Structure and activity of a bacterial defense‐associated 3′‐5′ exonuclease

Liang, Qishan; Richey, Sara T.; Ur, Sarah N.; Ye, Qiaozhen; Lau, Rebecca; Corbett, K.D.

doi:10.1002/pro.4374

Cited by 3 publications

(3 citation statements)

References 33 publications

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“…Further suggesting roles in sensing and responding to damage, the cluster represented by blue dots in Fig. 3 includes a protein (21) with remarkable structural homology to the 3’−5’ DNA exonuclease Cap18 from Escherichia coli (PDB match 7t2s , RMSD = 0.96) 15 . This is part of the bacterial immune cyclic oligonucleotide-based anti-phage signaling (CBASS) system, yet no other part of the system has been identified in Borgs and Methanoperedens .…”

Section: Resultsmentioning

confidence: 99%

Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

Schoelmerich,

Ly,

West-Roberts

et al. 2024

Nat Commun

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Borgs are huge extrachromosomal elements (ECE) of anaerobic methane-consuming “Candidatus Methanoperedens” archaea. Here, we used nanopore sequencing to validate published complete genomes curated from short reads and to reconstruct new genomes. 13 complete and four near-complete linear genomes share 40 genes that define a largely syntenous genome backbone. We use these conserved genes to identify new Borgs from peatland soil and to delineate Borg phylogeny, revealing two major clades. Remarkably, Borg genes encoding nanowire-like electron-transferring cytochromes and cell surface proteins are more highly expressed than those of host Methanoperedens, indicating that Borgs augment the Methanoperedens activity in situ. We reconstructed the first complete 4.00 Mbp genome for a Methanoperedens that is inferred to be a Borg host and predicted its methylation motifs, which differ from pervasive TC and CC methylation motifs of the Borgs. Thus, methylation may enable Methanoperedens to distinguish their genomes from those of Borgs. Very high Borg to Methanoperedens ratios and structural predictions suggest that Borgs may be capable of encapsulation. The findings clearly define Borgs as a distinct class of ECE with shared genomic signatures, establish their diversification from a common ancestor with genetic inheritance, and raise the possibility of periodic existence outside of host cells.

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Section: Resultsmentioning

confidence: 99%

Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

Schoelmerich,

Ly,

West-Roberts

et al. 2024

Nat Commun

View full text Add to dashboard Cite

show abstract

“…Further suggesting roles in sensing and responding to damage, the cluster represented in blue in Extended Data Figure 3 includes a protein (21) with remarkable structural homology to the 3'-5' DNA exonuclease Cap18 from Escherichia coli (PDB match 7t2s, RMSD = 0.96) 14 . This is part of the bacterial immune cyclic oligonucleotide-based anti-phage signaling (CBASS) system, yet no other part of the system has been identified in Borgs and Methanoperedens.…”

Section: Core Borg Proteins For Replication Nucleotide Processing Cel...mentioning

confidence: 99%

Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

Schoelmerich

Ly²,

West-Roberts

et al. 2023

Preprint

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Borgs are huge extrachromosomal elements (ECE) of anaerobic methane-consuming “CandidatusMethanoperedens” archaea. Here, we used nanopore sequencing to validate published complete genomes curated from short reads and to reconstruct new genomes. 13 complete and four near-complete linear genomes share 40 genes that define a largely syntenous genome backbone. We use these conserved genes to identify new Borgs from peatland soil and to delineate Borg phylogeny, revealing two major clades. Remarkably, Borg genes encoding OmcZ nanowire-like electron-exporting cytochromes and cell surface proteins are more highly expressed than those of hostMethanoperedens, indicating that Borgs augment theMethanoperedensactivityin situ. We reconstructed the first complete 4.00 Mbp genome for aMethanoperedensthat is inferred to be a Borg host and predicted its methylation motifs, which differ from pervasive TC and CC methylation motifs of the Borgs. Thus, methylation may enableMethanoperedensto distinguish their genomes from those of Borgs. Very high Borg toMethanoperedensratios and structural predictions suggest that Borgs may be capable of encapsulation. The findings clearly define Borgs as a distinct class of ECE with shared genomic signatures, establish their diversification from a common ancestor with genetic inheritance, and raise the possibility of periodic existence outside of host cells.

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“…In contrast to the endonucleases mentioned above, Cap18 has a 3'-5' exonuclease primitive activity for degrading ssDNA or ssRNA, not requiring cyclic oligonucleotide binding. Coexisting with transcription factors such as CapW or CapH+CapP and Cap4 genes in CBASS operons, this Cap18 homodimer may regulate CBASS activation by eliminating ssDNA or ssRNA related to CBASS transcription factors (15). The bacterial CRISPR system also harbors a series of nuclease effector complexes for DNA or RNA damage.…”

Section: Dna Degradationmentioning

confidence: 99%

The arms race between bacteria CBASS and bacteriophages

Wang

Zhang

2023

Front. Immunol.

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The Bacterial Cyclic oligonucleotide-Based Anti-phage Signaling System (CBASS) is an innate immune system that induces cell suicide to defend against phage infections. This system relies on cGAS/DncV-like nucleotidyltransferases (CD-NTase) to synthesize cyclic oligonucleotides (cOs) and CD-NTase-associated proteins (Caps) to execute cell death through DNA cleavage, membrane damage, and NAD depletion, thereby inhibiting phage replication. Ancillary proteins expressed in CBASS, in combination with CD-NTase, ensure the normal synthesis of cOs and prepare CD-NTase for full activation by binding to phage genomes, proteins, or other unknown products. To counteract cell death induced by CBASS, phage genes encode immune evasion proteins that curb Cap recognition of cOs, allowing for phage replication, assembly, and propagation in bacterial cells. This review provides a comprehensive understanding of CBASS immunity, comparing it with different bacterial immune systems and highlighting the interplay between CBASS and phage. Additionally, it explores similar immune escape methods based on shared proteins and action mechanisms between prokaryotic and eukaryotic viruses.

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Structure and activity of a bacterial defense‐associated 3′‐5′ exonuclease

Cited by 3 publications

References 33 publications

Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

The arms race between bacteria CBASS and bacteriophages

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