Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis
CRISPR interference confers adaptive, sequence-based immunity against viruses and plasmids and is specified by CRISPR RNAs (crRNAs) that are transcribed and processed from spacer-repeat units. Pre-crRNA processing is essential for CRISPR interference in all systems studied thus far. Here, our studie...
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| Veröffentlicht in: | Molecular cell 2013-05, Vol.50 (4), p.488-503 |
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| creator | Zhang, Yan Heidrich, Nadja Ampattu, Biju Joseph Gunderson, Carl W. Seifert, H. Steven Schoen, Christoph Vogel, Jörg Sontheimer, Erik J. |
| description | CRISPR interference confers adaptive, sequence-based immunity against viruses and plasmids and is specified by CRISPR RNAs (crRNAs) that are transcribed and processed from spacer-repeat units. Pre-crRNA processing is essential for CRISPR interference in all systems studied thus far. Here, our studies of crRNA biogenesis and CRISPR interference in naturally competent Neisseria spp. reveal a unique crRNA maturation pathway in which crRNAs are transcribed from promoters that are embedded within each repeat, yielding crRNA 5′ ends formed by transcription and not by processing. Although crRNA 3′ end formation involves RNase III and trans-encoded tracrRNA, as in other type II CRISPR systems, this processing is dispensable for interference. The meningococcal pathway is the most streamlined CRISPR/Cas system characterized to date. Endogenous CRISPR spacers limit natural transformation, which is the primary source of genetic variation that contributes to immune evasion, antibiotic resistance, and virulence in the human pathogen N. meningitidis.
•Unlike previously described CRISPRs, each Neisseria repeat carries its own promoter•Pre-crRNA processing is dispensable for CRISPR interference in Neisseria spp.•CRISPR interference blocks natural transformation in the pathogen N. meningitidis•Neisseria CRISPR/Cas systems are the most streamlined observed to date |
| doi_str_mv | 10.1016/j.molcel.2013.05.001 |
| format | Article |
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•Unlike previously described CRISPRs, each Neisseria repeat carries its own promoter•Pre-crRNA processing is dispensable for CRISPR interference in Neisseria spp.•CRISPR interference blocks natural transformation in the pathogen N. meningitidis•Neisseria CRISPR/Cas systems are the most streamlined observed to date</description><identifier>ISSN: 1097-2765</identifier><identifier>EISSN: 1097-4164</identifier><identifier>DOI: 10.1016/j.molcel.2013.05.001</identifier><identifier>PMID: 23706818</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>antibiotic resistance ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Base Sequence ; biogenesis ; Genes, Bacterial - genetics ; genetic variation ; Host-Pathogen Interactions ; Humans ; immune evasion ; immunity ; Inverted Repeat Sequences - genetics ; Meningococcal Infections - microbiology ; Models, Genetic ; Neisseria ; Neisseria meningitidis ; Neisseria meningitidis - genetics ; Neisseria meningitidis - pathogenicity ; Neisseria meningitidis - physiology ; pathogens ; plasmids ; Promoter Regions, Genetic - genetics ; Ribonuclease III - metabolism ; ribonucleases ; RNA ; RNA Processing, Post-Transcriptional ; RNA, Bacterial - genetics ; RNA, Bacterial - metabolism ; RNases ; Sequence Homology, Nucleic Acid ; Transcription, Genetic ; Transformation, Bacterial ; virulence ; Virulence - genetics ; viruses</subject><ispartof>Molecular cell, 2013-05, Vol.50 (4), p.488-503</ispartof><rights>2013 Elsevier Inc.</rights><rights>Copyright © 2013 Elsevier Inc. All rights reserved.</rights><rights>2013 Elsevier Inc. All rights reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c487t-bd4887d434319e7e46fd4eb9352dcba3ed2686cb91f0536a712a3748b7775f883</citedby><cites>FETCH-LOGICAL-c487t-bd4887d434319e7e46fd4eb9352dcba3ed2686cb91f0536a712a3748b7775f883</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.molcel.2013.05.001$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23706818$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Heidrich, Nadja</creatorcontrib><creatorcontrib>Ampattu, Biju Joseph</creatorcontrib><creatorcontrib>Gunderson, Carl W.</creatorcontrib><creatorcontrib>Seifert, H. Steven</creatorcontrib><creatorcontrib>Schoen, Christoph</creatorcontrib><creatorcontrib>Vogel, Jörg</creatorcontrib><creatorcontrib>Sontheimer, Erik J.</creatorcontrib><title>Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis</title><title>Molecular cell</title><addtitle>Mol Cell</addtitle><description>CRISPR interference confers adaptive, sequence-based immunity against viruses and plasmids and is specified by CRISPR RNAs (crRNAs) that are transcribed and processed from spacer-repeat units. Pre-crRNA processing is essential for CRISPR interference in all systems studied thus far. Here, our studies of crRNA biogenesis and CRISPR interference in naturally competent Neisseria spp. reveal a unique crRNA maturation pathway in which crRNAs are transcribed from promoters that are embedded within each repeat, yielding crRNA 5′ ends formed by transcription and not by processing. Although crRNA 3′ end formation involves RNase III and trans-encoded tracrRNA, as in other type II CRISPR systems, this processing is dispensable for interference. The meningococcal pathway is the most streamlined CRISPR/Cas system characterized to date. Endogenous CRISPR spacers limit natural transformation, which is the primary source of genetic variation that contributes to immune evasion, antibiotic resistance, and virulence in the human pathogen N. meningitidis.
