Genome replication dynamics of a bacteriophage and its satellite reveal strategies for parasitism and viral restriction
Abstract Phage-inducible chromosomal island-like elements (PLEs) are bacteriophage satellites found in Vibrio cholerae. PLEs parasitize the lytic phage ICP1, excising from the bacterial chromosome, replicating, and mobilizing to new host cells following cell lysis. PLEs protect their host cell popul...
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| Veröffentlicht in: | Nucleic acids research 2020-01, Vol.48 (1), p.249-263 |
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| creator | Barth, Zachary K Silvas, Tania V Angermeyer, Angus Seed, Kimberley D |
| description | Abstract
Phage-inducible chromosomal island-like elements (PLEs) are bacteriophage satellites found in Vibrio cholerae. PLEs parasitize the lytic phage ICP1, excising from the bacterial chromosome, replicating, and mobilizing to new host cells following cell lysis. PLEs protect their host cell populations by completely restricting the production of ICP1 progeny. Previously, it was found that ICP1 replication was reduced during PLE(+) infection. Despite robust replication of the PLE genome, relatively few transducing units are produced. We investigated if PLE DNA replication itself is antagonistic to ICP1 replication. Here we identify key constituents of PLE replication and assess their role in interference of ICP1. PLE encodes a RepA_N initiation factor that is sufficient to drive replication from the PLE origin of replication during ICP1 infection. In contrast to previously characterized bacteriophage satellites, expression of the PLE initiation factor was not sufficient for PLE replication in the absence of phage. Replication of PLE was necessary for interference of ICP1 DNA replication, but replication of a minimalized PLE replicon was not sufficient for ICP1 DNA replication interference. Despite restoration of ICP1 DNA replication, non-replicating PLE remained broadly inhibitory against ICP1. These results suggest that PLE DNA replication is one of multiple mechanisms contributing to ICP1 restriction. |
| doi_str_mv | 10.1093/nar/gkz1005 |
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Phage-inducible chromosomal island-like elements (PLEs) are bacteriophage satellites found in Vibrio cholerae. PLEs parasitize the lytic phage ICP1, excising from the bacterial chromosome, replicating, and mobilizing to new host cells following cell lysis. PLEs protect their host cell populations by completely restricting the production of ICP1 progeny. Previously, it was found that ICP1 replication was reduced during PLE(+) infection. Despite robust replication of the PLE genome, relatively few transducing units are produced. We investigated if PLE DNA replication itself is antagonistic to ICP1 replication. Here we identify key constituents of PLE replication and assess their role in interference of ICP1. PLE encodes a RepA_N initiation factor that is sufficient to drive replication from the PLE origin of replication during ICP1 infection. In contrast to previously characterized bacteriophage satellites, expression of the PLE initiation factor was not sufficient for PLE replication in the absence of phage. Replication of PLE was necessary for interference of ICP1 DNA replication, but replication of a minimalized PLE replicon was not sufficient for ICP1 DNA replication interference. Despite restoration of ICP1 DNA replication, non-replicating PLE remained broadly inhibitory against ICP1. These results suggest that PLE DNA replication is one of multiple mechanisms contributing to ICP1 restriction.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkz1005</identifier><identifier>PMID: 31667508</identifier><language>eng</language><publisher>OXFORD: Oxford University Press</publisher><subject>Bacteriophages - genetics ; Bacteriophages - metabolism ; Biochemistry & Molecular Biology ; Chromosomes, Bacterial - chemistry ; Chromosomes, Bacterial - immunology ; Chromosomes, Bacterial - virology ; DNA Helicases - genetics ; DNA Helicases - immunology ; DNA Replication ; DNA, Bacterial - genetics ; DNA, Bacterial - immunology ; Genome Integrity, Repair and ; Life Sciences & Biomedicine ; Lysogeny - genetics ; Replication Origin ; Science & Technology ; Vibrio cholerae - genetics ; Vibrio cholerae - immunology ; Vibrio cholerae - virology ; Virus Replication - genetics</subject><ispartof>Nucleic acids research, 2020-01, Vol.48 (1), p.249-263</ispartof><rights>The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research. 