The wobble nucleotide-excising anticodon nuclease RloC is governed by the zinc-hook and DNA-dependent ATPase of its Rad50-like region

Klaiman, Daniel; Steinfels-Kohn, Emmanuelle; Krutkina, Ekaterina; Davidov, Elena; Kaufmann, Gabriel

doi:10.1093/nar/gks593

Cited by 18 publications

(35 citation statements)

References 45 publications

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“…The cleavage of tRNA Lys inhibits the host translation and as a consequence the reproduction of the T4 phage. The RloC enzyme that is homologous to PrrC does not seem to be linked to R-M systems, has similar biochemical properties and is activated under genotoxic stress (52,53). Recent analysis has shown that the ACNase domain of both proteins belongs to the HEPN superfamily that is merging as a major group of ribonucleases that are involved in various forms of defense and stress response (54,55).…”

Section: Defense Mechanisms In Bacteria and Archaeamentioning

confidence: 99%

Comparative genomics of defense systems in archaea and bacteria

Makarova

Wolf

Koonin

2013

Nucleic Acids Research

387

402

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Our knowledge of prokaryotic defense systems has vastly expanded as the result of comparative genomic analysis, followed by experimental validation. This expansion is both quantitative, including the discovery of diverse new examples of known types of defense systems, such as restriction-modification or toxin-antitoxin systems, and qualitative, including the discovery of fundamentally new defense mechanisms, such as the CRISPR-Cas immunity system. Large-scale statistical analysis reveals that the distribution of different defense systems in bacterial and archaeal taxa is non-uniform, with four groups of organisms distinguishable with respect to the overall abundance and the balance between specific types of defense systems. The genes encoding defense system components in bacterial and archaea typically cluster in defense islands. In addition to genes encoding known defense systems, these islands contain numerous uncharacterized genes, which are candidates for new types of defense systems. The tight association of the genes encoding immunity systems and dormancy- or cell death-inducing defense systems in prokaryotic genomes suggests that these two major types of defense are functionally coupled, providing for effective protection at the population level.

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Section: Defense Mechanisms In Bacteria and Archaeamentioning

confidence: 99%

Comparative genomics of defense systems in archaea and bacteria

Makarova

Wolf

Koonin

2013

Nucleic Acids Research

387

402

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“…Structural studies on RAMPs have demonstrated that these independently acquired histidines and other polar residues might constitute distinct but catalytically equivalent active sites for this RNase superfamily [66,68]. Like the BECR RNases, the HEPN and RAMPs are also metal-independent endoRNases that generate products with cyclic 2’-3’ ends [64-66]. Metal-dependent active sites require a precise 3D configuration of metal-chelating residues coming from different parts of the fold probably making them harder to reconfigure.…”

Section: Reorganization Of Active Site Residues While Retaining Ancesmentioning

confidence: 99%

Resilience of biochemical activity in protein domains in the face of structural divergence

Zhang

Iyer

Burroughs

et al. 2014

Current Opinion in Structural Biology

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Recent studies point to the prevalence of the evolutionary phenomenon of drastic structural transformation of protein domains while continuing to preserve their basic biochemical function. These transformations span a wide spectrum, including simple domains incorporated into larger structural scaffolds, changes in the structural core, major active site shifts, topological rewiring and extensive structural transmogrifications. Proteins from biological conflict systems, such as toxinantitoxin, restriction-modification, CRISPR/Cas, polymorphic toxin and secondary metabolism systems commonly display such transformations. These include endoDNases, metal-independent RNases, deaminases, ADP ribosyltransferases, immunity proteins, kinases and E1-like enzymes. In eukaryotes such transformations are seen in domains involved in chromatin-related peptide recognition and protein/DNA-modification. Intense selective pressures from “arm-race”-like situations in conflict and macromolecular modification systems could favor drastic structural divergence while preserving function.

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“…The ACNase RloC that is homologous to PrrC, although usually not linked directly to RM systems, seems to function under the same logic, i.e. as an antiviral contingency that acts when DNA restriction is alleviated under genotoxic stress [32,33]. Although PrrC and RloC are not known to cause bacterial suicide or persistence, they clearly function on the exact same principle, namely inhibiting translation to prevent virus reproduction in situations when an innate anti-phage immunity mechanism fails.…”

Section: Introductionmentioning

confidence: 99%

Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes

et al. 2012

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BackgroundThe virus-host arms race is a major theater for evolutionary innovation. Archaea and bacteria have evolved diverse, elaborate antivirus defense systems that function on two general principles: i) immune systems that discriminate self DNA from nonself DNA and specifically destroy the foreign, in particular viral, genomes, whereas the host genome is protected, or ii) programmed cell suicide or dormancy induced by infection.Presentation of the hypothesisAlmost all genomic loci encoding immunity systems such as CRISPR-Cas, restriction-modification and DNA phosphorothioation also encompass suicide genes, in particular those encoding known and predicted toxin nucleases, which do not appear to be directly involved in immunity. In contrast, the immunity systems do not appear to encode antitoxins found in typical toxin-antitoxin systems. This raises the possibility that components of the immunity system themselves act as reversible inhibitors of the associated toxin proteins or domains as has been demonstrated for the Escherichia coli anticodon nuclease PrrC that interacts with the PrrI restriction-modification system. We hypothesize that coupling of diverse immunity and suicide/dormancy systems in prokaryotes evolved under selective pressure to provide robustness to the antivirus response. We further propose that the involvement of suicide/dormancy systems in the coupled antivirus response could take two distinct forms:1) induction of a dormancy-like state in the infected cell to ‘buy time’ for activation of adaptive immunity; 2) suicide or dormancy as the final recourse to prevent viral spread triggered by the failure of immunity.Testing the hypothesisThis hypothesis entails many experimentally testable predictions. Specifically, we predict that Cas2 protein present in all cas operons is a mRNA-cleaving nuclease (interferase) that might be activated at an early stage of virus infection to enable incorporation of virus-specific spacers into the CRISPR locus or to trigger cell suicide when the immune function of CRISPR-Cas systems fails. Similarly, toxin-like activity is predicted for components of numerous other defense loci.Implications of the hypothesisThe hypothesis implies that antivirus response in prokaryotes involves key decision-making steps at which the cell chooses the path to follow by sensing the course of virus infection.ReviewersThis article was reviewed by Arcady Mushegian, Etienne Joly and Nick Grishin. For complete reviews, go to the Reviewers’ reports section.

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The wobble nucleotide-excising anticodon nuclease RloC is governed by the zinc-hook and DNA-dependent ATPase of its Rad50-like region

Cited by 18 publications

References 45 publications

Comparative genomics of defense systems in archaea and bacteria

Comparative genomics of defense systems in archaea and bacteria

Resilience of biochemical activity in protein domains in the face of structural divergence

Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes

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