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Class II contact‐dependent growth inhibition (CDI) systems allow for broad‐range cross‐species toxin delivery within the Enterobacteriaceae family
Summary Contact‐dependent growth inhibition (CDI) allows bacteria to recognize kin cells in mixed bacterial populations. In Escherichia coli, CDI mediated effector delivery has been shown to be species‐specific, with a preference for the own strain over others. This specificity is achieved through a...
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Published in: | Molecular microbiology 2019-04, Vol.111 (4), p.1109-1125 |
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Contact‐dependent growth inhibition (CDI) allows bacteria to recognize kin cells in mixed bacterial populations. In Escherichia coli, CDI mediated effector delivery has been shown to be species‐specific, with a preference for the own strain over others. This specificity is achieved through an interaction between a receptor‐binding domain in the CdiA protein and its cognate receptor protein on the target cell. But how conserved this specificity is has not previously been investigated in detail. Here, we show that class II CdiA receptor‐binding domains and their Enterobacter cloacae analog are highly promiscuous, and can allow for efficient effector delivery into several different Enterobacteriaceae species, including Escherichia, Enterobacter, Klebsiella and Salmonella spp. In addition, although we observe a preference for the own receptors over others for two of the receptor‐binding domains, this did not limit cross‐species effector delivery in all experimental conditions. These results suggest that class II CdiA proteins could allow for broad‐range and cross‐species growth inhibition in mixed bacterial populations.
Contact‐dependent growth inhibition (CDI) has previously been thought to be species‐specific. Here we correct that misconception and show that CDI can be highly promiscuous and allow for cross‐species toxin delivery to a wide range of Enterobacteriaceae. Furthermore, we show that this promiscuous CDI activity is dependent on the environmental context, as we observe a preference for intra‐species CDI interactions in liquid media but not on solid media. |
doi_str_mv | 10.1111/mmi.14214 |
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Contact‐dependent growth inhibition (CDI) allows bacteria to recognize kin cells in mixed bacterial populations. In Escherichia coli, CDI mediated effector delivery has been shown to be species‐specific, with a preference for the own strain over others. This specificity is achieved through an interaction between a receptor‐binding domain in the CdiA protein and its cognate receptor protein on the target cell. But how conserved this specificity is has not previously been investigated in detail. Here, we show that class II CdiA receptor‐binding domains and their Enterobacter cloacae analog are highly promiscuous, and can allow for efficient effector delivery into several different Enterobacteriaceae species, including Escherichia, Enterobacter, Klebsiella and Salmonella spp. In addition, although we observe a preference for the own receptors over others for two of the receptor‐binding domains, this did not limit cross‐species effector delivery in all experimental conditions. These results suggest that class II CdiA proteins could allow for broad‐range and cross‐species growth inhibition in mixed bacterial populations.
Contact‐dependent growth inhibition (CDI) has previously been thought to be species‐specific. Here we correct that misconception and show that CDI can be highly promiscuous and allow for cross‐species toxin delivery to a wide range of Enterobacteriaceae. Furthermore, we show that this promiscuous CDI activity is dependent on the environmental context, as we observe a preference for intra‐species CDI interactions in liquid media but not on solid media.</description><identifier>ISSN: 0950-382X</identifier><identifier>ISSN: 1365-2958</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.14214</identifier><identifier>PMID: 30710431</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Bacteria ; Bacterial Toxins - genetics ; Bacterial Toxins - metabolism ; Binding ; Binding Sites ; Biological Transport ; Contact Inhibition ; E coli ; Enterobacter cloacae ; Enterobacteriaceae ; Enterobacteriaceae - genetics ; Enterobacteriaceae - growth & development ; Enterobacteriaceae - metabolism ; Escherichia coli - genetics ; Escherichia coli - metabolism ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Inhibition ; Klebsiella ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Populations ; Protein Binding ; Proteins ; Receptors ; Salmonella ; Species</subject><ispartof>Molecular microbiology, 2019-04, Vol.111 (4), p.1109-1125</ispartof><rights>2019 The Authors. Published by John Wiley & Sons Ltd</rights><rights>2019 The Authors. Molecular Microbiology Published by John Wiley & Sons Ltd.