A soft Tus-Ter interaction is hiding a fail-safe lock in the replication fork trap of Dickeya paradisiaca

Toft, Casey J.; Sorenson, Alanna E.; Schaeffer, Patrick M.

doi:10.1016/j.micres.2022.127147

Cited by 2 publications

(10 citation statements)

References 52 publications

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“…This mechanism of ‘clicking into place’ essentially blocks any movement along the DNA by a ratchet-type mechanism, and also slows the dissociation of Tus ( Mulcair et al, 2006 ; Berghuis et al, 2015 ; Elshenawy et al, 2015 ; Pandey et al, 2015 ). This ‘locked’ Tus- ter complex can be generated by unwinding of the double-stranded DNA alone; DnaB helicase is not essential for its formation ( Bastia et al, 2008 ; Berghuis et al, 2015 ; Elshenawy et al, 2015 ; Toft et al, 2022 ). Some stabilization by specific protein–protein interaction between Tus and DnaB has been reported ( Mulugu et al, 2001 ), but to what extent they contribute towards the efficient arrest is not clear.…”

Section: Introductionmentioning

confidence: 99%

“…The presence of a ter site is only implicated and therefore marked with a question mark. (C) Type I fork trap system in Dickeya paradisiaca , as described in Toft et al (2022) . (D) Type II fork trap system in E. coli (Di) and the fork trap system in Bacillus subtilis (Dii) .…”

Section: Introductionmentioning

confidence: 99%

“…In organisms such as Edwardsiella tarda and Cedecea neteri the second replichore is also restricted by only a single ter site, whereas in organisms such as Dickeya paradisiaca two functional ter sites are used ( Toft et al, 2021 , 2022 ). The authors speculate that the type I system is the ancestral system, whereas the type II system is more divergent ( Toft et al, 2021 , 2022 ), which seems overall to fit well with the notion of a plasmid-derived system ( Figure 3 ; Galli et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

“…Taken together, the data suggest that we can simplify the fork trap system in E. coli and related bacteria by focusing on the innermost ter sites A–D as those being active in termination. The main difference between the type I and type II systems remains whether the border of the fork trap is defined by a single ter site associated with the tus gene (type I), or whether a cluster of ter sites is used, with tus associated with one of the secondary ter sites (type II) ( Toft et al, 2022 ). All of the other ter sites in E. coli are likely to be still present because of selection pressures unrelated to termination issues.…”

Section: Introductionmentioning

confidence: 99%

“…However, despite this variability, our sequence analysis did not reveal even a single example of a phylogenetic group where the replication fork trap appears to be non-functional ( Goodall et al, 2021 ). Thus, while a fork trap clearly is not essential, and a wide variety of bacterial species appear not to utilize a fork trap ( Galli et al, 2019 ), it appears that, once acquired, such a fork trap system is strictly maintained ( Neylon et al, 2005 ; Goodall et al, 2021 ; Toft et al, 2022 ). Together with the fork trap system in B. subtilis , which has a similar functionality but has likely arisen by convergent evolution ( Franks et al, 1995 ; Neylon et al, 2005 ), these findings suggest that a fork trap system is involved in mitigating a problem important enough to selectively maintain the fork trap system.…”

Section: Introductionmentioning

confidence: 99%

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Interplay between chromosomal architecture and termination of DNA replication in bacteria

Goodall,

Warecka,

Hawkins

et al. 2023

Front. Microbiol.

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Faithful transmission of the genome from one generation to the next is key to life in all cellular organisms. In the majority of bacteria, the genome is comprised of a single circular chromosome that is normally replicated from a single origin, though additional genetic information may be encoded within much smaller extrachromosomal elements called plasmids. By contrast, the genome of a eukaryote is distributed across multiple linear chromosomes, each of which is replicated from multiple origins. The genomes of archaeal species are circular, but are predominantly replicated from multiple origins. In all three cases, replication is bidirectional and terminates when converging replication fork complexes merge and ‘fuse’ as replication of the chromosomal DNA is completed. While the mechanics of replication initiation are quite well understood, exactly what happens during termination is far from clear, although studies in bacterial and eukaryotic models over recent years have started to provide some insight. Bacterial models with a circular chromosome and a single bidirectional origin offer the distinct advantage that there is normally just one fusion event between two replication fork complexes as synthesis terminates. Moreover, whereas termination of replication appears to happen in many bacteria wherever forks happen to meet, termination in some bacterial species, including the well-studied bacteria Escherichia coli and Bacillus subtilis, is more restrictive and confined to a ‘replication fork trap’ region, making termination even more tractable. This region is defined by multiple genomic terminator (ter) sites, which, if bound by specific terminator proteins, form unidirectional fork barriers. In this review we discuss a range of experimental results highlighting how the fork fusion process can trigger significant pathologies that interfere with the successful conclusion of DNA replication, how these pathologies might be resolved in bacteria without a fork trap system and how the acquisition of a fork trap might have provided an alternative and cleaner solution, thus explaining why in bacterial species that have acquired a fork trap system, this system is remarkably well maintained. Finally, we consider how eukaryotic cells can cope with a much-increased number of termination events.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Interplay between chromosomal architecture and termination of DNA replication in bacteria

Goodall,

Warecka,

Hawkins

et al. 2023

Front. Microbiol.

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Inhibition of Replication Fork Formation and Progression: Targeting the Replication Initiation and Primosomal Proteins

Radford,

Toft,

Sorenson

et al. 2023

IJMS

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Over 1.2 million deaths are attributed to multi-drug-resistant (MDR) bacteria each year. Persistence of MDR bacteria is primarily due to the molecular mechanisms that permit fast replication and rapid evolution. As many pathogens continue to build resistance genes, current antibiotic treatments are being rendered useless and the pool of reliable treatments for many MDR-associated diseases is thus shrinking at an alarming rate. In the development of novel antibiotics, DNA replication is still a largely underexplored target. This review summarises critical literature and synthesises our current understanding of DNA replication initiation in bacteria with a particular focus on the utility and applicability of essential initiation proteins as emerging drug targets. A critical evaluation of the specific methods available to examine and screen the most promising replication initiation proteins is provided.

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A soft Tus-Ter interaction is hiding a fail-safe lock in the replication fork trap of Dickeya paradisiaca

Cited by 2 publications

References 52 publications

Interplay between chromosomal architecture and termination of DNA replication in bacteria

Interplay between chromosomal architecture and termination of DNA replication in bacteria

Inhibition of Replication Fork Formation and Progression: Targeting the Replication Initiation and Primosomal Proteins

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