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A Combinatorial Kin Discrimination System in Bacillus subtilis
Multicellularity inherently involves a number of cooperative behaviors that are potentially susceptible to exploitation but can be protected by mechanisms such as kin discrimination. Discrimination of kin from non-kin has been observed in swarms of the bacterium Bacillus subtilis, but the underlying...
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Published in: | Current biology 2016-03, Vol.26 (6), p.733-742 |
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description | Multicellularity inherently involves a number of cooperative behaviors that are potentially susceptible to exploitation but can be protected by mechanisms such as kin discrimination. Discrimination of kin from non-kin has been observed in swarms of the bacterium Bacillus subtilis, but the underlying molecular mechanism has been unknown. We used genetic, transcriptomic, and bioinformatic analyses to uncover kin recognition factors in this organism. Our results identified many molecules involved in cell-surface modification and antimicrobial production and response. These genes varied significantly in expression level and mutation phenotype among B. subtilis strains, suggesting interstrain variation in the exact kin discrimination mechanism used. Genome analyses revealed a substantial diversity of antimicrobial genes present in unique combinations in different strains, with many likely acquired by horizontal gene transfer. The dynamic combinatorial effect derived from this plethora of kin discrimination genes creates a tight relatedness cutoff for cooperation that has likely led to rapid diversification within the species. Our data suggest that genes likely originally selected for competitive purposes also generate preferential interactions among kin, thus stabilizing multicellular lifestyles.
[Display omitted]
•Kin discrimination (KD) in B. subtilis leads to cell death and stress response•Various genes are used for KD, generally antimicrobials and cell-surface modifiers•Transcription of KD genes varies extensively, especially when encountering non-kin•KD genes are poorly conserved, often absent even in the most closely related strains
Lyons et al. show that B. subtilis cells use a collection of intercellular attack and defense molecules to discriminate kin from non-kin—only those cells that contain the right set of immunities will survive and be treated as kin. These kin discrimination genes are numerous and vary greatly between strains in both conservation and expression levels. |
doi_str_mv | 10.1016/j.cub.2016.01.032 |
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[Display omitted]
•Kin discrimination (KD) in B. subtilis leads to cell death and stress response•Various genes are used for KD, generally antimicrobials and cell-surface modifiers•Transcription of KD genes varies extensively, especially when encountering non-kin•KD genes are poorly conserved, often absent even in the most closely related strains
Lyons et al. show that B. subtilis cells use a collection of intercellular attack and defense molecules to discriminate kin from non-kin—only those cells that contain the right set of immunities will survive and be treated as kin. These kin discrimination genes are numerous and vary greatly between strains in both conservation and expression levels.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2016.01.032</identifier><identifier>PMID: 26923784</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Adenosine Triphosphatases - genetics ; Antigens, Bacterial - genetics ; ATP-Binding Cassette Transporters - genetics ; Bacillus subtilis - genetics ; Bacillus subtilis - physiology ; Bacterial Physiological Phenomena ; Bacterial Proteins - genetics ; DNA Transposable Elements ; Gene Expression Regulation, Bacterial ; Gene Transfer, Horizontal ; Genome, Bacterial ; Microbial Interactions ; Mutation ; Phenotype ; Sigma Factor - genetics</subject><ispartof>Current biology, 2016-03, Vol.26 (6), p.733-742</ispartof><rights>2016 Elsevier Ltd</rights><rights>Copyright © 2016 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c517t-d9d9072edf92ed63236d0bb046ddbf2b2585fa8e72bca9621e009f895c14fc123</citedby><cites>FETCH-LOGICAL-c517t-d9d9072edf92ed63236d0bb046ddbf2b2585fa8e72bca9621e009f895c14fc123</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26923784$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lyons, Nicholas A.</creatorcontrib><creatorcontrib>Kraigher, Barbara</creatorcontrib><creatorcontrib>Stefanic, Polonca</creatorcontrib><creatorcontrib>Mandic-Mulec, Ines</creatorcontrib><creatorcontrib>Kolter, Roberto</creatorcontrib><title>A Combinatorial Kin Discrimination System in Bacillus subtilis</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>Multicellularity inherently involves a number of cooperative behaviors that are potentially susceptible to exploitation but can be protected by mechanisms such as kin discrimination. Discrimination of kin from non-kin has been observed in swarms of the bacterium Bacillus subtilis, but the underlying molecular mechanism has been unknown. We used genetic, transcriptomic, and bioinformatic analyses to uncover kin recognition factors in this organism. Our results identified many molecules involved in cell-surface modification and antimicrobial production and response. These genes varied significantly in expression level and mutation phenotype among B. subtilis strains, suggesting interstrain variation in the exact kin discrimination mechanism used. Genome analyses revealed a substantial diversity of antimicrobial genes present in unique combinations in different strains, with many likely acquired by horizontal gene transfer. The dynamic combinatorial effect derived from this plethora of kin discrimination genes creates a tight relatedness cutoff for cooperation that has likely led to rapid diversification within the species. Our data suggest that genes likely originally selected for competitive purposes also generate preferential interactions among kin, thus stabilizing multicellular lifestyles.
