Reprogramming of Yersinia from virulent to persistent mode revealed by complex in vivo RNA-seq analysis
We recently found that Yersinia pseudotuberculosis can be used as a model of persistent bacterial infections. We performed in vivo RNA-seq of bacteria in small cecal tissue biopsies at early and persistent stages of infection to determine strategies associated with persistence. Comprehensive analysi...
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| creator | Avican, Kemal Fahlgren, Anna Huss, Mikael Heroven, Ann Kathrin Beckstette, Michael Dersch, Petra Fällman, Maria |
| description | We recently found that Yersinia pseudotuberculosis can be used as a model of persistent bacterial infections. We performed in vivo RNA-seq of bacteria in small cecal tissue biopsies at early and persistent stages of infection to determine strategies associated with persistence. Comprehensive analysis of mixed RNA populations from infected tissues revealed that Y. pseudotuberculosis undergoes transcriptional reprogramming with drastic down-regulation of T3SS virulence genes during persistence when the pathogen resides within the cecum. At the persistent stage, the expression pattern in many respects resembles the pattern seen in vitro at 26oC, with for example, up-regulation of flagellar genes and invA. These findings are expected to have impact on future rationales to identify suitable bacterial targets for new antibiotics. Other genes that are up-regulated during persistence are genes involved in anaerobiosis, chemotaxis, and protection against oxidative and acidic stress, which indicates the influence of different environmental cues. We found that the Crp/CsrA/RovA regulatory cascades influence the pattern of bacterial gene expression during persistence. Furthermore, arcA, fnr, frdA, and wrbA play critical roles in persistence. Our findings suggest a model for the life cycle of this enteropathogen with reprogramming from a virulent to an adapted phenotype capable of persisting and spreading by fecal shedding. |
| doi_str_mv | 10.1371/journal.ppat.1004600 |
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We performed in vivo RNA-seq of bacteria in small cecal tissue biopsies at early and persistent stages of infection to determine strategies associated with persistence. Comprehensive analysis of mixed RNA populations from infected tissues revealed that Y. pseudotuberculosis undergoes transcriptional reprogramming with drastic down-regulation of T3SS virulence genes during persistence when the pathogen resides within the cecum. At the persistent stage, the expression pattern in many respects resembles the pattern seen in vitro at 26oC, with for example, up-regulation of flagellar genes and invA. These findings are expected to have impact on future rationales to identify suitable bacterial targets for new antibiotics. Other genes that are up-regulated during persistence are genes involved in anaerobiosis, chemotaxis, and protection against oxidative and acidic stress, which indicates the influence of different environmental cues. We found that the Crp/CsrA/RovA regulatory cascades influence the pattern of bacterial gene expression during persistence. Furthermore, arcA, fnr, frdA, and wrbA play critical roles in persistence. Our findings suggest a model for the life cycle of this enteropathogen with reprogramming from a virulent to an adapted phenotype capable of persisting and spreading by fecal shedding.