Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community
Summary Dental plaque biofilm formation proceeds through a developmental pathway initiated by the attachment of pioneer organisms, such as Streptococcus gordonii, to tooth surfaces. Through a variety of synergistic interactions, pioneer organisms facilitate the colonization of later arrivals includi...
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Veröffentlicht in: | Molecular microbiology 2006-04, Vol.60 (1), p.121-139 |
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creator | Kuboniwa, Masae Tribble, Gena D. James, Chloe E. Kilic, Ali O. Tao, Lin Herzberg, Mark C. Shizukuishi, Satoshi Lamont, Richard J. |
description | Summary
Dental plaque biofilm formation proceeds through a developmental pathway initiated by the attachment of pioneer organisms, such as Streptococcus gordonii, to tooth surfaces. Through a variety of synergistic interactions, pioneer organisms facilitate the colonization of later arrivals including Porphyromonas gingivalis, a potential periodontal pathogen. We have investigated genes of S. gordonii required to support a heterotypic biofilm community with P. gingivalis. By screening a plasmid integration library of S. gordonii, genes were identified that are crucial for the accumulation of planktonic P. gingivalis cells into a multispecies biofilm. These genes were further investigated by specific mutation and complementation analyses. The biofilm‐associated genes can be grouped into broad categories based on putative function as follows: (i) intercellular or intracellular signalling (cbe and spxB), (ii) cell wall integrity and maintenance of adhesive proteins (murE, msrA and atf), (iii) extracellular capsule biosynthesis (pgsA and atf), and (iv) physiology (gdhA, ccmA and ntpB). In addition, a gene for a hypothetical protein was identified. Biofilm visualization and quantification by confocal microscopy confirmed the role of these genes in the maturation of the multispecies community, including biofilm architectural development. The results suggest that S. gordonii governs the development of heterotypic oral biofilms through multiple genetic pathways. |
doi_str_mv | 10.1111/j.1365-2958.2006.05099.x |
format | Article |
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Dental plaque biofilm formation proceeds through a developmental pathway initiated by the attachment of pioneer organisms, such as Streptococcus gordonii, to tooth surfaces. Through a variety of synergistic interactions, pioneer organisms facilitate the colonization of later arrivals including Porphyromonas gingivalis, a potential periodontal pathogen. We have investigated genes of S. gordonii required to support a heterotypic biofilm community with P. gingivalis. By screening a plasmid integration library of S. gordonii, genes were identified that are crucial for the accumulation of planktonic P. gingivalis cells into a multispecies biofilm. These genes were further investigated by specific mutation and complementation analyses. The biofilm‐associated genes can be grouped into broad categories based on putative function as follows: (i) intercellular or intracellular signalling (cbe and spxB), (ii) cell wall integrity and maintenance of adhesive proteins (murE, msrA and atf), (iii) extracellular capsule biosynthesis (pgsA and atf), and (iv) physiology (gdhA, ccmA and ntpB). In addition, a gene for a hypothetical protein was identified. Biofilm visualization and quantification by confocal microscopy confirmed the role of these genes in the maturation of the multispecies community, including biofilm architectural development. The results suggest that S. gordonii governs the development of heterotypic oral biofilms through multiple genetic pathways.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2006.05099.x</identifier><identifier>PMID: 16556225</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Bacteria ; Bacterial Adhesion ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteriology ; Biofilms ; Biofilms - growth & development ; Biological and medical sciences ; Cell adhesion & migration ; Ecosystem ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Bacterial ; Genes ; Genetic Complementation Test ; Humans ; Microbiology ; Microscopy, Confocal ; Miscellaneous ; Mutation ; Porphyromonas gingivalis ; Porphyromonas gingivalis - growth & development ; Porphyromonas gingivalis - ultrastructure ; Streptococcus - genetics ; Streptococcus - growth & development ; Streptococcus - metabolism ; Streptococcus - ultrastructure ; Streptococcus gordonii</subject><ispartof>Molecular microbiology, 2006-04, Vol.60 (1), p.121-139</ispartof><rights>2006 INIST-CNRS</rights><rights>Copyright Blackwell Publishing Apr 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5059-1116c53aee66efce764de7f7e3b6187991d4f67515b949a1fddba05dc1a174fe3</citedby><cites>FETCH-LOGICAL-c5059-1116c53aee66efce764de7f7e3b6187991d4f67515b949a1fddba05dc1a174fe3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1365-2958.2006.05099.