2019</rights><rights>The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>27</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000524741700024</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c412t-84993ac7ced9563dc0dd8b3eb1af2a8a46df7d5d2ea538bff4f313d052c839243</citedby><cites>FETCH-LOGICAL-c412t-84993ac7ced9563dc0dd8b3eb1af2a8a46df7d5d2ea538bff4f313d052c839243</cites><orcidid>0000-0002-0139-1600 ; 0000-0002-9072-4760</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/PMC7145576/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7145576/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,1605,2115,27929,27930,28253,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31667508$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Barth, Zachary K</creatorcontrib><creatorcontrib>Silvas, Tania V</creatorcontrib><creatorcontrib>Angermeyer, Angus</creatorcontrib><creatorcontrib>Seed, Kimberley D</creatorcontrib><title>Genome replication dynamics of a bacteriophage and its satellite reveal strategies for parasitism and viral restriction</title><title>Nucleic acids research</title><addtitle>NUCLEIC ACIDS RES</addtitle><addtitle>Nucleic Acids Res</addtitle><description>Abstract
Phage-inducible chromosomal island-like elements (PLEs) are bacteriophage satellites found in Vibrio cholerae. PLEs parasitize the lytic phage ICP1, excising from the bacterial chromosome, replicating, and mobilizing to new host cells following cell lysis. PLEs protect their host cell populations by completely restricting the production of ICP1 progeny. Previously, it was found that ICP1 replication was reduced during PLE(+) infection. Despite robust replication of the PLE genome, relatively few transducing units are produced. We investigated if PLE DNA replication itself is antagonistic to ICP1 replication. Here we identify key constituents of PLE replication and assess their role in interference of ICP1. PLE encodes a RepA_N initiation factor that is sufficient to drive replication from the PLE origin of replication during ICP1 infection. In contrast to previously characterized bacteriophage satellites, expression of the PLE initiation factor was not sufficient for PLE replication in the absence of phage. Replication of PLE was necessary for interference of ICP1 DNA replication, but replication of a minimalized PLE replicon was not sufficient for ICP1 DNA replication interference. Despite restoration of ICP1 DNA replication, non-replicating PLE remained broadly inhibitory against ICP1. These results suggest that PLE DNA replication is one of multiple mechanisms contributing to ICP1 restriction.</description><subject>Bacteriophages - genetics</subject><subject>Bacteriophages - metabolism</subject><subject>Biochemistry & Molecular Biology</subject><subject>Chromosomes, Bacterial - chemistry</subject><subject>Chromosomes, Bacterial - immunology</subject><subject>Chromosomes, Bacterial - virology</subject><subject>DNA Helicases - genetics</subject><subject>DNA Helicases - immunology</subject><subject>DNA Replication</subject><subject>DNA, Bacterial - genetics</subject><subject>DNA, Bacterial - immunology</subject><subject>Genome Integrity, Repair and</subject><subject>Life Sciences & Biomedicine</subject><subject>Lysogeny - genetics</subject><subject>Replication Origin</subject><subject>Science & Technology</subject><subject>Vibrio cholerae - genetics</subject><subject>Vibrio cholerae - immunology</subject><subject>Vibrio cholerae - virology</subject><subject>Virus Replication - genetics</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><recordid>eNqNkUuLFDEUhQtRnHZ05V6yEmEoJ896bIShcUZhwI2uw608eqJVSZmkehh_vemHrW7EVULynXPP5VTVS4LfEtyzSw_xcvPtB8FYPKpWhDW05n1DH1crzLCoCebdWfUspa8YE04Ef1qdMdI0rcDdqrq_MT5MBkUzj05BdsEj_eBhciqhYBGgAVQ20YX5DjYGgdfI5YQSZDOOLu-UWwMjSjmWp40zCdkQ0QwRkssuTXvJ1sXCRFMop3ZDnldPLIzJvDie59WX6_ef1x_q2083H9dXt7XihOa6433PQLXK6F40TCusdTcwMxCwFDrgjbatFpoaEKwbrOWWEaaxoKpjPeXsvHp38J2XYTJaGV9yjnKOboL4IAM4-fePd3dyE7ayJVyItikGb44GMXxfygJyckmV3cGbsCRJGcEtob1gBb04oCqGlKKxpzEEy11VslQlj1UV-tWfyU7sr25-292bIdiknPHKnDBcPChvOWnLbb9o9__02uV91euw-Fykrw_SsMz_jPwT0mfCWg</recordid><startdate>20200110</startdate><enddate>20200110</enddate><creator>Barth, Zachary K</creator><creator>Silvas, Tania V</creator><creator>Angermeyer, Angus</creator><creator>Seed, Kimberley D</creator><general>Oxford University Press</general><general>Oxford Univ Press</general><scope>TOX</scope><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</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><orcidid>https://orcid.org/0000-0002-0139-1600</orcidid><orcidid>https://orcid.org/0000-0002-9072-4760</orcidid></search><sort><creationdate>20200110</creationdate><title>Genome replication dynamics of a bacteriophage and its satellite