[Display omitted]
•Kin discrimination (KD) in B. subtilis leads to cell death and stress response•Various genes are used for KD, generally antimicrobials and cell-surface modifiers•Transcription of KD genes varies extensively, especially when encountering non-kin•KD genes are poorly conserved, often absent even in the most closely related strains
Lyons et al. show that B. subtilis cells use a collection of intercellular attack and defense molecules to discriminate kin from non-kin—only those cells that contain the right set of immunities will survive and be treated as kin. These kin discrimination genes are numerous and vary greatly between strains in both conservation and expression levels.</description><subject>Adenosine Triphosphatases - genetics</subject><subject>Antigens, Bacterial - genetics</subject><subject>ATP-Binding Cassette Transporters - genetics</subject><subject>Bacillus subtilis - genetics</subject><subject>Bacillus subtilis - physiology</subject><subject>Bacterial Physiological Phenomena</subject><subject>Bacterial Proteins - genetics</subject><subject>DNA Transposable Elements</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gene Transfer, Horizontal</subject><subject>Genome, Bacterial</subject><subject>Microbial Interactions</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Sigma Factor - genetics</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNp9kEtLxDAUhYMozvj4AW6kSzetN2mbNggD4_hEwYW6DnlVM7TNmLSC_94Mo6IbN0m459xzbz6EjjBkGDA9XWZqlBmJzwxwBjnZQlNcVyyFoii30RQYhZTVhEzQXghLAExqRnfRhFBG8qoupmg2Txauk7YXg_NWtMmd7ZMLG5S33bpoXZ88foTBdEkUzoWybTuGJIxysK0NB2inEW0wh1_3Pnq-unxa3KT3D9e3i_l9qkpcDalmmkFFjG5YPGhOcqpBSiio1rIhkpR12YjaVEQqwSjBBoA1NSsVLhqFSb6PZpvc1Sg7o5XpBy9avopbCv_BnbD8r9LbV_7i3nlRQ06BxoCTrwDv3kYTBt7FT5q2Fb1xY-C4qkqal6QqoxVvrMq7ELxpfsZg4GvufMkjd77mzgHzyD32HP_e76fjG3Q0nG0MJlJ6t8bzoKzpldHWGzVw7ew_8Z9S3JRU</recordid><startdate>20160321</startdate><enddate>20160321</enddate><creator>Lyons, Nicholas A.</creator><creator>Kraigher, Barbara</creator><creator>Stefanic, Polonca</creator><creator>Mandic-Mulec, Ines</creator><creator>Kolter, Roberto</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</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>20160321</creationdate><title>A Combinatorial Kin Discrimination System in Bacillus subtilis</title><author>Lyons, Nicholas A. ; Kraigher, Barbara ; Stefanic, Polonca ; Mandic-Mulec, Ines ; Kolter, Roberto</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c517t-d9d9072edf92ed63236d0bb046ddbf2b2585fa8e72bca9621e009f895c14fc123</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adenosine Triphosphatases - genetics</topic><topic>Antigens, Bacterial - genetics</topic><topic>ATP-Binding Cassette Transporters - genetics</topic><topic>Bacillus subtilis - genetics</topic><topic>Bacillus subtilis - physiology</topic><topic>Bacterial Physiological Phenomena</topic><topic>Bacterial Proteins - genetics</topic><topic>DNA Transposable Elements</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Gene Transfer, Horizontal</topic><topic>Genome, Bacterial</topic><topic>Microbial Interactions</topic><topic>Mutation</topic><topic>Phenotype</topic><topic>Sigma Factor - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lyons, Nicholas A.</creatorcontrib><creatorcontrib>Kraigher, Barbara</creatorcontrib><creatorcontrib>Stefanic, Polonca</creatorcontrib><creatorcontrib>Mandic-Mulec, Ines</creatorcontrib><creatorcontrib>Kolter, Roberto</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lyons, Nicholas A.</au><au>Kraigher, Barbara</au><au>Stefanic, Polonca</au><au>Mandic-Mulec, Ines</au><au>Kolter, Roberto</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Combinatorial Kin Discrimination System in Bacillus subtilis</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2016-03-21</date><risdate>2016</risdate><volume>26</volume><issue>6</issue><spage>733</spage><epage>742</epage><pages>733-742</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>Multicellularity inherently involves a number of cooperative behaviors that are potentially susceptible to exploitation but can be protected by mechanisms such as kin discrimination. Discrimination of kin from non-kin has been observed in swarms of the bacterium Bacillus subtilis, but the underlying molecular mechanism has been unknown. We used genetic, transcriptomic, and bioinformatic analyses to uncover kin recognition factors in this organism. Our results identified many molecules involved in cell-surface modification and antimicrobial production and response. These genes varied significantly in expression level and mutation phenotype among B. subtilis strains, suggesting interstrain variation in the exact kin discrimination mechanism used. Genome analyses revealed a substantial diversity of antimicrobial genes present in unique combinations in different strains, with many likely acquired by horizontal gene transfer. The dynamic combinatorial effect derived from this plethora of kin discrimination genes creates a tight relatedness cutoff for cooperation that has likely led to rapid diversification within the species. Our data suggest that genes likely originally selected for competitive purposes also generate preferential interactions among kin, thus stabilizing multicellular lifestyles.
[Display omitted]
•Kin discrimination (KD) in B. subtilis leads to cell death and stress response•Various genes are used for KD, generally antimicrobials and cell-surface modifiers•Transcription of KD genes varies extensively, especially when encountering non-kin•KD genes are poorly conserved, often absent even in the most closely related strains
Lyons et al. show that B. subtilis cells use a collection of intercellular attack and defense molecules to discriminate kin from non-kin—only those cells that contain the right set of immunities will survive and be treated as kin. These kin discrimination genes are numerous and vary greatly between strains in both conservation and expression levels.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>26923784</pmid><doi>10.1016/j.cub.2016.01.032</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adenosine Triphosphatases - genetics Antigens, Bacterial - genetics ATP-Binding Cassette Transporters - genetics Bacillus subtilis - genetics Bacillus subtilis - physiology Bacterial Physiological Phenomena Bacterial Proteins - genetics DNA Transposable Elements Gene Expression Regulation, Bacterial Gene Transfer, Horizontal Genome, Bacterial Microbial Interactions Mutation Phenotype Sigma Factor - genetics |
title | A Combinatorial Kin Discrimination System in Bacillus subtilis |
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