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-2958.2006.05099.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27903,27904,45553,45554,46388,46812</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=17588887$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16556225$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuboniwa, Masae</creatorcontrib><creatorcontrib>Tribble, Gena D.</creatorcontrib><creatorcontrib>James, Chloe E.</creatorcontrib><creatorcontrib>Kilic, Ali O.</creatorcontrib><creatorcontrib>Tao, Lin</creatorcontrib><creatorcontrib>Herzberg, Mark C.</creatorcontrib><creatorcontrib>Shizukuishi, Satoshi</creatorcontrib><creatorcontrib>Lamont, Richard J.</creatorcontrib><title>Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Dental plaque biofilm formation proceeds through a developmental pathway initiated by the attachment of pioneer organisms, such as Streptococcus gordonii, to tooth surfaces. Through a variety of synergistic interactions, pioneer organisms facilitate the colonization of later arrivals including Porphyromonas gingivalis, a potential periodontal pathogen. We have investigated genes of S. gordonii required to support a heterotypic biofilm community with P. gingivalis. By screening a plasmid integration library of S. gordonii, genes were identified that are crucial for the accumulation of planktonic P. gingivalis cells into a multispecies biofilm. These genes were further investigated by specific mutation and complementation analyses. The biofilm‐associated genes can be grouped into broad categories based on putative function as follows: (i) intercellular or intracellular signalling (cbe and spxB), (ii) cell wall integrity and maintenance of adhesive proteins (murE, msrA and atf), (iii) extracellular capsule biosynthesis (pgsA and atf), and (iv) physiology (gdhA, ccmA and ntpB). In addition, a gene for a hypothetical protein was identified. Biofilm visualization and quantification by confocal microscopy confirmed the role of these genes in the maturation of the multispecies community, including biofilm architectural development. The results suggest that S. gordonii governs the development of heterotypic oral biofilms through multiple genetic pathways.</description><subject>Bacteria</subject><subject>Bacterial Adhesion</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biofilms</subject><subject>Biofilms - growth & development</subject><subject>Biological and medical sciences</subject><subject>Cell adhesion & migration</subject><subject>Ecosystem</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genes</subject><subject>Genetic Complementation Test</subject><subject>Humans</subject><subject>Microbiology</subject><subject>Microscopy, Confocal</subject><subject>Miscellaneous</subject><subject>Mutation</subject><subject>Porphyromonas gingivalis</subject><subject>Porphyromonas gingivalis - growth & development</subject><subject>Porphyromonas gingivalis - ultrastructure</subject><subject>Streptococcus - genetics</subject><subject>Streptococcus - growth & development</subject><subject>Streptococcus - metabolism</subject><subject>Streptococcus - ultrastructure</subject><subject>Streptococcus gordonii</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUGL1DAUx4Mo7rj6FSQIemtN2iZpDh5kWXVhFwUVvIVM8jpmaJMxadaZ_fSmzuCCF32XPMjvveTPDyFMSU1Lvd7WtOWsaiTr64YQXhNGpKz3D9Dqz8VDtCKSkartm29n6ElKW0JoS3j7GJ1RzhhvGrZCd5_nCLs5mGBMTngTog3eOZxnN7o7SDjBLUQ9YuvS7LyZ8QY84CGX1gWf8BxwBBOzm_GnEHffDzFMweuyyvmNu9WjS9j5Qmk8uT1YbMI0Ze_mw1P0aNBjgmen8xx9fXf55eJDdf3x_dXF2-vKMMJkVfJyw1oNwDkMBgTvLIhBQLvmtBdSUtsNXDDK1rKTmg7WrjVh1lBNRTdAe45eHffuYviRIc1qcsnAOGoPISfFheg7QcQ_QSpo35SHCvjiL3AbcvQlhKKSs6Zp-AL1R8jEkFKEQe2im3Q8KErUYlFt1SJLLbLUYlH9tqj2ZfT5aX9eT2DvB0_aCvDyBOhk9DhE7Y1L95xgfakl0Zsj99ONcPjvD6ibm6ula38B7Cm7cg</recordid><startdate>200604</startdate><enddate>200604</enddate><creator>Kuboniwa, Masae</creator><creator>Tribble, Gena D.</creator><creator>James, Chloe E.</creator><creator>Kilic, Ali O.</creator><creator>Tao, Lin</creator><creator>Herzberg, Mark C.</creator><creator>Shizukuishi, Satoshi</creator><creator>Lamont, Richard J.