reveal strategies for parasitism and viral restriction</title><author>Barth, Zachary K ; Silvas, Tania V ; Angermeyer, Angus ; Seed, Kimberley D</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-84993ac7ced9563dc0dd8b3eb1af2a8a46df7d5d2ea538bff4f313d052c839243</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Bacteriophages - genetics</topic><topic>Bacteriophages - metabolism</topic><topic>Biochemistry & Molecular Biology</topic><topic>Chromosomes, Bacterial - chemistry</topic><topic>Chromosomes, Bacterial - immunology</topic><topic>Chromosomes, Bacterial - virology</topic><topic>DNA Helicases - genetics</topic><topic>DNA Helicases - immunology</topic><topic>DNA Replication</topic><topic>DNA, Bacterial - genetics</topic><topic>DNA, Bacterial - immunology</topic><topic>Genome Integrity, Repair and</topic><topic>Life Sciences & Biomedicine</topic><topic>Lysogeny - genetics</topic><topic>Replication Origin</topic><topic>Science & Technology</topic><topic>Vibrio cholerae - genetics</topic><topic>Vibrio cholerae - immunology</topic><topic>Vibrio cholerae - virology</topic><topic>Virus Replication - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barth, Zachary K</creatorcontrib><creatorcontrib>Silvas, Tania V</creatorcontrib><creatorcontrib>Angermeyer, Angus</creatorcontrib><creatorcontrib>Seed, Kimberley D</creatorcontrib><collection>Access via Oxford University Press (Open Access Collection)</collection><collection>Web of Science - Science Citation Index Expanded - 2020</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</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>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barth, Zachary K</au><au>Silvas, Tania V</au><au>Angermeyer, Angus</au><au>Seed, Kimberley D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome replication dynamics of a bacteriophage and its satellite reveal strategies for parasitism and viral restriction</atitle><jtitle>Nucleic acids research</jtitle><stitle>NUCLEIC ACIDS RES</stitle><addtitle>Nucleic Acids Res</addtitle><date>2020-01-10</date><risdate>2020</risdate><volume>48</volume><issue>1</issue><spage>249</spage><epage>263</epage><pages>249-263</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Abstract
Phage-inducible chromosomal island-like elements (PLEs) are bacteriophage satellites found in Vibrio cholerae. PLEs parasitize the lytic phage ICP1, excising from the bacterial chromosome, replicating, and mobilizing to new host cells following cell lysis. PLEs protect their host cell populations by completely restricting the production of ICP1 progeny. Previously, it was found that ICP1 replication was reduced during PLE(+) infection. Despite robust replication of the PLE genome, relatively few transducing units are produced. We investigated if PLE DNA replication itself is antagonistic to ICP1 replication. Here we identify key constituents of PLE replication and assess their role in interference of ICP1. PLE encodes a RepA_N initiation factor that is sufficient to drive replication from the PLE origin of replication during ICP1 infection. In contrast to previously characterized bacteriophage satellites, expression of the PLE initiation factor was not sufficient for PLE replication in the absence of phage. Replication of PLE was necessary for interference of ICP1 DNA replication, but replication of a minimalized PLE replicon was not sufficient for ICP1 DNA replication interference. Despite restoration of ICP1 DNA replication, non-replicating PLE remained broadly inhibitory against ICP1. These results suggest that PLE DNA replication is one of multiple mechanisms contributing to ICP1 restriction.</abstract><cop>OXFORD</cop><pub>Oxford University Press</pub><pmid>31667508</pmid><doi>10.1093/nar/gkz1005</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-0139-1600</orcidid><orcidid>https://orcid.org/0000-0002-9072-4760</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Bacteriophages - genetics Bacteriophages - metabolism Biochemistry & Molecular Biology Chromosomes, Bacterial - chemistry Chromosomes, Bacterial - immunology Chromosomes, Bacterial - virology DNA Helicases - genetics DNA Helicases - immunology DNA Replication DNA, Bacterial - genetics DNA, Bacterial - immunology Genome Integrity, Repair and Life Sciences & Biomedicine Lysogeny - genetics Replication Origin Science & Technology Vibrio cholerae - genetics Vibrio cholerae - immunology Vibrio cholerae - virology Virus Replication - genetics |
| title | Genome replication dynamics of a bacteriophage and its satellite reveal strategies for parasitism and viral restriction |
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