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1004600</identifier><identifier>PMID: 25590628</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antibiotics ; arcA ; Bacteria ; Bacterial infections ; Biopsy ; Cecum - immunology ; Cecum - microbiology ; Cecum - pathology ; Environmental Science ; Female ; fnr ; Gene expression ; Gene Expression Regulation, Bacterial ; Genes, Bacterial ; Genetic aspects ; Genotype & phenotype ; Health aspects ; Infections ; Methods ; Mice ; Microarray Analysis ; Microbiota - immunology ; miljövetenskap ; Persistent infection ; PMNs ; rfaH ; RNA sequencing ; RNA, Bacterial - genetics ; RNA-seq ; rovA ; Sequence Analysis, RNA - methods ; Text editing ; Transcriptome ; Virulence (Microbiology) ; Virulence - genetics ; wrba ; Yersinia ; Yersinia pseudotuberculosis - genetics ; Yersinia pseudotuberculosis - immunology ; Yersinia pseudotuberculosis - pathogenicity ; Yersinia pseudotuberculosis Infections - genetics ; Yersinia pseudotuberculosis Infections - immunology ; Yersinia pseudotuberculosis Infections - pathology</subject><ispartof>PLoS pathogens, 2015-01, Vol.11 (1), p.e1004600-e1004600</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Avican et al 2015 Avican et al</rights><rights>2015 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: RNA-seq Analysis. PLoS Pathog 11(1): e1004600. doi:10.1371/journal.ppat.1004600</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c779t-c96a06f841dd2e8508b6572f7c8aab6c29c452e79ceee9e3601ba875806ed8ca3</citedby><cites>FETCH-LOGICAL-c779t-c96a06f841dd2e8508b6572f7c8aab6c29c452e79ceee9e3601ba875806ed8ca3</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/PMC4295882/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4295882/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,550,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25590628$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:kth:diva-161637$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-100980$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Avican, Kemal</creatorcontrib><creatorcontrib>Fahlgren, Anna</creatorcontrib><creatorcontrib>Huss, Mikael</creatorcontrib><creatorcontrib>Heroven, Ann Kathrin</creatorcontrib><creatorcontrib>Beckstette, Michael</creatorcontrib><creatorcontrib>Dersch, Petra</creatorcontrib><creatorcontrib>Fällman, Maria</creatorcontrib><title>Reprogramming of Yersinia from virulent to persistent mode revealed by complex in vivo RNA-seq analysis</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>We recently found that Yersinia pseudotuberculosis can be used as a model of persistent bacterial infections. We performed in vivo RNA-seq of bacteria in small cecal tissue biopsies at early and persistent stages of infection to determine strategies associated with persistence. Comprehensive analysis of mixed RNA populations from infected tissues revealed that Y. pseudotuberculosis undergoes transcriptional reprogramming with drastic down-regulation of T3SS virulence genes during persistence when the pathogen resides within the cecum. At the persistent stage, the expression pattern in many respects resembles the pattern seen in vitro at 26oC, with for example, up-regulation of flagellar genes and invA. These findings are expected to have impact on future rationales to identify suitable bacterial targets for new antibiotics. Other genes that are up-regulated during persistence are genes involved in anaerobiosis, chemotaxis, and protection against oxidative and acidic stress, which indicates the influence of different environmental cues. We found that the Crp/CsrA/RovA regulatory cascades influence the pattern of bacterial gene expression during persistence. Furthermore, arcA, fnr, frdA, and wrbA play critical roles in persistence. Our findings suggest a model for the life cycle of this enteropathogen with reprogramming from a virulent to an adapted phenotype capable of persisting and spreading by fecal shedding.