Control of competence for DNA transformation in streptococcus suis by genetically transferable pherotypes
Here we show that S. suis, a major bacterial pathogen of pigs and emerging pathogen in humans responds to a peptide pheromone by developing competence for DNA transformation. This species does not fall within any of the phylogenetic clusters of streptococci previously shown to regulate competence vi...
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description | Here we show that S. suis, a major bacterial pathogen of pigs and emerging pathogen in humans responds to a peptide pheromone by developing competence for DNA transformation. This species does not fall within any of the phylogenetic clusters of streptococci previously shown to regulate competence via peptide pheromones suggesting that more species of streptococci may be naturally competent. Induction of competence was dependent on ComX, a sigma factor that controls the streptococcal late competence regulon, extracellular addition of a comX-inducing peptide (XIP), and ComR, a regulator of comX. XIP was identified as an N-terminally truncated variant of ComS. Different comS alleles are present among strains of S. suis. These comS alleles are not functionally equivalent and appear to operate in conjuction with a cognate ComR to regulate comX through a conserved comR-box promoter. We demonstrate that these 'pherotypes' can be genetically transferred between strains, suggesting that similar approaches might be used to control competence induction in other lactic acid bacteria that lack ComR/ComS homologues but possess comX and the late competence regulon. The approaches described in this paper to identify and optimize peptide-induced competence may also assist other researchers wishing to identify natural competence in other bacteria. Harnessing natural competence is expected to accelerate genetic research on this and other important streptococcal pathogens and to allow high-throughput mutation approaches to be implemented, opening up new avenues for research. |
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This species does not fall within any of the phylogenetic clusters of streptococci previously shown to regulate competence via peptide pheromones suggesting that more species of streptococci may be naturally competent. Induction of competence was dependent on ComX, a sigma factor that controls the streptococcal late competence regulon, extracellular addition of a comX-inducing peptide (XIP), and ComR, a regulator of comX. XIP was identified as an N-terminally truncated variant of ComS. Different comS alleles are present among strains of S. suis. These comS alleles are not functionally equivalent and appear to operate in conjuction with a cognate ComR to regulate comX through a conserved comR-box promoter. We demonstrate that these 'pherotypes' can be genetically transferred between strains, suggesting that similar approaches might be used to control competence induction in other lactic acid bacteria that lack ComR/ComS homologues but possess comX and the late competence regulon. The approaches described in this paper to identify and optimize peptide-induced competence may also assist other researchers wishing to identify natural competence in other bacteria. Harnessing natural competence is expected to accelerate genetic research on this and other important streptococcal pathogens and to allow high-throughput mutation approaches to be implemented, opening up new avenues for research.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0099394</identifier><identifier>PMID: 24968201</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>activation ; Alleles ; Amino Acid Sequence ; Animal sciences ; Bacteria ; Bacterial genetics ; Bacterial Proteins - chemistry ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; bacterial transformation ; Binding sites ; Bioinformatics ; Biology and Life Sciences ; Cell division ; Deoxyribonucleic acid ; DNA ; DNA Transformation Competence - genetics ; expression ; Gene expression ; Genetic transformation ; Genomes ; Genomics ; haemophilus-influenzae ; Homology ; horizontal gene-transfer ; Lactic acid ; Lactic acid bacteria ; Lactobacillus ; Molecular Sequence Data ; Mutation ; Pathogens ; peptide pheromone ; Peptides ; Pheromones ; Phylogeny ; Pigs ; pneumoniae ; Proteins ; regulator ; Sigma factor ; Strains (organisms) ; Streptococcus infections ; Streptococcus pneumoniae ; Streptococcus suis ; Streptococcus suis - genetics ; Streptococcus thermophilus ; Swine ; system ; thermophilus ; Transcription Factors - chemistry ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transformation</subject><ispartof>PloS one, 2014-06, Vol.9 (6), p.e99394-e99394</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Zaccaria 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>2014 Zaccaria et al 2014 Zaccaria et al</rights><rights>Wageningen University & Research</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c809t-64a7fa9ee122523205088678b04c0bb9ccb5fee49154df662ea24f05111d9f853</citedby><cites>FETCH-LOGICAL-c809t-64a7fa9ee122523205088678b04c0bb9ccb5fee49154df662ea24f05111d9f853</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/PMC4072589/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4072589/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24968201$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zaccaria, Edoardo</creatorcontrib><creatorcontrib>van Baarlen, Peter</creatorcontrib><creatorcontrib>de Greeff, Astrid</creatorcontrib><creatorcontrib>Morrison, Donald A</creatorcontrib><creatorcontrib>Smith, Hilde</creatorcontrib><creatorcontrib>Wells, Jerry M</creatorcontrib><title>Control of competence for DNA transformation in streptococcus suis by genetically transferable pherotypes</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Here we show that S. suis, a major bacterial pathogen of pigs and emerging pathogen in humans responds to a peptide pheromone by developing competence for DNA transformation. This species does not fall within any of the phylogenetic clusters of streptococci previously shown to regulate competence via peptide pheromones suggesting that more species of streptococci may be naturally competent. Induction of competence was dependent on ComX, a sigma factor that controls the streptococcal late competence regulon, extracellular addition of a comX-inducing peptide (XIP), and ComR, a regulator of comX. XIP was identified as an N-terminally truncated variant of ComS. Different comS alleles are present among strains of S. suis. These comS alleles are not functionally equivalent and appear to operate in conjuction with a cognate ComR to regulate comX through a conserved comR-box promoter. We demonstrate that these 'pherotypes' can be genetically transferred between strains, suggesting that similar approaches might be used to control competence induction in other lactic acid bacteria that lack ComR/ComS homologues but possess comX and the late competence regulon. The approaches described in this paper to identify and optimize peptide-induced competence may also assist other researchers wishing to identify natural competence in other bacteria. Harnessing natural competence is expected to accelerate genetic research on this and other important streptococcal pathogens and to allow high-throughput mutation approaches to be implemented, opening up new avenues for research.</description><subject>activation</subject><subject>Alleles</subject><subject>Amino Acid Sequence</subject><subject>Animal sciences</subject><subject>Bacteria</subject><subject>Bacterial genetics</subject><subject>Bacterial Proteins - chemistry</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>bacterial transformation</subject><subject>Binding sites</subject><subject>Bioinformatics</subject><subject>Biology and Life Sciences</subject><subject>Cell division</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Transformation Competence - genetics</subject><subject>expression</subject><subject>Gene expression</subject><subject>Genetic transformation</subject><subject>Genomes</subject><subject>Genomics</subject><subject>haemophilus-influenzae</subject><subject>Homology</subject><subject>horizontal gene-transfer</subject><subject>Lactic acid</subject><subject>Lactic acid bacteria</subject><subject>Lactobacillus</subject><subject>Molecular Sequence Data</subject><subject>Mutation</subject><subject>Pathogens</subject><subject>peptide