</creator><general>Blackwell Publishing Ltd</general><general>Blackwell Science</general><scope>IQODW</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>200604</creationdate><title>Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community</title><author>Kuboniwa, Masae ; Tribble, Gena D. ; James, Chloe E. ; Kilic, Ali O. ; Tao, Lin ; Herzberg, Mark C. ; Shizukuishi, Satoshi ; Lamont, Richard J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5059-1116c53aee66efce764de7f7e3b6187991d4f67515b949a1fddba05dc1a174fe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Bacteria</topic><topic>Bacterial Adhesion</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Biofilms</topic><topic>Biofilms - growth & development</topic><topic>Biological and medical sciences</topic><topic>Cell adhesion & migration</topic><topic>Ecosystem</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genes</topic><topic>Genetic Complementation Test</topic><topic>Humans</topic><topic>Microbiology</topic><topic>Microscopy, Confocal</topic><topic>Miscellaneous</topic><topic>Mutation</topic><topic>Porphyromonas gingivalis</topic><topic>Porphyromonas gingivalis - growth & development</topic><topic>Porphyromonas gingivalis - ultrastructure</topic><topic>Streptococcus - genetics</topic><topic>Streptococcus - growth & development</topic><topic>Streptococcus - metabolism</topic><topic>Streptococcus - ultrastructure</topic><topic>Streptococcus gordonii</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuboniwa, Masae</creatorcontrib><creatorcontrib>Tribble, Gena D.</creatorcontrib><creatorcontrib>James, Chloe E.</creatorcontrib><creatorcontrib>Kilic, Ali O.</creatorcontrib><creatorcontrib>Tao, Lin</creatorcontrib><creatorcontrib>Herzberg, Mark C.</creatorcontrib><creatorcontrib>Shizukuishi, Satoshi</creatorcontrib><creatorcontrib>Lamont, Richard J.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuboniwa, Masae</au><au>Tribble, Gena D.</au><au>James, Chloe E.</au><au>Kilic, Ali O.</au><au>Tao, Lin</au><au>Herzberg, Mark C.</au><au>Shizukuishi, Satoshi</au><au>Lamont, Richard J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2006-04</date><risdate>2006</risdate><volume>60</volume><issue>1</issue><spage>121</spage><epage>139</epage><pages>121-139</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Dental plaque biofilm formation proceeds through a developmental pathway initiated by the attachment of pioneer organisms, such as Streptococcus gordonii, to tooth surfaces. Through a variety of synergistic interactions, pioneer organisms facilitate the colonization of later arrivals including Porphyromonas gingivalis, a potential periodontal pathogen. We have investigated genes of S. gordonii required to support a heterotypic biofilm community with P. gingivalis. By screening a plasmid integration library of S. gordonii, genes were identified that are crucial for the accumulation of planktonic P. gingivalis cells into a multispecies biofilm. These genes were further investigated by specific mutation and complementation analyses. The biofilm‐associated genes can be grouped into broad categories based on putative function as follows: (i) intercellular or intracellular signalling (cbe and spxB), (ii) cell wall integrity and maintenance of adhesive proteins (murE, msrA and atf), (iii) extracellular capsule biosynthesis (pgsA and atf), and (iv) physiology (gdhA, ccmA and ntpB). In addition, a gene for a hypothetical protein was identified. Biofilm visualization and quantification by confocal microscopy confirmed the role of these genes in the maturation of the multispecies community, including biofilm architectural development. The results suggest that S. gordonii governs the development of heterotypic oral biofilms through multiple genetic pathways.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>16556225</pmid><doi>10.1111/j.1365-2958.2006.05099.x</doi><tpages>19</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Bacterial Adhesion Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Biofilms Biofilms - growth & development Biological and medical sciences Cell adhesion & migration Ecosystem Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Bacterial Genes Genetic Complementation Test Humans Microbiology Microscopy, Confocal Miscellaneous Mutation Porphyromonas gingivalis Porphyromonas gingivalis - growth & development Porphyromonas gingivalis - ultrastructure Streptococcus - genetics Streptococcus - growth & development Streptococcus - metabolism Streptococcus - ultrastructure Streptococcus gordonii |
title | Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community |
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