</description><subject>Animals</subject><subject>Antibiotics</subject><subject>arcA</subject><subject>Bacteria</subject><subject>Bacterial infections</subject><subject>Biopsy</subject><subject>Cecum - immunology</subject><subject>Cecum - microbiology</subject><subject>Cecum - pathology</subject><subject>Environmental Science</subject><subject>Female</subject><subject>fnr</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genes, Bacterial</subject><subject>Genetic aspects</subject><subject>Genotype & phenotype</subject><subject>Health aspects</subject><subject>Infections</subject><subject>Methods</subject><subject>Mice</subject><subject>Microarray Analysis</subject><subject>Microbiota - immunology</subject><subject>miljövetenskap</subject><subject>Persistent infection</subject><subject>PMNs</subject><subject>rfaH</subject><subject>RNA sequencing</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA-seq</subject><subject>rovA</subject><subject>Sequence Analysis, RNA - methods</subject><subject>Text editing</subject><subject>Transcriptome</subject><subject>Virulence (Microbiology)</subject><subject>Virulence - genetics</subject><subject>wrba</subject><subject>Yersinia</subject><subject>Yersinia pseudotuberculosis - genetics</subject><subject>Yersinia pseudotuberculosis - immunology</subject><subject>Yersinia pseudotuberculosis - pathogenicity</subject><subject>Yersinia pseudotuberculosis Infections - genetics</subject><subject>Yersinia pseudotuberculosis Infections - immunology</subject><subject>Yersinia pseudotuberculosis Infections - pathology</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>D8T</sourceid><sourceid>DOA</sourceid><recordid>eNqVk0tv1DAUhSMEoqXwDxBYYgOLDLYTO_YGaVReI1VFKg-JleU4N6mHJE7tZOj8e5zOtOpILEBexLG_c3R9rm6SPCd4QbKCvF27yfe6XQyDHhcE45xj_CA5JoxlaZEV-cN7-6PkSQjryJCM8MfJEWVMYk7FcdJcwOBd43XX2b5BrkY_wQfbW41q7zq0sX5qoR_R6NAw34Rx_utcBcjDBnQLFSq3yLhuaOEa2T5KNg5dnC_TAFdIxxK3UfU0eVTrNsCz_fck-f7xw7fTz-nZl0-r0-VZaopCjqmRXGNei5xUFQXBsCg5K2hdGKF1yQ2VJmcUCmkAQELGMSm1KJjAHCphdHaSvNz5Dq0Lap9RUIQLRmV8PYnEakdUTq_V4G2n_VY5bdXNgfON0n60pgVlsKZMaqox47kshChxLnnFapCSFCWNXunOK_yGYSoP3N7bH8sbt6mbVOyPFPjf-F_jZayX8KyI_Lv9a6ayg8rE6L1uD2SHN729VI3bqJxKJsRc4Ou9gXdXE4RRdTYYaFvdg5vmXBjNcc6wjOirHdrEnirb1y46mhlXy5yILM8yziO1-AsVVwWdNa6H2sbzA8GbA0FkRrgeGz2FoFZfL_6DPT9k8x1rvAvBQ32XCsFqHpDb5qt5QNR-QKLsxf1E70S3E5H9ASZ1DWE</recordid><startdate>20150101</startdate><enddate>20150101</enddate><creator>Avican, Kemal</creator><creator>Fahlgren, Anna</creator><creator>Huss, Mikael</creator><creator>Heroven, Ann Kathrin</creator><creator>Beckstette, Michael</creator><creator>Dersch, Petra</creator><creator>Fällman, Maria</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>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8V</scope><scope>ADHXS</scope><scope>D8T</scope><scope>D93</scope><scope>ZZAVC</scope><scope>DOA</scope></search><sort><creationdate>20150101</creationdate><title>Reprogramming of Yersinia from virulent to persistent mode revealed by complex in vivo RNA-seq analysis</title><author>Avican, Kemal ; Fahlgren, Anna ; Huss, Mikael ; Heroven, Ann Kathrin ; Beckstette, Michael ; Dersch, Petra ; Fällman, Maria</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c779t-c96a06f841dd2e8508b6572f7c8aab6c29c452e79ceee9e3601ba875806ed8ca3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Antibiotics</topic><topic>arcA</topic><topic>Bacteria</topic><topic>Bacterial infections</topic><topic>Biopsy</topic><topic>Cecum - immunology</topic><topic>Cecum - microbiology</topic><topic>Cecum - pathology</topic><topic>Environmental Science</topic><topic>Female</topic><topic>fnr</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genes, Bacterial</topic><topic>Genetic aspects</topic><topic>Genotype & phenotype</topic><topic>Health aspects</topic><topic>Infections</topic><topic>Methods</topic><topic>Mice</topic><topic>Microarray Analysis</topic><topic>Microbiota - immunology</topic><topic>miljövetenskap</topic><topic>Persistent infection</topic><topic>PMNs</topic><topic>rfaH</topic><topic>RNA sequencing</topic><topic>RNA, Bacterial - genetics</topic><topic>RNA-seq</topic><topic>rovA</topic><topic>Sequence Analysis, RNA - methods</topic><topic>Text editing</topic><topic>Transcriptome</topic><topic>Virulence (Microbiology)</topic><topic>Virulence - genetics</topic><topic>wrba</topic><topic>Yersinia</topic><topic>Yersinia pseudotuberculosis - genetics</topic><topic>Yersinia pseudotuberculosis - immunology</topic><topic>Yersinia pseudotuberculosis - pathogenicity</topic><topic>Yersinia pseudotuberculosis Infections - genetics</topic><topic>Yersinia pseudotuberculosis Infections - immunology</topic><topic>Yersinia pseudotuberculosis Infections - pathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Avican, Kemal</creatorcontrib><creatorcontrib>Fahlgren, Anna</creatorcontrib><creatorcontrib>Huss, Mikael</creatorcontrib><creatorcontrib>Heroven, Ann Kathrin</creatorcontrib><creatorcontrib>Beckstette, Michael</creatorcontrib><creatorcontrib>Dersch, Petra</creatorcontrib><creatorcontrib>Fällman, Maria</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Kungliga Tekniska Högskolan</collection><collection>SWEPUB Umeå universitet full text</collection><collection>SWEPUB Freely available online</collection><collection>SWEPUB Umeå universitet</collection><collection>SwePub Articles full text</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Avican, Kemal</au><au>Fahlgren, Anna</au><au>Huss, Mikael</au><au>Heroven, Ann Kathrin</au><au>Beckstette, Michael</au><au>Dersch, Petra</au><au>Fällman, Maria</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reprogramming of Yersinia from virulent to persistent mode revealed by complex in vivo RNA-seq analysis</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2015-01-01</date><risdate>2015</risdate><volume>11</volume><issue>1</issue><spage>e1004600</spage><epage>e1004600</epage><pages>e1004600-e1004600</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>We recently found that Yersinia pseudotuberculosis can be used as a model of persistent bacterial infections. We performed in vivo RNA-seq of bacteria in small cecal tissue biopsies at early and persistent stages of infection to determine strategies associated with persistence. Comprehensive analysis of mixed RNA populations from infected tissues revealed that Y. pseudotuberculosis undergoes transcriptional reprogramming with drastic down-regulation of T3SS virulence genes during persistence when the pathogen resides within the cecum. At the persistent stage, the expression pattern in many respects resembles the pattern seen in vitro at 26oC, with for example, up-regulation of flagellar genes and invA. These findings are expected to have impact on future rationales to identify suitable bacterial targets for new antibiotics. Other genes that are up-regulated during persistence are genes involved in anaerobiosis, chemotaxis, and protection against oxidative and acidic stress, which indicates the influence of different environmental cues. We found that the Crp/CsrA/RovA regulatory cascades influence the pattern of bacterial gene expression during persistence. Furthermore, arcA, fnr, frdA, and wrbA play critical roles in persistence. Our findings suggest a model for the life cycle of this enteropathogen with reprogramming from a virulent to an adapted phenotype capable of persisting and spreading by fecal shedding.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25590628</pmid><doi>10.1371/journal.ppat.1004600</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Antibiotics arcA Bacteria Bacterial infections Biopsy Cecum - immunology Cecum - microbiology Cecum - pathology Environmental Science Female fnr Gene expression Gene Expression Regulation, Bacterial Genes, Bacterial Genetic aspects Genotype & phenotype Health aspects Infections Methods Mice Microarray Analysis Microbiota - immunology miljövetenskap Persistent infection PMNs rfaH RNA sequencing RNA, Bacterial - genetics RNA-seq rovA Sequence Analysis, RNA - methods Text editing Transcriptome Virulence (Microbiology) Virulence - genetics wrba Yersinia Yersinia pseudotuberculosis - genetics Yersinia pseudotuberculosis - immunology Yersinia pseudotuberculosis - pathogenicity Yersinia pseudotuberculosis Infections - genetics Yersinia pseudotuberculosis Infections - immunology Yersinia pseudotuberculosis Infections - pathology |
| title | Reprogramming of Yersinia from virulent to persistent mode revealed by complex in vivo RNA-seq analysis |
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