G-quadruplexes in bacteria: insights into the regulatory roles and interacting proteins of non-canonical nucleic acid structures

Cueny, Rachel R; McMillan, Sarah; Keck, James L.

doi:10.1080/10409238.2023.2181310

Cited by 8 publications

(4 citation statements)

References 165 publications

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“…The origin of these dual roles can be investigated by studying prokaryotic organisms. While the formation of G4s in bacteria has been documented, the study of their functions is still very limited compared to eukaryotes ( 75 ). Until now, there have been virtually no data on the detection and function of G4s in archaea.…”

Section: Discussionmentioning

confidence: 99%

G-quadruplexes inHaloferax volcanii

Aktary,

Cucchiarini,

Vesco

et al. 2024

Preprint

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The archaeal domain is a taxonomically rich component of microbial communities that inhabit a wide range of habitats on Earth, including the human body. Phylogenomic analyses have indicated that archaea represent the closest known relatives of eukaryotes, thus suggesting that eukaryotes may have evolved from an archaeal ancestor. G-quadruplex structures (G4), formed by guanine rich sequences, are among the most intensively studied local DNA/RNA structures and regulate key biological processes such as replication and gene expression. A bioinformatics analysis of the genome of the salt-loving archaea H. volcanii revealed a large number of potential G4 sequences (PQS). Biophysical analyses showed that a representative panel of these sequences form stable G4 structures under physiological conditions in vitro. In addition, immunofluorescence experiments using the G4-specific antibody, BG4, detected G4s in vivo at the single-cell level with super-resolution microscopy. Moreover, we directly visualized G4 in exponentially growing or stationary cells both at the DNA and RNA levels. G4s were also observed in the RNA and DNA of the hyperthermophile archaeon T. barophilus. Finally, we identified helicases potentially involved in G4 unfolding. Together, with H. volcanii as a new model, our work helps to fill the gap between bacteria and eukaryotic organisms for G4 studies and will aid in uncovering the evolutionary history of G4 structures in the tree of life.

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Section: Discussionmentioning

confidence: 99%

G-quadruplexes inHaloferax volcanii

Aktary,

Cucchiarini,

Vesco

et al. 2024

Preprint

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“…In principle, any DNA sequence that can fold up quickly -a G-quadruplex or any other stable tertiary structure -as duplex DNA is unwound during replication, could potentially block full replication of the lagging strand template and create a transient gap (Supplementary Figure S8). Sequences with the potential to form Gquadruplexes are common in eukaryotic genomes, with approximately 700,000 such sequences in the human genome (47)(48)(49)(50)(51)(52). Triggering transient gap formation, in the service of chromosome structural transitions or replication, could be a function of some or many of them, perhaps to facilitate chromosome folding or relieve topological stress.…”

Section: Discussionmentioning

confidence: 99%

Controlling Genome Topology with Sequences that Trigger Post-replication Gap Formation During Replisome Passage: TheE. coliRRS Elements

Pham,

Wood,

Dunbar

et al. 2023

Preprint

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We report that theEscherichia colichromosome includes novel GC-rich genomic structural elements that trigger formation of post-replication gaps upon replisome passage. The two nearly perfect 222 bp repeats, designated Replication Risk Sequences or RRS, are each 650 kbp from the terminus sequencedifand flank the Ter macrodomain. RRS sequence and positioning is highly conserved in enterobacteria. At least one RRS appears to be essential unless a 200 kbp region encompassing one of them is amplified. The RRS produce lagging strand ssDNA gaps, ≤2000 bp long, upon replisome passage, regardless of genome placement. Deletion of both RRS elements has substantial effects on global genome structure and topology. We hypothesize that RRS elements serve as topological relief valves during chromosome replication and segregation. There have been no screens for genomic sequences that trigger transient gap formation. Functional analogs of RRS could be widespread, possibly including some enigmatic G-quadruplexes.

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“…Thus, DNA helicases that unwind replication-blocking structures, including G-quadruplexes, and can influence genomic instability have been identified [ 24 ]. Additionally, proteins other than helicases (ATP independent) may also influence the genetic instability in bacteria [ 25 , 26 , 27 ]. Therefore, the enzymes involved in replication restart and recombination may be expected to influence the instability of G-quadruplex-forming repeats.…”

Section: Introductionmentioning

confidence: 99%

“…In Escherichia coli , several helicases and nucleic acid remodeling proteins could potentially affect G-quadruplexes [ 26 ]. Few bacterial G4 helicases have been identified, but the best characterized is bacterial RecQ.…”

Section: Introductionmentioning

confidence: 99%

Genomic Instability of G-Quadruplex Sequences in Escherichia coli: Roles of DinG, RecG, and RecQ Helicases

Parekh,

Węgrzyn,

Arluison

et al. 2023

Genes

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Guanine-rich DNA can fold into highly stable four-stranded DNA structures called G-quadruplexes (G4). Originally identified in sequences from telomeres and oncogene promoters, they can alter DNA metabolism. Indeed, G4-forming sequences represent obstacles for the DNA polymerase, with important consequences for cell life as they may lead to genomic instability. To understand their role in bacterial genomic instability, different G-quadruplex-forming repeats were cloned into an Escherichia coli genetic system that reports frameshifts and complete or partial deletions of the repeat when the G-tract comprises either the leading or lagging template strand during replication. These repeats formed stable G-quadruplexes in single-stranded DNA but not naturally supercoiled double-stranded DNA. Nevertheless, transcription promoted G-quadruplex formation in the resulting R-loop for (G3T)4 and (G3T)8 repeats. Depending on genetic background and sequence propensity for structure formation, mutation rates varied by five orders of magnitude. Furthermore, while in vitro approaches have shown that bacterial helicases can resolve G4, it is still unclear whether G4 unwinding is important in vivo. Here, we show that a mutation in recG decreased mutation rates, while deficiencies in the structure-specific helicases DinG and RecQ increased mutation rates. These results suggest that G-quadruplex formation promotes genetic instability in bacteria and that helicases play an important role in controlling this process in vivo.

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G-quadruplexes in bacteria: insights into the regulatory roles and interacting proteins of non-canonical nucleic acid structures

Cited by 8 publications

References 165 publications

G-quadruplexes inHaloferax volcanii

G-quadruplexes inHaloferax volcanii

Controlling Genome Topology with Sequences that Trigger Post-replication Gap Formation During Replisome Passage: TheE. coliRRS Elements

Genomic Instability of G-Quadruplex Sequences in Escherichia coli: Roles of DinG, RecG, and RecQ Helicases

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