Quantitative mapping of DNA phosphorothioatome reveals phosphorothioate heterogeneity of low modification frequency
Phosphorothioate (PT) modifications of the DNA backbone, widespread in prokaryotes, are first identified in bacterial enteropathogens Escherichia coli B7A more than a decade ago. However, methods for high resolution mapping of PT modification level are still lacking. Here, we developed the PT-IC-seq...
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description | Phosphorothioate (PT) modifications of the DNA backbone, widespread in prokaryotes, are first identified in bacterial enteropathogens Escherichia coli B7A more than a decade ago. However, methods for high resolution mapping of PT modification level are still lacking. Here, we developed the PT-IC-seq technique, based on iodine-induced selective cleavage at PT sites and high-throughput next generation sequencing, as a mean to quantitatively characterizing the genomic landscape of PT modifications. Using PT-IC-seq we foud that most PT sites are partially modified at a lower PT frequency (< 5%) in E. coli B7A and Salmonella enterica serovar Cerro 87, and both show a heterogeneity pattern of PT modification similar to those of the typical methylation modification. Combining the iodine-induced cleavage and absolute quantification by droplet digital PCR, we developed the PT-IC-ddPCR technique to further measure the PT modification level. Consistent with the PT-IC-seq measurements, PT-IC-ddPCR analysis confirmed the lower PT frequency in E. coli B7A. Our study has demonstrated the heterogeneity of PT modification in the bacterial population and we also established general tools for rigorous mapping and characterization of PT modification events at whole genome level. We describe to our knowledge the first genome-wide quantitative characterization of PT landscape and provides appropriate strategies for further functional studies of PT modification. |
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However, methods for high resolution mapping of PT modification level are still lacking. Here, we developed the PT-IC-seq technique, based on iodine-induced selective cleavage at PT sites and high-throughput next generation sequencing, as a mean to quantitatively characterizing the genomic landscape of PT modifications. Using PT-IC-seq we foud that most PT sites are partially modified at a lower PT frequency (< 5%) in E. coli B7A and Salmonella enterica serovar Cerro 87, and both show a heterogeneity pattern of PT modification similar to those of the typical methylation modification. Combining the iodine-induced cleavage and absolute quantification by droplet digital PCR, we developed the PT-IC-ddPCR technique to further measure the PT modification level. Consistent with the PT-IC-seq measurements, PT-IC-ddPCR analysis confirmed the lower PT frequency in E. coli B7A. Our study has demonstrated the heterogeneity of PT modification in the bacterial population and we also established general tools for rigorous mapping and characterization of PT modification events at whole genome level. We describe to our knowledge the first genome-wide quantitative characterization of PT landscape and provides appropriate strategies for further functional studies of PT modification.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1008026</identifier><identifier>PMID: 30933976</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bacteria ; Biology and Life Sciences ; Biotechnology ; Chromosome mapping ; Deoxyribonucleic acid ; DNA ; DNA methylation ; E coli ; Enzymes ; Epigenetics ; Escherichia coli ; Evolution ; Gene expression ; Gene mapping ; Genetic research ; Genomes ; Genomics ; Iodine ; Laboratories ; Life sciences ; Medicine and Health Sciences ; Metabolism ; Methylation ; Next-generation sequencing ; Phosphorothioate ; Phosphorus compounds ; Physical Sciences ; Physiology ; Post-translational modifications ; Prokaryotes ; Research and Analysis Methods ; Salmonella</subject><ispartof>PLoS genetics, 2019-04, Vol.15 (4), p.e1008026-e1008026</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>2019 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2019 Li et al 2019 Li et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c792t-ec579238892498ec13f39b6acc1a6c787e0896c344515504be0d5e68ca01e21f3</citedby><cites>FETCH-LOGICAL-c792t-ec579238892498ec13f39b6acc1a6c787e0896c344515504be0d5e68ca01e21f3</cites><orcidid>0000-0001-6195-8720 ; 0000-0003-1644-9825</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6459556/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6459556/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30933976$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Song, Chunxiao</contributor><creatorcontrib>Li, Jinli</creatorcontrib><creatorcontrib>Chen, Yi</creatorcontrib><creatorcontrib>Zheng, Tao</creatorcontrib><creatorcontrib>Kong, Lingxin</creatorcontrib><creatorcontrib>Zhu, Sucheng</creatorcontrib><creatorcontrib>Sun, Yihua</creatorcontrib><creatorcontrib>Deng, Zixin</creatorcontrib><creatorcontrib>Yang, Litao</creatorcontrib><creatorcontrib>You, Delin</creatorcontrib><title>Quantitative mapping of DNA phosphorothioatome reveals phosphorothioate heterogeneity of low modification frequency</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Phosphorothioate (PT) modifications of the DNA backbone, widespread in prokaryotes, are first identified in bacterial enteropathogens Escherichia coli B7A more than a decade ago. However, methods for high resolution mapping of PT modification level are still lacking. Here, we developed the PT-IC-seq technique, based on iodine-induced selective cleavage at PT sites and high-throughput next generation sequencing, as a mean to quantitatively characterizing the genomic landscape of PT modifications. Using PT-IC-seq we foud that most PT sites are partially modified at a lower PT frequency (< 5%) in E. coli B7A and Salmonella enterica serovar Cerro 87, and both show a heterogeneity pattern of PT modification similar to those of the typical methylation modification. Combining the iodine-induced cleavage and absolute quantification by droplet digital PCR, we developed the PT-IC-ddPCR technique to further measure the PT modification level. Consistent with the PT-IC-seq measurements, PT-IC-ddPCR analysis confirmed the lower PT frequency in E. coli B7A. Our study has demonstrated the heterogeneity of PT modification in the bacterial population and we also established general tools for rigorous mapping and characterization of PT modification events at whole genome level. We describe to our knowledge the first genome-wide quantitative characterization of PT landscape and provides appropriate strategies for further functional studies of PT modification.