</rights><rights>Copyright © 2019 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4804-9e2dc3ec26cd1a8e95d8d75de79f59a8b90d99915a3dff2e327de1315fb3be103</citedby><cites>FETCH-LOGICAL-c4804-9e2dc3ec26cd1a8e95d8d75de79f59a8b90d99915a3dff2e327de1315fb3be103</cites><orcidid>0000-0002-3275-0936</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30710431$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-382983$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Virtanen, Petra</creatorcontrib><creatorcontrib>Wäneskog, Marcus</creatorcontrib><creatorcontrib>Koskiniemi, Sanna</creatorcontrib><title>Class II contact‐dependent growth inhibition (CDI) systems allow for broad‐range cross‐species toxin delivery within the Enterobacteriaceae family</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Contact‐dependent growth inhibition (CDI) allows bacteria to recognize kin cells in mixed bacterial populations. In Escherichia coli, CDI mediated effector delivery has been shown to be species‐specific, with a preference for the own strain over others. This specificity is achieved through an interaction between a receptor‐binding domain in the CdiA protein and its cognate receptor protein on the target cell. But how conserved this specificity is has not previously been investigated in detail. Here, we show that class II CdiA receptor‐binding domains and their Enterobacter cloacae analog are highly promiscuous, and can allow for efficient effector delivery into several different Enterobacteriaceae species, including Escherichia, Enterobacter, Klebsiella and Salmonella spp. In addition, although we observe a preference for the own receptors over others for two of the receptor‐binding domains, this did not limit cross‐species effector delivery in all experimental conditions. These results suggest that class II CdiA proteins could allow for broad‐range and cross‐species growth inhibition in mixed bacterial populations.
Contact‐dependent growth inhibition (CDI) has previously been thought to be species‐specific. Here we correct that misconception and show that CDI can be highly promiscuous and allow for cross‐species toxin delivery to a wide range of Enterobacteriaceae. Furthermore, we show that this promiscuous CDI activity is dependent on the environmental context, as we observe a preference for intra‐species CDI interactions in liquid media but not on solid media.</description><subject>Bacteria</subject><subject>Bacterial Toxins - genetics</subject><subject>Bacterial Toxins - metabolism</subject><subject>Binding</subject><subject>Binding Sites</subject><subject>Biological Transport</subject><subject>Contact Inhibition</subject><subject>E coli</subject><subject>Enterobacter cloacae</subject><subject>Enterobacteriaceae</subject><subject>Enterobacteriaceae - genetics</subject><subject>Enterobacteriaceae - growth & development</subject><subject>Enterobacteriaceae - metabolism</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - metabolism</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Inhibition</subject><subject>Klebsiella</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Populations</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>Receptors</subject><subject>Salmonella</subject><subject>Species</subject><issn>0950-382X</issn><issn>1365-2958</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1ksFu1DAQhiMEokvhwAsgS1xaibR2HCfxBanaFhqpFRdA3CzHnuy6SuzFdhr2xiNw5Pl4EtxuqSgScxmN_M3v0a8_y14SfERSHY-jOSJlQcpH2YLQiuUFZ83jbIE5wzltii972bMQrjAmFFf0abZHcU1wScki-7kcZAiobZFyNkoVf33_oWEDVoONaOXdHNfI2LXpTDTOooPlaXuIwjZEGAOSw-Bm1DuPOu-kTrte2hUg5V0IaQobUAYCiu6bsUjDYK7Bb9Fs4jrNcQ3ozEbwrksfgzdSgQTUy9EM2-fZk14OAV7c9f3s07uzj8vz_OLD-3Z5cpGrssFlzqHQioIqKqWJbIAz3eiaaah5z7hsOo4155wwSXXfF0CLWgOhhPUd7YBgup-92emGGTZTJzbejNJvhZNGnJrPJ8L5lZgmkWzkDU342x2e2BG0Si55OTzYevhizVqs3LWoGoYJr5LAwZ2Ad18nCFGMJigYBmnBTUEUpOasbGpaJvT1P-iVm7xNboiiwKypcMXrRB3uqFvTPfT3xxAsbuIhUjzEbTwS--rv6-_JP3lIwPEOmM0A2_8ricvLdif5GyZZy4k</recordid><startdate>201904</startdate><enddate>201904</enddate><creator>Virtanen, Petra</creator><creator>Wäneskog, Marcus</creator><creator>Koskiniemi, Sanna</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</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><scope>5PM</scope><scope>ACNBI</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>DF2</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0002-3275-0936</orcidid></search><sort><creationdate>201904</creationdate><title>Class II contact‐dependent growth inhibition (CDI) systems allow for broad‐range cross‐species toxin delivery within the Enterobacteriaceae