Klebsiella oxytoca causes colonization resistance against multidrug-resistant K. pneumoniae in the gut via cooperative carbohydrate competition
Gut colonization with multidrug-resistant (MDR) bacteria enhances the risk of bloodstream infections in susceptible individuals. We demonstrate highly variable degrees of ex vivo colonization resistance against a carbapenem-resistant Klebsiella pneumoniae strain in human feces samples and subsequent...
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| Veröffentlicht in: | Cell host & microbe 2021-11, Vol.29 (11), p.1663-1679.e7 |
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| creator | Osbelt, Lisa Wende, Marie Almási, Éva Derksen, Elisabeth Muthukumarasamy, Uthayakumar Lesker, Till R. Galvez, Eric J.C. Pils, Marina C. Schalk, Enrico Chhatwal, Patrick Färber, Jacqueline Neumann-Schaal, Meina Fischer, Thomas Schlüter, Dirk Strowig, Till |
| description | Gut colonization with multidrug-resistant (MDR) bacteria enhances the risk of bloodstream infections in susceptible individuals. We demonstrate highly variable degrees of ex vivo colonization resistance against a carbapenem-resistant Klebsiella pneumoniae strain in human feces samples and subsequently isolate diverse K. oxytoca strains from protected donors. Several of these K. oxytoca strains reduce gut colonization of MDR K. pneumoniae strains in antibiotic-treated and gnotobiotic mouse models. Comparative analysis of K. oxytoca strains coupled with CRISPR-Cas9-mediated deletion of casA, a protein essential for utilization of selected beta-glucosides, identified competition for specific carbohydrates as key in promoting colonization resistance. In addition to direct competition between K. oxytoca and K. pneumoniae, cooperation with additional commensals is required to reestablish full colonization resistance and gut decolonization. Finally, humanized microbiota mice generated from K. pneumoniae-susceptible donors are protected by K. oxytoca administration, demonstrating the potential of commensal K. oxytoca strains as next-generation probiotics.
[Display omitted]
•Ex vivo colonization resistance against K. pneumoniae is variable between individuals•Diverse commensal Klebsiella oxytoca strains are isolated from protected individuals•K. oxytoca establishes colonization resistance against of K. pneumoniae in vivo•Cooperation with commensal bacteria restricts nutrient availability in the gut
Gut colonization with multidrug-resistant enterobacteria increases risk of bloodstream infections. Osbelt et al. characterize the ability of human stools to inhibit growth of multidrug-resistant Klebsiella pneumoniae. Commensal Klebsiella oxytoca strains were identified in protected human donors, which in cooperation with other commensals outcompete K. pneumoniae through beta-glucoside utilization in mice. |
| doi_str_mv | 10.1016/j.chom.2021.09.003 |
| format | Article |
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[Display omitted]
•Ex vivo colonization resistance against K. pneumoniae is variable between individuals•Diverse commensal Klebsiella oxytoca strains are isolated from protected individuals•K. oxytoca establishes colonization resistance against of K. pneumoniae in vivo•Cooperation with commensal bacteria restricts nutrient availability in the gut
Gut colonization with multidrug-resistant enterobacteria increases risk of bloodstream infections. Osbelt et al. characterize the ability of human stools to inhibit growth of multidrug-resistant Klebsiella pneumoniae. Commensal Klebsiella oxytoca strains were identified in protected human donors, which in cooperation with other commensals outcompete K. pneumoniae through beta-glucoside utilization in mice.</description><identifier>ISSN: 1931-3128</identifier><identifier>EISSN: 1934-6069</identifier><identifier>DOI: 10.1016/j.chom.2021.09.003</identifier><identifier>PMID: 34610293</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>16S rRNA gene sequencing ; Adaptive Immunity ; Adult ; Animals ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; beta-glucosides ; Carbohydrate Metabolism ; Child ; colonization resistance ; Drug Resistance, Multiple, Bacterial ; enteric infections ; Feces - microbiology ; Gastrointestinal Microbiome ; Gastrointestinal Tract - microbiology ; Germ-Free Life ; Glucosides - metabolism ; humanized mouse models ; Humans ; intestinal microbiota ; Klebsiella Infections - immunology ; Klebsiella Infections - microbiology ; Klebsiella oxytoca ; Klebsiella oxytoca - genetics ; Klebsiella oxytoca - isolation & purification ; Klebsiella oxytoca - physiology ; Klebsiella pneumoniae ; Klebsiella pneumoniae - drug effects ; Klebsiella pneumoniae - growth & development ; Mice ; Mice, Inbred C57BL ; Microbial Interactions ; multidrug-resistant bacteria ; probiotics</subject><ispartof>Cell host & microbe, 2021-11, Vol.29 (11), p.1663-1679.e7</ispartof><rights>2021 Elsevier Inc.