNA) that encircles the DNA. We determined the cryo-EM structure of the DNA-bound PolD-PCNA complex from Pyrococcus abyssi at 3.77 Å. Using an integrative structural biology approachcombining cryo-EM, X-ray crystallography, protein-protein interaction measurements, and activity assayswe describe the molecular basis for the interaction and cooperativity between a replicative DNAP and PCNA. PolD recruits PCNA via a complex mechanism, which requires two different PIP-boxes. We infer that the second PIP-box, which is shared with the eukaryotic Polα replicative DNAP, plays a dual role in binding either PCNA or primase, and could be a master switch between an initiation and a processive phase during replication.

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Section: Discussionmentioning

confidence: 99%

Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA

et al. 2020

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“…In contrast with cellular transcriptases and ribosomes, which evolved by accretion of complexity from a conserved catalytic core, it is striking that DNA replication was reinvented several times during evolution and that no replicative DNA polymerase family is universally conserved. Bacteria, Archaea, and Eukarya have evolved three distinct protein folds to replicate their genomes: i) the Polb-like fold -found in bacterial Pol-III, ii) the Klenow-like fold -found both in archaeal/eukaryotic B-family DNAPs and in bacterial Pol-I, iii) the two-barrel fold -the third structural class of DNAPs that was recently unveiled with the structure of archaeal PolD (Sauguet, 2019;Sauguet et al, 2016). While structurally divergent, all replicative DNAPs share unifying features.…”

Section: Discussionmentioning

confidence: 99%

Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA

Madru

Raia

Hugonneau-Beaufet

et al. 2020

Preprint

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Replicative DNA polymerases (DNAPs) have evolved the ability to copy the genome with high processivity and fidelity. In Eukarya and Archaea, the processivity of replicative DNAPs is greatly enhanced by its binding to the proliferative cell nuclear antigen (PCNA) that encircles the DNA. We determined the cryo-EM structure of the DNA-bound PolD-PCNA complex from Pyrococcus abyssi at 3.77Å. Using an integrative structural biology approach -combining cryo-EM, X-ray crystallography and proteinprotein interaction measurements -we describe the molecular basis for the interaction and cooperativity between a replicative DNAP and PCNA with an unprecedented level of detail. PolD recruits PCNA via a complex mechanism, which requires two different PIPboxes. We infer that the second PIP-box, which is shared with the eukaryotic Pola replicative DNAP, plays a dual role in binding either PCNA or primase, and could be a master switch between an initiation phase and a processive phase during replication.

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“…These highly conserved regions were discerned based on both alignment conservation and quality (see “Methods”). Many of these regions corresponded to known conserved motifs in RNAP; within the β-subunit, these structures included the DNA-binding site, double-psi beta barrels, and the connector to the β′-subunit 23 . Within the β′-subunit, conserved regions included double-psi beta-barrel structures and the catalytic core 23 .…”

Section: Resultsmentioning

confidence: 99%

A distinct lineage of Caudovirales that encodes a deeply branching multi-subunit RNA polymerase

Weinheimer

Aylward²

2020

Nat Commun

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Bacteriophages play critical roles in the biosphere, but their vast genomic diversity has obscured their evolutionary origins, and phylogenetic analyses have traditionally been hindered by their lack of universal phylogenetic marker genes. In this study we mine metagenomic data and identify a clade of Caudovirales that encodes the β and β′ subunits of multi-subunit RNA polymerase (RNAP), a high-resolution phylogenetic marker which enables detailed evolutionary analyses. Our RNAP phylogeny revealed that the Caudovirales RNAP forms a clade distinct from cellular homologs, suggesting an ancient acquisition of this enzyme. Within these multimeric RNAP-encoding Caudovirales (mReC), we find that the similarity of major capsid proteins and terminase large subunits further suggests they form a distinct clade with common evolutionary origin. Our study characterizes a clade of RNAP-encoding Caudovirales and suggests the ancient origin of this enzyme in this group, underscoring the important role of viruses in the early evolution of life on Earth.

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The Extended “Two-Barrel” Polymerases Superfamily: Structure, Function and Evolution

Cited by 30 publications

References 98 publications

Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA

Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA

Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA

A distinct lineage of Caudovirales that encodes a deeply branching multi-subunit RNA polymerase

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