•Unlike previously described CRISPRs, each Neisseria repeat carries its own promoter•Pre-crRNA processing is dispensable for CRISPR interference in Neisseria spp.•CRISPR interference blocks natural transformation in the pathogen N. meningitidis•Neisseria CRISPR/Cas systems are the most streamlined observed to date</description><subject>antibiotic resistance</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Base Sequence</subject><subject>biogenesis</subject><subject>Genes, Bacterial - genetics</subject><subject>genetic variation</subject><subject>Host-Pathogen Interactions</subject><subject>Humans</subject><subject>immune evasion</subject><subject>immunity</subject><subject>Inverted Repeat Sequences - genetics</subject><subject>Meningococcal Infections - microbiology</subject><subject>Models, Genetic</subject><subject>Neisseria</subject><subject>Neisseria meningitidis</subject><subject>Neisseria meningitidis - genetics</subject><subject>Neisseria meningitidis - pathogenicity</subject><subject>Neisseria meningitidis - physiology</subject><subject>pathogens</subject><subject>plasmids</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Ribonuclease III - metabolism</subject><subject>ribonucleases</subject><subject>RNA</subject><subject>RNA Processing, Post-Transcriptional</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA, Bacterial - metabolism</subject><subject>RNases</subject><subject>Sequence Homology, Nucleic Acid</subject><subject>Transcription, Genetic</subject><subject>Transformation, Bacterial</subject><subject>virulence</subject><subject>Virulence - genetics</subject><subject>viruses</subject><issn>1097-2765</issn><issn>1097-4164</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UU1v1DAQjRCIlsI_QJAjlwQ7dmznglSt-FhptVTb9sDJcuzJMqvEXuxsJf49rnbbwoXLeCS_efPmvaJ4S0lNCRUfd_UURgtj3RDKatLWhNBnxTklnaw4Ffz5qW-kaM-KVyntMoC3qntZnDVMEqGoOi9-XMVgISX022rpHewhFz-Xi83y-mpTbtaXqVzhhHO5NvMhmrG8icanIcTJzBh8ib5cA6YEEU05gc9EOKPD9Lp4MZgxwZvTe1Hcfvl8s_hWrb5_XS4uV5XlSs5V77hS0nHGGe1AAheD49B3rG2c7Q0D1wglbN_RgbRMGEkbwyRXvZSyHZRiF8WnI-_-0E_gbFafZep9xMnE3zoY1P_-ePypt-FOM9Fx3tBM8OFEEMOvA6RZT5iysaPxEA5JU9YK1pFGkQzlR6iNIaUIw-MaSvR9Knqnj6no-1Q0aXU2PY-9-1vi49BDDBnw_ggYTNBmGzHp2-vMIAghDc13P10J2co7hKiTRfAWHEaws3YB_6_hD-f-qkQ</recordid><startdate>20130523</startdate><enddate>20130523</enddate><creator>Zhang, Yan</creator><creator>Heidrich, Nadja</creator><creator>Ampattu, Biju Joseph</creator><creator>Gunderson, Carl W.</creator><creator>Seifert, H. Steven</creator><creator>Schoen, Christoph</creator><creator>Vogel, Jörg</creator><creator>Sontheimer, Erik J.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</scope><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20130523</creationdate><title>Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis</title><author>Zhang, Yan ; Heidrich, Nadja ; Ampattu, Biju Joseph ; Gunderson, Carl W. ; Seifert, H. Steven ; Schoen, Christoph ; Vogel, Jörg ; Sontheimer, Erik J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c487t-bd4887d434319e7e46fd4eb9352dcba3ed2686cb91f0536a712a3748b7775f883</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>antibiotic resistance</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Base Sequence</topic><topic>biogenesis</topic><topic>Genes, Bacterial - genetics</topic><topic>genetic variation</topic><topic>Host-Pathogen Interactions</topic><topic>Humans</topic><topic>immune evasion</topic><topic>immunity</topic><topic>Inverted Repeat Sequences - genetics</topic><topic>Meningococcal Infections - microbiology</topic><topic>Models, Genetic</topic><topic>Neisseria</topic><topic>Neisseria meningitidis</topic><topic>Neisseria meningitidis - genetics</topic><topic>Neisseria meningitidis - pathogenicity</topic><topic>Neisseria meningitidis - physiology</topic><topic>pathogens</topic><topic>plasmids</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Ribonuclease III - metabolism</topic><topic>ribonucleases</topic><topic>RNA</topic><topic>RNA Processing, Post-Transcriptional</topic><topic>RNA, Bacterial - genetics</topic><topic>RNA, Bacterial - metabolism</topic><topic>RNases</topic><topic>Sequence Homology, Nucleic Acid</topic><topic>Transcription, Genetic</topic><topic>Transformation, Bacterial</topic><topic>virulence</topic><topic>Virulence - genetics</topic><topic>viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Heidrich, Nadja</creatorcontrib><creatorcontrib>Ampattu, Biju Joseph</creatorcontrib><creatorcontrib>Gunderson, Carl W.</creatorcontrib><creatorcontrib>Seifert, H. Steven</creatorcontrib><creatorcontrib>Schoen, Christoph</creatorcontrib><creatorcontrib>Vogel, Jörg</creatorcontrib><creatorcontrib>Sontheimer, Erik J.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Yan</au><au>Heidrich, Nadja</au><au>Ampattu, Biju Joseph</au><au>Gunderson, Carl W.</au><au>Seifert, H. Steven</au><au>Schoen, Christoph</au><au>Vogel, Jörg</au><au>Sontheimer, Erik J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis</atitle><jtitle>Molecular cell</jtitle><addtitle>Mol Cell</addtitle><date>2013-05-23</date><risdate>2013</risdate><volume>50</volume><issue>4</issue><spage>488</spage><epage>503</epage><pages>488-503</pages><issn>1097-2765</issn><eissn>1097-4164</eissn><abstract>CRISPR interference confers adaptive, sequence-based immunity against viruses and plasmids and is specified by CRISPR RNAs (crRNAs) that are transcribed and processed from spacer-repeat units. Pre-crRNA processing is essential for CRISPR interference in all systems studied thus far. Here, our studies of crRNA biogenesis and CRISPR interference in naturally competent Neisseria spp. reveal a unique crRNA maturation pathway in which crRNAs are transcribed from promoters that are embedded within each repeat, yielding crRNA 5′ ends formed by transcription and not by processing. Although crRNA 3′ end formation involves RNase III and trans-encoded tracrRNA, as in other type II CRISPR systems, this processing is dispensable for interference. The meningococcal pathway is the most streamlined CRISPR/Cas system characterized to date. Endogenous CRISPR spacers limit natural transformation, which is the primary source of genetic variation that contributes to immune evasion, antibiotic resistance, and virulence in the human pathogen N. meningitidis.
•Unlike previously described CRISPRs, each Neisseria repeat carries its own promoter•Pre-crRNA processing is dispensable for CRISPR interference in Neisseria spp.•CRISPR interference blocks natural transformation in the pathogen N. meningitidis•Neisseria CRISPR/Cas systems are the most streamlined observed to date</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23706818</pmid><doi>10.1016/j.molcel.2013.05.001</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | antibiotic resistance Bacterial Proteins - genetics Bacterial Proteins - metabolism Base Sequence biogenesis Genes, Bacterial - genetics genetic variation Host-Pathogen Interactions Humans immune evasion immunity Inverted Repeat Sequences - genetics Meningococcal Infections - microbiology Models, Genetic Neisseria Neisseria meningitidis Neisseria meningitidis - genetics Neisseria meningitidis - pathogenicity Neisseria meningitidis - physiology pathogens plasmids Promoter Regions, Genetic - genetics Ribonuclease III - metabolism ribonucleases RNA RNA Processing, Post-Transcriptional RNA, Bacterial - genetics RNA, Bacterial - metabolism RNases Sequence Homology, Nucleic Acid Transcription, Genetic Transformation, Bacterial virulence Virulence - genetics viruses |
| title | Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis |
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