DNA Replication Control Is Linked to Genomic Positioning of Control Regions in Escherichia coli
Chromosome replication in Escherichia coli is in part controlled by three non-coding genomic sequences, DARS1, DARS2, and datA that modulate the activity of the initiator protein DnaA. The relative distance from oriC to the non-coding regions are conserved among E. coli species, despite large variat...
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description | Chromosome replication in Escherichia coli is in part controlled by three non-coding genomic sequences, DARS1, DARS2, and datA that modulate the activity of the initiator protein DnaA. The relative distance from oriC to the non-coding regions are conserved among E. coli species, despite large variations in genome size. Here we use a combination of i) site directed translocation of each region to new positions on the bacterial chromosome and ii) random transposon mediated translocation followed by culture evolution, to show genetic evidence for the importance of position. Here we provide evidence that the genomic locations of these regulatory sequences are important for cell cycle control and bacterial fitness. In addition, our work shows that the functionally redundant DARS1 and DARS2 regions play different roles in replication control. DARS1 is mainly involved in maintaining the origin concentration, whether DARS2 is also involved in maintaining single cell synchrony. |
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The relative distance from oriC to the non-coding regions are conserved among E. coli species, despite large variations in genome size. Here we use a combination of i) site directed translocation of each region to new positions on the bacterial chromosome and ii) random transposon mediated translocation followed by culture evolution, to show genetic evidence for the importance of position. Here we provide evidence that the genomic locations of these regulatory sequences are important for cell cycle control and bacterial fitness. In addition, our work shows that the functionally redundant DARS1 and DARS2 regions play different roles in replication control. DARS1 is mainly involved in maintaining the origin concentration, whether DARS2 is also involved in maintaining single cell synchrony.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006286</identifier><identifier>PMID: 27589233</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biology ; Biology and Life Sciences ; Cell cycle ; Chromosomes ; Chromosomes, Bacterial - genetics ; Cloning ; Colleges & universities ; Deoxyribonucleic acid ; Directed Molecular Evolution ; DNA ; DNA replication ; DNA Replication - genetics ; DNA Transposable Elements - genetics ; DNA-Binding Proteins - genetics ; E coli ; Escherichia coli ; Escherichia coli - genetics ; Escherichia coli Proteins - genetics ; Funding ; Gene expression ; Genetic aspects ; Genetic Fitness ; Genome, Bacterial - genetics ; Genomes ; Genomics ; Observations ; Proteins ; Regulatory Sequences, Nucleic Acid - genetics ; Replication Origin - genetics ; Research and Analysis Methods ; Stress response</subject><ispartof>PLoS genetics, 2016-09, Vol.12 (9), p.e1006286-e1006286</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 12(9): e1006286. doi:10.1371/journal.pgen.1006286</rights><rights>2016 Frimodt-Møller et al 2016 Frimodt-Møller et al</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . 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DARS1 is mainly involved in maintaining the origin concentration, whether DARS2 is also involved in maintaining single cell synchrony.</description><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cell cycle</subject><subject>Chromosomes</subject><subject>Chromosomes, Bacterial - genetics</subject><subject>Cloning</subject><subject>Colleges & universities</subject><subject>Deoxyribonucleic acid</subject><subject>Directed Molecular Evolution</subject><subject>DNA</subject><subject>DNA replication</subject><subject>DNA Replication - genetics</subject><subject>DNA Transposable Elements - genetics</subject><subject>DNA-Binding Proteins - genetics</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Funding</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Genetic Fitness</subject><subject>Genome, Bacterial - genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Observations</subject><subject>Proteins</subject><subject>Regulatory Sequences, Nucleic Acid - genetics</subject><subject>Replication Origin - genetics</subject><subject>Research and Analysis Methods</subject><subject>Stress