</description><subject>Bacteria</subject><subject>Biology and Life Sciences</subject><subject>Biotechnology</subject><subject>Chromosome mapping</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>E coli</subject><subject>Enzymes</subject><subject>Epigenetics</subject><subject>Escherichia coli</subject><subject>Evolution</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Genetic research</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Iodine</subject><subject>Laboratories</subject><subject>Life sciences</subject><subject>Medicine and Health Sciences</subject><subject>Metabolism</subject><subject>Methylation</subject><subject>Next-generation sequencing</subject><subject>Phosphorothioate</subject><subject>Phosphorus compounds</subject><subject>Physical Sciences</subject><subject>Physiology</subject><subject>Post-translational modifications</subject><subject>Prokaryotes</subject><subject>Research and Analysis 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mapping of DNA phosphorothioatome reveals phosphorothioate heterogeneity of low modification frequency</title><author>Li, Jinli ; Chen, Yi ; Zheng, Tao ; Kong, Lingxin ; Zhu, Sucheng ; Sun, Yihua ; Deng, Zixin ; Yang, Litao ; You, Delin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c792t-ec579238892498ec13f39b6acc1a6c787e0896c344515504be0d5e68ca01e21f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Bacteria</topic><topic>Biology and Life Sciences</topic><topic>Biotechnology</topic><topic>Chromosome mapping</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>E coli</topic><topic>Enzymes</topic><topic>Epigenetics</topic><topic>Escherichia coli</topic><topic>Evolution</topic><topic>Gene expression</topic><topic>Gene mapping</topic><topic>Genetic research</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Iodine</topic><topic>Laboratories</topic><topic>Life sciences</topic><topic>Medicine and Health Sciences</topic><topic>Metabolism</topic><topic>Methylation</topic><topic>Next-generation sequencing</topic><topic>Phosphorothioate</topic><topic>Phosphorus compounds</topic><topic>Physical Sciences</topic><topic>Physiology</topic><topic>Post-translational modifications</topic><topic>Prokaryotes</topic><topic>Research and Analysis Methods</topic><topic>Salmonella</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Jinli</creatorcontrib><creatorcontrib>Chen, Yi</creatorcontrib><creatorcontrib>Zheng, Tao</creatorcontrib><creatorcontrib>Kong, Lingxin</creatorcontrib><creatorcontrib>Zhu, Sucheng</creatorcontrib><creatorcontrib>Sun, Yihua</creatorcontrib><creatorcontrib>Deng, Zixin</creatorcontrib><creatorcontrib>Yang, Litao</creatorcontrib><creatorcontrib>You, 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Yi</au><au>Zheng, Tao</au><au>Kong, Lingxin</au><au>Zhu, Sucheng</au><au>Sun, Yihua</au><au>Deng, Zixin</au><au>Yang, Litao</au><au>You, Delin</au><au>Song, Chunxiao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Quantitative mapping of DNA phosphorothioatome reveals phosphorothioate heterogeneity of low modification frequency</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2019-04-01</date><risdate>2019</risdate><volume>15</volume><issue>4</issue><spage>e1008026</spage><epage>e1008026</epage><pages>e1008026-e1008026</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Phosphorothioate (PT) modifications of the DNA backbone, widespread in prokaryotes, are first identified in bacterial enteropathogens Escherichia coli B7A more than a decade ago. However, methods for high resolution mapping of PT modification level are still lacking. Here, we developed the PT-IC-seq technique, based on iodine-induced selective cleavage at PT sites and high-throughput next generation sequencing, as a mean to quantitatively characterizing the genomic landscape of PT modifications. Using PT-IC-seq we foud that most PT sites are partially modified at a lower PT frequency (< 5%) in E. coli B7A and Salmonella enterica serovar Cerro 87, and both show a heterogeneity pattern of PT modification similar to those of the typical methylation modification. Combining the iodine-induced cleavage and absolute quantification by droplet digital PCR, we developed the PT-IC-ddPCR technique to further measure the PT modification level. Consistent with the PT-IC-seq measurements, PT-IC-ddPCR analysis confirmed the lower PT frequency in E. coli B7A. Our study has demonstrated the heterogeneity of PT modification in the bacterial population and we also established general tools for rigorous mapping and characterization of PT modification events at whole genome level. We describe to our knowledge the first genome-wide quantitative characterization of PT landscape and provides appropriate strategies for further functional studies of PT modification.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>30933976</pmid><doi>10.1371/journal.pgen.1008026</doi><orcidid>https://orcid.org/0000-0001-6195-8720</orcidid><orcidid>https://orcid.org/0000-0003-1644-9825</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Biology and Life Sciences Biotechnology Chromosome mapping Deoxyribonucleic acid DNA DNA methylation E coli Enzymes Epigenetics Escherichia coli Evolution Gene expression Gene mapping Genetic research Genomes Genomics Iodine Laboratories Life sciences Medicine and Health Sciences Metabolism Methylation Next-generation sequencing Phosphorothioate Phosphorus compounds Physical Sciences Physiology Post-translational modifications Prokaryotes Research and Analysis Methods Salmonella |
title | Quantitative mapping of DNA phosphorothioatome reveals phosphorothioate heterogeneity of low modification frequency |
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