A geometrical model for DNA organization in bacteria
Recent experimental studies have revealed that bacteria, such as C. crescentus, show a remarkable spatial ordering of their chromosome. A strong linear correlation has been found between the position of genes on the chromosomal map and their spatial position in the cellular volume. We show that this...
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| description | Recent experimental studies have revealed that bacteria, such as C. crescentus, show a remarkable spatial ordering of their chromosome. A strong linear correlation has been found between the position of genes on the chromosomal map and their spatial position in the cellular volume. We show that this correlation can be explained by a purely geometrical model. Namely, self-avoidance of DNA, specific positioning of one or few DNA loci (such as origin or terminus) together with the action of DNA compaction proteins (that organize the chromosome into topological domains) are sufficient to get a linear arrangement of the chromosome along the cell axis. We develop a Monte-Carlo method that allows us to test our model numerically and to analyze the dependence of the spatial ordering on various physiologically relevant parameters. We show that the proposed geometrical ordering mechanism is robust and universal (i.e. does not depend on specific bacterial details). The geometrical mechanism should work in all bacteria that have compacted chromosomes with spatially fixed regions. We use our model to make specific and experimentally testable predictions about the spatial arrangement of the chromosome in mutants of C. crescentus and the growth-stage dependent ordering in E. coli. |
| doi_str_mv | 10.1371/journal.pone.0013806 |
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A strong linear correlation has been found between the position of genes on the chromosomal map and their spatial position in the cellular volume. We show that this correlation can be explained by a purely geometrical model. Namely, self-avoidance of DNA, specific positioning of one or few DNA loci (such as origin or terminus) together with the action of DNA compaction proteins (that organize the chromosome into topological domains) are sufficient to get a linear arrangement of the chromosome along the cell axis. We develop a Monte-Carlo method that allows us to test our model numerically and to analyze the dependence of the spatial ordering on various physiologically relevant parameters. We show that the proposed geometrical ordering mechanism is robust and universal (i.e. does not depend on specific bacterial details). The geometrical mechanism should work in all bacteria that have compacted chromosomes with spatially fixed regions. We use our model to make specific and experimentally testable predictions about the spatial arrangement of the chromosome in mutants of C. crescentus and the growth-stage dependent ordering in E. coli.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0013806</identifier><identifier>PMID: 21085464</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Algorithms ; Analysis ; Architects ; Bacteria ; Bacterial genetics ; Biophysics ; Caulobacter crescentus - genetics ; Cell Biology ; Chromosome Mapping ; Chromosomes ; Chromosomes, Bacterial - genetics ; Compaction ; Computational Biology ; Computer simulation ; Correlation ; Deoxyribonucleic acid ; DNA ; DNA Replication ; DNA, Bacterial - chemistry ; DNA, Bacterial - genetics ; DNA, Circular - chemistry ; DNA, Circular - genetics ; E coli ; Escherichia coli ; Escherichia coli - genetics ; Genomes ; Models, Molecular ; Monte Carlo Method ; Monte Carlo methods ; Monte Carlo simulation ; Mutants ; Nucleic Acid Conformation ; Physics ; Polymers ; Proteins ; Robustness (mathematics) ; Viscoelasticity</subject><ispartof>PloS one, 2010-11, Vol.5 (11), p.e13806-e13806</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Buenemann, Lenz. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Buenemann, Lenz. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c723t-39d26d54474c687b7d0013df270c9226956ee67b020b3df37e3a8e40229572a33</citedby><cites>FETCH-LOGICAL-c723t-39d26d54474c687b7d0013df270c9226956ee67b020b3df37e3a8e40229572a33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2972204/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2972204/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21085464$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Driks, Adam</contributor><creatorcontrib>Buenemann, Mathias</creatorcontrib><creatorcontrib>Lenz, Peter</creatorcontrib><title>A geometrical model for DNA organization in bacteria</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Recent experimental studies have revealed that