response</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk1tv0zAUxyMEYmPwDRBEQkLw0OJr7LxMqsoYlaoNlcur5TonqYcblzhB8O1xaFY1aA9DfrB1_Dv_c7FPkjzHaIqpwO9ufNfU2k13FdRTjFBGZPYgOcWc04lgiD08Op8kT0K4QYhymYvHyQkR8UAoPU3U-6tZuoKds0a31tfp3Ndt4126COnS1t-hSFufXkLtt9akn3ywPWXrKvXlgV1BFY0htXV6EcwGGms2VqfGO_s0eVRqF-DZsJ8lXz9cfJl_nCyvLxfz2XJiJOHtRAqdZQCYZJyBRswwI3lOUQ4ECo4KCnKdG15yaQyJLCoRQ9qURBidacD0LHm51905H9TQm6CwJDljNMtRJBZ7ovD6Ru0au9XNb-W1VX8NvqmUblprHCgZ43IpJAAULGNrzcqiMFgyU0KuuY5a50O0br2FwkDsg3Yj0fFNbTeq8j8VRxgRJqPAm0Gg8T86CK3a2mDAOV2D7_q8qaCI5oTcA8WCZ4iJvsRX_6B3N2KgKh1rtXXpY4qmF1UzJrKcZ0T0Yad3UHEVEH-Cr6G00T5yeDtyiEwLv9pKdyGoxefVf7BX92evv43Z10fsBrRrN8G7rv-zYQyyPWgaH0ID5eHtMFL9eN12TvXjpYbxim4vjt_94HQ7T_QPQf4eVg</recordid><startdate>20160902</startdate><enddate>20160902</enddate><creator>Frimodt-Møller, Jakob</creator><creator>Charbon, Godefroid</creator><creator>Krogfelt, Karen A</creator><creator>Løbner-Olesen, Anders</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>7QL</scope><scope>C1K</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160902</creationdate><title>DNA Replication Control Is Linked to Genomic Positioning of Control Regions in Escherichia coli</title><author>Frimodt-Møller, Jakob ; Charbon, Godefroid ; Krogfelt, Karen A ; Løbner-Olesen, Anders</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c825t-87a66ee12654ea04c4c859309e2ed50d3e8b9c5f58cc27a60f040acf27ca6ae13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Cell cycle</topic><topic>Chromosomes</topic><topic>Chromosomes, Bacterial - genetics</topic><topic>Cloning</topic><topic>Colleges & universities</topic><topic>Deoxyribonucleic acid</topic><topic>Directed Molecular Evolution</topic><topic>DNA</topic><topic>DNA replication</topic><topic>DNA Replication - genetics</topic><topic>DNA Transposable Elements - genetics</topic><topic>DNA-Binding Proteins - genetics</topic><topic>E coli</topic><topic>Escherichia coli</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Funding</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Genetic Fitness</topic><topic>Genome, Bacterial - genetics</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Observations</topic><topic>Proteins</topic><topic>Regulatory Sequences, Nucleic Acid - genetics</topic><topic>Replication Origin - genetics</topic><topic>Research and Analysis Methods</topic><topic>Stress response</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Frimodt-Møller, Jakob</creatorcontrib><creatorcontrib>Charbon, Godefroid</creatorcontrib><creatorcontrib>Krogfelt, Karen A</creatorcontrib><creatorcontrib>Løbner-Olesen, Anders</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Opposing Viewpoints In Context</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environmental Sciences and Pollution Management</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Frimodt-Møller, Jakob</au><au>Charbon, Godefroid</au><au>Krogfelt, Karen A</au><au>Løbner-Olesen, Anders</au><au>Viollier, Patrick H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>DNA Replication Control Is Linked to Genomic Positioning of Control Regions in Escherichia coli</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2016-09-02</date><risdate>2016</risdate><volume>12</volume><issue>9</issue><spage>e1006286</spage><epage>e1006286</epage><pages>e1006286-e1006286</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Chromosome replication in Escherichia coli is in part controlled by three non-coding genomic sequences, DARS1, DARS2, and datA that modulate the activity of the initiator protein DnaA. The relative distance from oriC to the non-coding regions are conserved among E. coli species, despite large variations in genome size. Here we use a combination of i) site directed translocation of each region to new positions on the bacterial chromosome and ii) random transposon mediated translocation followed by culture evolution, to show genetic evidence for the importance of position. Here we provide evidence that the genomic locations of these regulatory sequences are important for cell cycle control and bacterial fitness. In addition, our work shows that the functionally redundant DARS1 and DARS2 regions play different roles in replication control. DARS1 is mainly involved in maintaining the origin concentration, whether DARS2 is also involved in maintaining single cell synchrony.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27589233</pmid><doi>10.1371/journal.pgen.1006286</doi><oa>free_for_read</oa></addata></record> |
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subjects | Biology Biology and Life Sciences Cell cycle Chromosomes Chromosomes, Bacterial - genetics Cloning Colleges & universities Deoxyribonucleic acid Directed Molecular Evolution DNA DNA replication DNA Replication - genetics DNA Transposable Elements - genetics DNA-Binding Proteins - genetics E coli Escherichia coli Escherichia coli - genetics Escherichia coli Proteins - genetics Funding Gene expression Genetic aspects Genetic Fitness Genome, Bacterial - genetics Genomes Genomics Observations Proteins Regulatory Sequences, Nucleic Acid - genetics Replication Origin - genetics Research and Analysis Methods Stress response |
title | DNA Replication Control Is Linked to Genomic Positioning of Control Regions in Escherichia coli |
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