family</title><author>Virtanen, Petra ; Wäneskog, Marcus ; Koskiniemi, Sanna</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4804-9e2dc3ec26cd1a8e95d8d75de79f59a8b90d99915a3dff2e327de1315fb3be103</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Bacteria</topic><topic>Bacterial Toxins - genetics</topic><topic>Bacterial Toxins - metabolism</topic><topic>Binding</topic><topic>Binding Sites</topic><topic>Biological Transport</topic><topic>Contact Inhibition</topic><topic>E coli</topic><topic>Enterobacter cloacae</topic><topic>Enterobacteriaceae</topic><topic>Enterobacteriaceae - genetics</topic><topic>Enterobacteriaceae - growth & development</topic><topic>Enterobacteriaceae - metabolism</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - metabolism</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Inhibition</topic><topic>Klebsiella</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - metabolism</topic><topic>Populations</topic><topic>Protein Binding</topic><topic>Proteins</topic><topic>Receptors</topic><topic>Salmonella</topic><topic>Species</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Virtanen, Petra</creatorcontrib><creatorcontrib>Wäneskog, Marcus</creatorcontrib><creatorcontrib>Koskiniemi, Sanna</creatorcontrib><collection>Wiley Online Library 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>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><collection>PubMed Central (Full Participant titles)</collection><collection>SWEPUB Uppsala universitet full text</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SWEPUB Uppsala universitet</collection><collection>SwePub Articles full text</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Virtanen, Petra</au><au>Wäneskog, Marcus</au><au>Koskiniemi, Sanna</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Class II contact‐dependent growth inhibition (CDI) systems allow for broad‐range cross‐species toxin delivery within the Enterobacteriaceae family</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2019-04</date><risdate>2019</risdate><volume>111</volume><issue>4</issue><spage>1109</spage><epage>1125</epage><pages>1109-1125</pages><issn>0950-382X</issn><issn>1365-2958</issn><eissn>1365-2958</eissn><abstract>Summary
Contact‐dependent growth inhibition (CDI) allows bacteria to recognize kin cells in mixed bacterial populations. In Escherichia coli, CDI mediated effector delivery has been shown to be species‐specific, with a preference for the own strain over others. This specificity is achieved through an interaction between a receptor‐binding domain in the CdiA protein and its cognate receptor protein on the target cell. But how conserved this specificity is has not previously been investigated in detail. Here, we show that class II CdiA receptor‐binding domains and their Enterobacter cloacae analog are highly promiscuous, and can allow for efficient effector delivery into several different Enterobacteriaceae species, including Escherichia, Enterobacter, Klebsiella and Salmonella spp. In addition, although we observe a preference for the own receptors over others for two of the receptor‐binding domains, this did not limit cross‐species effector delivery in all experimental conditions. These results suggest that class II CdiA proteins could allow for broad‐range and cross‐species growth inhibition in mixed bacterial populations.
Contact‐dependent growth inhibition (CDI) has previously been thought to be species‐specific. Here we correct that misconception and show that CDI can be highly promiscuous and allow for cross‐species toxin delivery to a wide range of Enterobacteriaceae. Furthermore, we show that this promiscuous CDI activity is dependent on the environmental context, as we observe a preference for intra‐species CDI interactions in liquid media but not on solid media.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>30710431</pmid><doi>10.1111/mmi.14214</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-3275-0936</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Bacterial Toxins - genetics Bacterial Toxins - metabolism Binding Binding Sites Biological Transport Contact Inhibition E coli Enterobacter cloacae Enterobacteriaceae Enterobacteriaceae - genetics Enterobacteriaceae - growth & development Enterobacteriaceae - metabolism Escherichia coli - genetics Escherichia coli - metabolism Escherichia coli Proteins - genetics Escherichia coli Proteins - metabolism Inhibition Klebsiella Membrane Proteins - genetics Membrane Proteins - metabolism Populations Protein Binding Proteins Receptors Salmonella Species |
title | Class II contact‐dependent growth inhibition (CDI) systems allow for broad‐range cross‐species toxin delivery within the Enterobacteriaceae family |
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