bacteria, such as C. crescentus, show a remarkable spatial ordering of their chromosome. A strong linear correlation has been found between the position of genes on the chromosomal map and their spatial position in the cellular volume. We show that this correlation can be explained by a purely geometrical model. Namely, self-avoidance of DNA, specific positioning of one or few DNA loci (such as origin or terminus) together with the action of DNA compaction proteins (that organize the chromosome into topological domains) are sufficient to get a linear arrangement of the chromosome along the cell axis. We develop a Monte-Carlo method that allows us to test our model numerically and to analyze the dependence of the spatial ordering on various physiologically relevant parameters. We show that the proposed geometrical ordering mechanism is robust and universal (i.e. does not depend on specific bacterial details). The geometrical mechanism should work in all bacteria that have compacted chromosomes with spatially fixed regions. 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genetics</subject><subject>Genomes</subject><subject>Models, Molecular</subject><subject>Monte Carlo Method</subject><subject>Monte Carlo methods</subject><subject>Monte Carlo simulation</subject><subject>Mutants</subject><subject>Nucleic Acid Conformation</subject><subject>Physics</subject><subject>Polymers</subject><subject>Proteins</subject><subject>Robustness (mathematics)</subject><subject>Viscoelasticity</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</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>eNqNk22L1DAQx4so3nn6DUQLguKLXdMkTdI3wnI-LRwe-PQ2pMl0N0va7CWtqJ_e1O0dWzlQ8iJh8pt_ZiYzWfa4QMuC8OLVzg-hU2659x0sESqIQOxOdlpUBC8YRuTu0fkkexDjDqGSCMbuZye4QKKkjJ5mdJVvwLfQB6uVy1tvwOWND_mbj6vch43q7C_VW9_ltstrpXsIVj3M7jXKRXg07WfZ13dvv5x_WFxcvl-fry4WmmPSL0hlMDMlpZxqJnjNzRimaTBHusKYVSUDYLxGGNXJTDgQJYAijKuSY0XIWfb0oLt3Psop4SiLdE94xShNxPpAGK92ch9sq8JP6ZWVfwwpAalCb7UDWRUUCwMcoNZUIZPKVSpdaGOYKpniSev19NpQt2A0dH1QbiY6v-nsVm78d4krjjEag3kxCQR_NUDsZWujBudUB36IUjBa0UqQ6t8kEpSViIlEPvuLvL0ME7VRKVPbNT4FqEdNuaKcCCK4KBK1vIVKy0BrdWqjxib7zOHlzCExPfzoN2qIUa4_f_p_9vLbnH1-xG5BuX4bvRvGPotzkB5AHXyMAZqb3yiQHKfguhpynAI5TUFye3L8kzdO121PfgPzzP7S</recordid><startdate>20101103</startdate><enddate>20101103</enddate><creator>Buenemann, Mathias</creator><creator>Lenz, Peter</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>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20101103</creationdate><title>A geometrical model for DNA organization in bacteria</title><author>Buenemann, Mathias ; Lenz, Peter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c723t-39d26d54474c687b7d0013df270c9226956ee67b020b3df37e3a8e40229572a33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Algorithms</topic><topic>Analysis</topic><topic>Architects</topic><topic>Bacteria</topic><topic>Bacterial genetics</topic><topic>Biophysics</topic><topic>Caulobacter crescentus - 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A strong linear correlation has been found between the position of genes on the chromosomal map and their spatial position in the cellular volume. We show that this correlation can be explained by a purely geometrical model. Namely, self-avoidance of DNA, specific positioning of one or few DNA loci (such as origin or terminus) together with the action of DNA compaction proteins (that organize the chromosome into topological domains) are sufficient to get a linear arrangement of the chromosome along the cell axis. We develop a Monte-Carlo method that allows us to test our model numerically and to analyze the dependence of the spatial ordering on various physiologically relevant parameters. We show that the proposed geometrical ordering mechanism is robust and universal (i.e. does not depend on specific bacterial details). The geometrical mechanism should work in all bacteria that have compacted chromosomes with spatially fixed regions. 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| subjects | Algorithms Analysis Architects Bacteria Bacterial genetics Biophysics Caulobacter crescentus - genetics Cell Biology Chromosome Mapping Chromosomes Chromosomes, Bacterial - genetics Compaction Computational Biology Computer simulation Correlation Deoxyribonucleic acid DNA DNA Replication DNA, Bacterial - chemistry DNA, Bacterial - genetics DNA, Circular - chemistry DNA, Circular - genetics E coli Escherichia coli Escherichia coli - genetics Genomes Models, Molecular Monte Carlo Method Monte Carlo methods Monte Carlo simulation Mutants Nucleic Acid Conformation Physics Polymers Proteins Robustness (mathematics) Viscoelasticity |
| title | A geometrical model for DNA organization in bacteria |
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