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Interplay between chromosomal architecture and termination of DNA replication in bacteria

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 wi...

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Autores principales: Goodall, Daniel J., Warecka, Dominika, Hawkins, Michelle, Rudolph, Christian J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10331603/
https://www.ncbi.nlm.nih.gov/pubmed/37434703
http://dx.doi.org/10.3389/fmicb.2023.1180848
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author Goodall, Daniel J.
Warecka, Dominika
Hawkins, Michelle
Rudolph, Christian J.
author_facet Goodall, Daniel J.
Warecka, Dominika
Hawkins, Michelle
Rudolph, Christian J.
author_sort Goodall, Daniel J.
collection PubMed
description 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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spelling pubmed-103316032023-07-11 Interplay between chromosomal architecture and termination of DNA replication in bacteria Goodall, Daniel J. Warecka, Dominika Hawkins, Michelle Rudolph, Christian J. Front Microbiol Microbiology 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. Frontiers Media S.A. 2023-06-26 /pmc/articles/PMC10331603/ /pubmed/37434703 http://dx.doi.org/10.3389/fmicb.2023.1180848 Text en Copyright © 2023 Goodall, Warecka, Hawkins and Rudolph. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Goodall, Daniel J.
Warecka, Dominika
Hawkins, Michelle
Rudolph, Christian J.
Interplay between chromosomal architecture and termination of DNA replication in bacteria
title Interplay between chromosomal architecture and termination of DNA replication in bacteria
title_full Interplay between chromosomal architecture and termination of DNA replication in bacteria
title_fullStr Interplay between chromosomal architecture and termination of DNA replication in bacteria
title_full_unstemmed Interplay between chromosomal architecture and termination of DNA replication in bacteria
title_short Interplay between chromosomal architecture and termination of DNA replication in bacteria
title_sort interplay between chromosomal architecture and termination of dna replication in bacteria
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10331603/
https://www.ncbi.nlm.nih.gov/pubmed/37434703
http://dx.doi.org/10.3389/fmicb.2023.1180848
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