pheromone</subject><subject>Peptides</subject><subject>Pheromones</subject><subject>Phylogeny</subject><subject>Pigs</subject><subject>pneumoniae</subject><subject>Proteins</subject><subject>regulator</subject><subject>Sigma factor</subject><subject>Strains (organisms)</subject><subject>Streptococcus infections</subject><subject>Streptococcus pneumoniae</subject><subject>Streptococcus suis</subject><subject>Streptococcus suis - genetics</subject><subject>Streptococcus thermophilus</subject><subject>Swine</subject><subject>system</subject><subject>thermophilus</subject><subject>Transcription Factors - chemistry</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transformation</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk0uP0zAUhSMEYoaBf4AgEhKCRYud2EnMAqkqr0ojRuK1tRz3unXl2sF2GPrvcdrMqEWzQJHixPnOie-xb5Y9xWiKyxq_2bjeW2GmnbMwRYixkpF72TlmZTGpClTeP3o-yx6FsEGIlk1VPczOCsKqpkD4PNNzZ6N3Jncql27bQQQrIVfO5--_zPLohQ3pZSuidjbXNg_RQxeddFL2IQ-9Dnm7y1dgIWopjNmNGvCiNZB3a_Au7joIj7MHSpgAT8bxIvvx8cP3-efJ5dWnxXx2OZENYnFSEVErwQBwUdCiLBBFTVPVTYuIRG3LpGypAiAMU7JUVVWAKIhCFGO8ZKqh5UX2_ODbGRf4mFLgCUc1JawgiVgciKUTG955vRV-x53QfD_h_IoLn6oxwFmDkFBKorotiWgIgyVlSmJRC0KlVMnr7cHrWqQMtE03boWXOuwNjW79YH7de27NMHR9GzihtKFVEr8bl9q3W1hKSFshzMmKTr9YveYr95unUgrasGTwajTw7lcPIfKtDhKMERZcvy86nZWmYmVCX_yD3h3NSK1Eql5b5dJ_5WDKZwTXNStxNUQ8vYNK1xK2WqbzqHSaPxG8PhEkJsKfuBJ9CHzx7ev_s1c_T9mXR-wahInr4Ew_HNZwCpIDKL0LwYO6DRkjPrTTTRp8aCc-tlOSPTveoFvRTf-UfwG0px3M</recordid><startdate>20140626</startdate><enddate>20140626</enddate><creator>Zaccaria, Edoardo</creator><creator>van Baarlen, Peter</creator><creator>de Greeff, Astrid</creator><creator>Morrison, Donald A</creator><creator>Smith, Hilde</creator><creator>Wells, Jerry M</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>AEUYN</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>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>QVL</scope><scope>DOA</scope></search><sort><creationdate>20140626</creationdate><title>Control of competence for DNA transformation in streptococcus suis by genetically transferable pherotypes</title><author>Zaccaria, Edoardo ; van Baarlen, Peter ; de Greeff, Astrid ; Morrison, Donald A ; Smith, Hilde ; Wells, Jerry M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c809t-64a7fa9ee122523205088678b04c0bb9ccb5fee49154df662ea24f05111d9f853</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>activation</topic><topic>Alleles</topic><topic>Amino Acid Sequence</topic><topic>Animal sciences</topic><topic>Bacteria</topic><topic>Bacterial genetics</topic><topic>Bacterial Proteins - chemistry</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>bacterial transformation</topic><topic>Binding sites</topic><topic>Bioinformatics</topic><topic>Biology and Life Sciences</topic><topic>Cell division</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA Transformation Competence - genetics</topic><topic>expression</topic><topic>Gene expression</topic><topic>Genetic transformation</topic><topic>Genomes</topic><topic>Genomics</topic><topic>haemophilus-influenzae</topic><topic>Homology</topic><topic>horizontal gene-transfer</topic><topic>Lactic acid</topic><topic>Lactic acid bacteria</topic><topic>Lactobacillus</topic><topic>Molecular Sequence Data</topic><topic>Mutation</topic><topic>Pathogens</topic><topic>peptide pheromone</topic><topic>Peptides</topic><topic>Pheromones</topic><topic>Phylogeny</topic><topic>Pigs</topic><topic>pneumoniae</topic><topic>Proteins</topic><topic>regulator</topic><topic>Sigma factor</topic><topic>Strains (organisms)</topic><topic>Streptococcus infections</topic><topic>Streptococcus pneumoniae</topic><topic>Streptococcus suis</topic><topic>Streptococcus suis - genetics</topic><topic>Streptococcus thermophilus</topic><topic>Swine</topic><topic>system</topic><topic>thermophilus</topic><topic>Transcription Factors - chemistry</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Transformation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zaccaria, Edoardo</creatorcontrib><creatorcontrib>van Baarlen, Peter</creatorcontrib><creatorcontrib>de Greeff, Astrid</creatorcontrib><creatorcontrib>Morrison, Donald A</creatorcontrib><creatorcontrib>Smith, Hilde</creatorcontrib><creatorcontrib>Wells, Jerry