</rights><rights>Copyright © 2021 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c400t-9ddfcf7f842b0682934c8ae9520a17a7a0a2086e240f3c5d2db8d6ce147397923</citedby><cites>FETCH-LOGICAL-c400t-9ddfcf7f842b0682934c8ae9520a17a7a0a2086e240f3c5d2db8d6ce147397923</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1931312821004194$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34610293$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Osbelt, Lisa</creatorcontrib><creatorcontrib>Wende, Marie</creatorcontrib><creatorcontrib>Almási, Éva</creatorcontrib><creatorcontrib>Derksen, Elisabeth</creatorcontrib><creatorcontrib>Muthukumarasamy, Uthayakumar</creatorcontrib><creatorcontrib>Lesker, Till R.</creatorcontrib><creatorcontrib>Galvez, Eric J.C.</creatorcontrib><creatorcontrib>Pils, Marina C.</creatorcontrib><creatorcontrib>Schalk, Enrico</creatorcontrib><creatorcontrib>Chhatwal, Patrick</creatorcontrib><creatorcontrib>Färber, Jacqueline</creatorcontrib><creatorcontrib>Neumann-Schaal, Meina</creatorcontrib><creatorcontrib>Fischer, Thomas</creatorcontrib><creatorcontrib>Schlüter, Dirk</creatorcontrib><creatorcontrib>Strowig, Till</creatorcontrib><title>Klebsiella oxytoca causes colonization resistance against multidrug-resistant K. pneumoniae in the gut via cooperative carbohydrate competition</title><title>Cell host & microbe</title><addtitle>Cell Host Microbe</addtitle><description>Gut colonization with multidrug-resistant (MDR) bacteria enhances the risk of bloodstream infections in susceptible individuals. We demonstrate highly variable degrees of ex vivo colonization resistance against a carbapenem-resistant Klebsiella pneumoniae strain in human feces samples and subsequently isolate diverse K. oxytoca strains from protected donors. Several of these K. oxytoca strains reduce gut colonization of MDR K. pneumoniae strains in antibiotic-treated and gnotobiotic mouse models. Comparative analysis of K. oxytoca strains coupled with CRISPR-Cas9-mediated deletion of casA, a protein essential for utilization of selected beta-glucosides, identified competition for specific carbohydrates as key in promoting colonization resistance. In addition to direct competition between K. oxytoca and K. pneumoniae, cooperation with additional commensals is required to reestablish full colonization resistance and gut decolonization. Finally, humanized microbiota mice generated from K. pneumoniae-susceptible donors are protected by K. oxytoca administration, demonstrating the potential of commensal K. oxytoca strains as next-generation probiotics.
[Display omitted]
•Ex vivo colonization resistance against K. pneumoniae is variable between individuals•Diverse commensal Klebsiella oxytoca strains are isolated from protected individuals•K. oxytoca establishes colonization resistance against of K. pneumoniae in vivo•Cooperation with commensal bacteria restricts nutrient availability in the gut
Gut colonization with multidrug-resistant enterobacteria increases risk of bloodstream infections. Osbelt et al. characterize the ability of human stools to inhibit growth of multidrug-resistant Klebsiella pneumoniae. Commensal Klebsiella oxytoca strains were identified in protected human donors, which in cooperation with other commensals outcompete K. pneumoniae through beta-glucoside utilization in mice.</description><subject>16S rRNA gene sequencing</subject><subject>Adaptive Immunity</subject><subject>Adult</subject><subject>Animals</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>beta-glucosides</subject><subject>Carbohydrate Metabolism</subject><subject>Child</subject><subject>colonization resistance</subject><subject>Drug Resistance, Multiple, Bacterial</subject><subject>enteric infections</subject><subject>Feces - microbiology</subject><subject>Gastrointestinal Microbiome</subject><subject>Gastrointestinal Tract - microbiology</subject><subject>Germ-Free Life</subject><subject>Glucosides - metabolism</subject><subject>humanized mouse models</subject><subject>Humans</subject><subject>intestinal microbiota</subject><subject>Klebsiella Infections - immunology</subject><subject>Klebsiella Infections - microbiology</subject><subject>Klebsiella oxytoca</subject><subject>Klebsiella oxytoca - genetics</subject><subject>Klebsiella oxytoca - isolation & purification</subject><subject>Klebsiella oxytoca - physiology</subject><subject>Klebsiella pneumoniae</subject><subject>Klebsiella pneumoniae - drug effects</subject><subject>Klebsiella pneumoniae - growth & development</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Microbial Interactions</subject><subject>multidrug-resistant