Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics

Each cell division requires the complete and accurate duplication of the entire genome. In bacteria, the duplication process of the often-circular chromosomes is initiated at a single origin per chromosome, resulting in two replication forks that traverse the chromosome in opposite directions. DNA s...

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Main Authors: Aisha H. Syeda, Juachi U. Dimude, Ole Skovgaard, Christian J. Rudolph
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00534/full
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author Aisha H. Syeda
Juachi U. Dimude
Ole Skovgaard
Christian J. Rudolph
author_facet Aisha H. Syeda
Juachi U. Dimude
Ole Skovgaard
Christian J. Rudolph
author_sort Aisha H. Syeda
collection DOAJ
description Each cell division requires the complete and accurate duplication of the entire genome. In bacteria, the duplication process of the often-circular chromosomes is initiated at a single origin per chromosome, resulting in two replication forks that traverse the chromosome in opposite directions. DNA synthesis is completed once the two forks fuse in a region diametrically opposite the origin. In some bacteria, such as Escherichia coli, the region where forks fuse forms a specialized termination area. Polar replication fork pause sites flanking this area can pause the progression of replication forks, thereby allowing forks to enter but not to leave. Transcription of all required genes has to take place simultaneously with genome duplication. As both of these genome trafficking processes share the same template, conflicts are unavoidable. In this review, we focus on recent attempts to add additional origins into various ectopic chromosomal locations of the E. coli chromosome. As ectopic origins disturb the native replichore arrangements, the problems resulting from such perturbations can give important insights into how genome trafficking processes are coordinated and the problems that arise if this coordination is disturbed. The data from these studies highlight that head-on replication–transcription conflicts are indeed highly problematic and multiple repair pathways are required to restart replication forks arrested at obstacles. In addition, the existing data also demonstrate that the replication fork trap in E. coli imposes significant constraints to genome duplication if ectopic origins are active. We describe the current models of how replication fork fusion events can cause serious problems for genome duplication, as well as models of how such problems might be alleviated both by a number of repair pathways as well as the replication fork trap system. Considering the problems associated both with head-on replication-transcription conflicts as well as head-on replication fork fusion events might provide clues of how these genome trafficking issues have contributed to shape the distinct architecture of bacterial chromosomes.
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spelling doaj.art-cba11620ddb2471bbc1659ce5b28787b2022-12-22T02:34:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-04-011110.3389/fmicb.2020.00534528236Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication DynamicsAisha H. Syeda0Juachi U. Dimude1Ole Skovgaard2Christian J. Rudolph3Department of Biology, University of York, York, United KingdomDivision of Biosciences, College of Health and Life Sciences, Brunel University London, Uxbridge, United KingdomDepartment of Science and Environment, Roskilde University, Roskilde, DenmarkDivision of Biosciences, College of Health and Life Sciences, Brunel University London, Uxbridge, United KingdomEach cell division requires the complete and accurate duplication of the entire genome. In bacteria, the duplication process of the often-circular chromosomes is initiated at a single origin per chromosome, resulting in two replication forks that traverse the chromosome in opposite directions. DNA synthesis is completed once the two forks fuse in a region diametrically opposite the origin. In some bacteria, such as Escherichia coli, the region where forks fuse forms a specialized termination area. Polar replication fork pause sites flanking this area can pause the progression of replication forks, thereby allowing forks to enter but not to leave. Transcription of all required genes has to take place simultaneously with genome duplication. As both of these genome trafficking processes share the same template, conflicts are unavoidable. In this review, we focus on recent attempts to add additional origins into various ectopic chromosomal locations of the E. coli chromosome. As ectopic origins disturb the native replichore arrangements, the problems resulting from such perturbations can give important insights into how genome trafficking processes are coordinated and the problems that arise if this coordination is disturbed. The data from these studies highlight that head-on replication–transcription conflicts are indeed highly problematic and multiple repair pathways are required to restart replication forks arrested at obstacles. In addition, the existing data also demonstrate that the replication fork trap in E. coli imposes significant constraints to genome duplication if ectopic origins are active. We describe the current models of how replication fork fusion events can cause serious problems for genome duplication, as well as models of how such problems might be alleviated both by a number of repair pathways as well as the replication fork trap system. Considering the problems associated both with head-on replication-transcription conflicts as well as head-on replication fork fusion events might provide clues of how these genome trafficking issues have contributed to shape the distinct architecture of bacterial chromosomes.https://www.frontiersin.org/article/10.3389/fmicb.2020.00534/fullreplicationtranscriptionrecG genetermination of DNA replicationectopic replication originsbacterial replication dynamics
spellingShingle Aisha H. Syeda
Juachi U. Dimude
Ole Skovgaard
Christian J. Rudolph
Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics
Frontiers in Microbiology
replication
transcription
recG gene
termination of DNA replication
ectopic replication origins
bacterial replication dynamics
title Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics
title_full Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics
title_fullStr Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics
title_full_unstemmed Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics
title_short Too Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics
title_sort too much of a good thing how ectopic dna replication affects bacterial replication dynamics
topic replication
transcription
recG gene
termination of DNA replication
ectopic replication origins
bacterial replication dynamics
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00534/full
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