M</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: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>NARCIS:Publications</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zaccaria, Edoardo</au><au>van Baarlen, Peter</au><au>de Greeff, Astrid</au><au>Morrison, Donald A</au><au>Smith, Hilde</au><au>Wells, Jerry M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Control of competence for DNA transformation in streptococcus suis by genetically transferable pherotypes</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-06-26</date><risdate>2014</risdate><volume>9</volume><issue>6</issue><spage>e99394</spage><epage>e99394</epage><pages>e99394-e99394</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Here we show that S. suis, a major bacterial pathogen of pigs and emerging pathogen in humans responds to a peptide pheromone by developing competence for DNA transformation. This species does not fall within any of the phylogenetic clusters of streptococci previously shown to regulate competence via peptide pheromones suggesting that more species of streptococci may be naturally competent. Induction of competence was dependent on ComX, a sigma factor that controls the streptococcal late competence regulon, extracellular addition of a comX-inducing peptide (XIP), and ComR, a regulator of comX. XIP was identified as an N-terminally truncated variant of ComS. Different comS alleles are present among strains of S. suis. These comS alleles are not functionally equivalent and appear to operate in conjuction with a cognate ComR to regulate comX through a conserved comR-box promoter. We demonstrate that these 'pherotypes' can be genetically transferred between strains, suggesting that similar approaches might be used to control competence induction in other lactic acid bacteria that lack ComR/ComS homologues but possess comX and the late competence regulon. The approaches described in this paper to identify and optimize peptide-induced competence may also assist other researchers wishing to identify natural competence in other bacteria. Harnessing natural competence is expected to accelerate genetic research on this and other important streptococcal pathogens and to allow high-throughput mutation approaches to be implemented, opening up new avenues for research.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24968201</pmid><doi>10.1371/journal.pone.0099394</doi><oa>free_for_read</oa></addata></record> |
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subjects | activation Alleles Amino Acid Sequence Animal sciences Bacteria Bacterial genetics Bacterial Proteins - chemistry Bacterial Proteins - genetics Bacterial Proteins - metabolism bacterial transformation Binding sites Bioinformatics Biology and Life Sciences Cell division Deoxyribonucleic acid DNA DNA Transformation Competence - genetics expression Gene expression Genetic transformation Genomes Genomics haemophilus-influenzae Homology horizontal gene-transfer Lactic acid Lactic acid bacteria Lactobacillus Molecular Sequence Data Mutation Pathogens peptide pheromone Peptides Pheromones Phylogeny Pigs pneumoniae Proteins regulator Sigma factor Strains (organisms) Streptococcus infections Streptococcus pneumoniae Streptococcus suis Streptococcus suis - genetics Streptococcus thermophilus Swine system thermophilus Transcription Factors - chemistry Transcription Factors - genetics Transcription Factors - metabolism Transformation |
title | Control of competence for DNA transformation in streptococcus suis by genetically transferable pherotypes |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-20T15%3A33%3A04IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Control%20of%20competence%20for%20DNA%20transformation%20in%20streptococcus%20suis%20by%20genetically%20transferable%20pherotypes&rft.jtitle=PloS%20one&rft.au=Zaccaria,%20Edoardo&rft.date=2014-06-26&rft.volume=9&rft.issue=6&rft.spage=e99394&rft.epage=e99394&rft.pages=e99394-e99394&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0099394&rft_dat=%3Cgale_plos_%3EA417793165%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1540754924&rft_id=info:pmid/24968201&rft_galeid=A417793165&rft_doaj_id=oai_doaj_org_article_9800affc07b34a849ed59fc1a7a45ccf&rfr_iscdi=true |