bacteria</subject><subject>probiotics</subject><issn>1931-3128</issn><issn>1934-6069</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9Ubtu3DAQJAIHsWPnB1IELN1IWVJPAm4Mw3nABtIkNUGRqzseJFEhqYPPX5FPyLfky0L57JSpdhc7M4udIeQ9g5wBqz_ucr11Y86BsxxEDlC8ImdMFGVWQy1OnnqWFYy3p-RtCDuAqoKGvSGnRVkz4KI4I7_uBuyCxWFQ1D0cotOKarUEDFS7wU32UUXrJuox2BDVpJGqjbJTiHRchmiNXzbZyzLSu_zP73nCZUxMhdRONG6RbpZI9zYJOzejT4J7TEd857YHk8Y0uHHGaNdLF-R1r4aA757rOfnx6fb7zZfs_tvnrzfX95kuAWImjOl13_RtyTuo2_RLqVuFouKgWKMaBYpDWyMvoS90ZbjpWlNrZGVTiEbw4pxcHnVn734uGKIcbdCrDxO6JUheNaLmbVWxBOVHqPYuBI-9nL0dlT9IBnJNQu7kmoRck5AgZEoikT486y_diOYf5cX6BLg6AjB9ubfoZdAWk8HGetRRGmf_p_8XHNGfBA</recordid><startdate>20211110</startdate><enddate>20211110</enddate><creator>Osbelt, Lisa</creator><creator>Wende, Marie</creator><creator>Almási, Éva</creator><creator>Derksen, Elisabeth</creator><creator>Muthukumarasamy, Uthayakumar</creator><creator>Lesker, Till R.</creator><creator>Galvez, Eric J.C.</creator><creator>Pils, Marina C.</creator><creator>Schalk, Enrico</creator><creator>Chhatwal, Patrick</creator><creator>Färber, Jacqueline</creator><creator>Neumann-Schaal, Meina</creator><creator>Fischer, Thomas</creator><creator>Schlüter, Dirk</creator><creator>Strowig, Till</creator><general>Elsevier Inc</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>7X8</scope></search><sort><creationdate>20211110</creationdate><title>Klebsiella oxytoca causes colonization resistance against multidrug-resistant K. pneumoniae in the gut via cooperative carbohydrate competition</title><author>Osbelt, Lisa ; 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We demonstrate highly variable degrees of ex vivo colonization resistance against a carbapenem-resistant Klebsiella pneumoniae strain in human feces samples and subsequently isolate diverse K. oxytoca strains from protected donors. Several of these K. oxytoca strains reduce gut colonization of MDR K. pneumoniae strains in antibiotic-treated and gnotobiotic mouse models. Comparative analysis of K. oxytoca strains coupled with CRISPR-Cas9-mediated deletion of casA, a protein essential for utilization of selected beta-glucosides, identified competition for specific carbohydrates as key in promoting colonization resistance. In addition to direct competition between K. oxytoca and K. pneumoniae, cooperation with additional commensals is required to reestablish full colonization resistance and gut decolonization. Finally, humanized microbiota mice generated from K. pneumoniae-susceptible donors are protected by K. oxytoca administration, demonstrating the potential of commensal K. oxytoca strains as next-generation probiotics.
[Display omitted]
•Ex vivo colonization resistance against K. pneumoniae is variable between individuals•Diverse commensal Klebsiella oxytoca strains are isolated from protected individuals•K. oxytoca establishes colonization resistance against of K. pneumoniae in vivo•Cooperation with commensal bacteria restricts nutrient availability in the gut
Gut colonization with multidrug-resistant enterobacteria increases risk of bloodstream infections. Osbelt et al. characterize the ability of human stools to inhibit growth of multidrug-resistant Klebsiella pneumoniae. Commensal Klebsiella oxytoca strains were identified in protected human donors, which in cooperation with other commensals outcompete K. pneumoniae through beta-glucoside utilization in mice.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34610293</pmid><doi>10.1016/j.chom.2021.09.003</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
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| ispartof | Cell host & microbe, 2021-11, Vol.29 (11), p.1663-1679.e7 |
| issn | 1931-3128 1934-6069 |
| language | eng |
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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; EZB-FREE-00999 freely available EZB journals |
| subjects | 16S rRNA gene sequencing Adaptive Immunity Adult Animals Bacterial Proteins - genetics Bacterial Proteins - metabolism beta-glucosides Carbohydrate Metabolism Child colonization resistance Drug Resistance, Multiple, Bacterial enteric infections Feces - microbiology Gastrointestinal Microbiome Gastrointestinal Tract - microbiology Germ-Free Life Glucosides - metabolism humanized mouse models Humans intestinal microbiota Klebsiella Infections - immunology Klebsiella Infections - microbiology Klebsiella oxytoca Klebsiella oxytoca - genetics Klebsiella oxytoca - isolation & purification Klebsiella oxytoca - physiology Klebsiella pneumoniae Klebsiella pneumoniae - drug effects Klebsiella pneumoniae - growth & development Mice Mice, Inbred C57BL Microbial Interactions multidrug-resistant bacteria probiotics |
| title | Klebsiella oxytoca causes colonization resistance against multidrug-resistant K. pneumoniae in the gut via cooperative carbohydrate competition |
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