Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23
Lactobacillus reuteri strain 100-23 together with a Lactobacillus -free mouse model, provides a system with which the molecular traits underpinning bacterial commensalism in vertebrates can be studied. A polysaccharide was extracted from sucrose-containing liquid cultures of strain 100-23. Chemical...
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creator | Sims, Ian M Frese, Steven A Walter, Jens Loach, Diane Wilson, Michelle Appleyard, Kay Eason, Jocelyn Livingston, Megan Baird, Margaret Cook, Gregory Tannock, Gerald W |
description | Lactobacillus reuteri
strain 100-23 together with a
Lactobacillus
-free mouse model, provides a system with which the molecular traits underpinning bacterial commensalism in vertebrates can be studied. A polysaccharide was extracted from sucrose-containing liquid cultures of strain 100-23. Chemical analysis showed that this exopolysaccharide was a levan (β-2, 6-linked fructan). Mutation of the fructosyl transferase (
ftf
) gene resulted in loss of exopolysaccharide production. The
ftf
mutant was able to colonise the murine gastrointestinal tract in the absence of competition, but colonisation was impaired in competition with the wild type. Biofilm formation by the mutant on the forestomach epithelial surface was not impaired and the matrix between cells was indistinguishable from that of the wild type in electron micrographs. Colonisation of the mouse gut by the wild-type strain led to increased proportions of regulatory T cells (Foxp3+) in the spleen, whereas colonisation by the
ftf
mutant did not. Survival of the mutant in sucrose-containing medium was markedly reduced relative to the wild type. Comparison of the genomic
ftf
loci of strain 100-23 with other
L. reuteri
strains suggested that the
ftf
gene was acquired by lateral gene transfer early in the evolution of the species and subsequently diversified at accelerated rates. Levan production by
L. reuteri
100-23 may represent a function acquired by the bacterial species for life in moderate to high-sucrose extra-gastrointestinal environments that has subsequently been diverted to novel uses, including immunomodulation, that aid in colonisation of the murine gut. |
doi_str_mv | 10.1038/ismej.2010.201 |
format | Article |
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strain 100-23 together with a
Lactobacillus
-free mouse model, provides a system with which the molecular traits underpinning bacterial commensalism in vertebrates can be studied. A polysaccharide was extracted from sucrose-containing liquid cultures of strain 100-23. Chemical analysis showed that this exopolysaccharide was a levan (β-2, 6-linked fructan). Mutation of the fructosyl transferase (
ftf
) gene resulted in loss of exopolysaccharide production. The
ftf
mutant was able to colonise the murine gastrointestinal tract in the absence of competition, but colonisation was impaired in competition with the wild type. Biofilm formation by the mutant on the forestomach epithelial surface was not impaired and the matrix between cells was indistinguishable from that of the wild type in electron micrographs. Colonisation of the mouse gut by the wild-type strain led to increased proportions of regulatory T cells (Foxp3+) in the spleen, whereas colonisation by the
ftf
mutant did not. Survival of the mutant in sucrose-containing medium was markedly reduced relative to the wild type. Comparison of the genomic
ftf
loci of strain 100-23 with other
L. reuteri
strains suggested that the
ftf
gene was acquired by lateral gene transfer early in the evolution of the species and subsequently diversified at accelerated rates. Levan production by
L. reuteri
100-23 may represent a function acquired by the bacterial species for life in moderate to high-sucrose extra-gastrointestinal environments that has subsequently been diverted to novel uses, including immunomodulation, that aid in colonisation of the murine gut.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/ismej.2010.201</identifier><identifier>PMID: 21248858</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/250/2152/569 ; 631/326/2565/855 ; 631/45/72/1205 ; 692/698/2741/2135 ; Animals ; Biofilms ; Biomedical and Life Sciences ; Chemical analysis ; Colonization ; Commensalism ; Competition ; Culture Media ; Ecology ; Evolutionary Biology ; Fructans - biosynthesis ; Fructans - chemistry ; Gastrointestinal Contents - microbiology ; Gastrointestinal tract ; Genes, Bacterial ; Hexosyltransferases - genetics ; Lactobacillus reuteri ; Lactobacillus reuteri - genetics ; Lactobacillus reuteri - growth & development ; Lactobacillus reuteri - metabolism ; Life Sciences ; Mice ; Mice, Inbred BALB C ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Mutagenesis, Insertional ; Mutants ; Mutation ; Original ; original-article ; Polysaccharides, Bacterial - biosynthesis ; Polysaccharides, Bacterial - chemistry ; Spleen - cytology ; Spleen - immunology ; Stomach - microbiology ; Sucrose - metabolism ; T-Lymphocytes, Regulatory - microbiology ; Vertebrates</subject><ispartof>The ISME Journal, 2011-07, Vol.5 (7), p.1115-1124</ispartof><rights>International Society for Microbial Ecology 2011</rights><rights>Copyright Nature Publishing Group Jul 2011</rights><rights>Copyright © 2011 International Society for Microbial Ecology 2011 International Society for Microbial Ecology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c488t-ac8b5e87044c5166d92dbfebcef56b09d37595ed14df7489410b094e95ba708b3</citedby><cites>FETCH-LOGICAL-c488t-ac8b5e87044c5166d92dbfebcef56b09d37595ed14df7489410b094e95ba708b3</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/PMC3146279/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3146279/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21248858$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sims, Ian M</creatorcontrib><creatorcontrib>Frese, Steven A</creatorcontrib><creatorcontrib>Walter, Jens</creatorcontrib><creatorcontrib>Loach, Diane</creatorcontrib><creatorcontrib>Wilson, Michelle</creatorcontrib><creatorcontrib>Appleyard, Kay</creatorcontrib><creatorcontrib>Eason, Jocelyn</creatorcontrib><creatorcontrib>Livingston, Megan</creatorcontrib><creatorcontrib>Baird, Margaret</creatorcontrib><creatorcontrib>Cook, Gregory</creatorcontrib><creatorcontrib>Tannock, Gerald W</creatorcontrib><title>Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Lactobacillus reuteri
strain 100-23 together with a
Lactobacillus
-free mouse model, provides a system with which the molecular traits underpinning bacterial commensalism in vertebrates can be studied. A polysaccharide was extracted from sucrose-containing liquid cultures of strain 100-23. Chemical analysis showed that this exopolysaccharide was a levan (β-2, 6-linked fructan). Mutation of the fructosyl transferase (
ftf
) gene resulted in loss of exopolysaccharide production. The
ftf
mutant was able to colonise the murine gastrointestinal tract in the absence of competition, but colonisation was impaired in competition with the wild type. Biofilm formation by the mutant on the forestomach epithelial surface was not impaired and the matrix between cells was indistinguishable from that of the wild type in electron micrographs. Colonisation of the mouse gut by the wild-type strain led to increased proportions of regulatory T cells (Foxp3+) in the spleen, whereas colonisation by the
ftf
mutant did not. Survival of the mutant in sucrose-containing medium was markedly reduced relative to the wild type. Comparison of the genomic
ftf
loci of strain 100-23 with other
L. reuteri
strains suggested that the
ftf
gene was acquired by lateral gene transfer early in the evolution of the species and subsequently diversified at accelerated rates. Levan production by
L. reuteri
100-23 may represent a function acquired by the bacterial species for life in moderate to high-sucrose extra-gastrointestinal environments that has subsequently been diverted to novel uses, including immunomodulation, that aid in colonisation of the murine gut.</description><subject>631/250/2152/569</subject><subject>631/326/2565/855</subject><subject>631/45/72/1205</subject><subject>692/698/2741/2135</subject><subject>Animals</subject><subject>Biofilms</subject><subject>Biomedical and Life Sciences</subject><subject>Chemical analysis</subject><subject>Colonization</subject><subject>Commensalism</subject><subject>Competition</subject><subject>Culture Media</subject><subject>Ecology</subject><subject>Evolutionary Biology</subject><subject>Fructans - biosynthesis</subject><subject>Fructans - chemistry</subject><subject>Gastrointestinal Contents - microbiology</subject><subject>Gastrointestinal tract</subject><subject>Genes, Bacterial</subject><subject>Hexosyltransferases - genetics</subject><subject>Lactobacillus reuteri</subject><subject>Lactobacillus reuteri - genetics</subject><subject>Lactobacillus reuteri - growth & development</subject><subject>Lactobacillus reuteri - metabolism</subject><subject>Life Sciences</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Mutagenesis, Insertional</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Original</subject><subject>original-article</subject><subject>Polysaccharides, Bacterial - biosynthesis</subject><subject>Polysaccharides, Bacterial - chemistry</subject><subject>Spleen - cytology</subject><subject>Spleen - immunology</subject><subject>Stomach - microbiology</subject><subject>Sucrose - metabolism</subject><subject>T-Lymphocytes, Regulatory - microbiology</subject><subject>Vertebrates</subject><issn>1751-7362</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kU1v1DAQhi1ERUvhyhFZXDhlayd27FyQUMWXtFIPwNnyx2TrVWIvdlyx_x4vWxao1MvYnnn8zoxehF5RsqKkk1c-z7BdtaS-a3iCLqjgtBGdIE9P9749R89z3hLCRd-LZ-i8pS2TkssLZL8uqdilJMA6ODyWYBcfQ8ZxxPAz7uK0z9raW528A7xL0RULDps93pQF2zjPELKe8FrbJRpt_TSVjBOUBZLHlJCm7V6gs1FPGV7en5fo-8cP364_N-ubT1-u368bW4dZGm2l4SAFYcxy2vduaJ0ZwVgYeW_I4DrBBw6OMjcKJgdGSc0yGLjRgkjTXaJ3R91dMTM4C2FJelK75Ged9ipqr_6vBH-rNvFOdZT1rRiqwNt7gRR_FMiLmn22ME06QCxZDUTQnksmK_nmAbmNJYW6nZKiSgk68AqtjpBNMecE42kUStTBPfXbPXVw7xDqh9f_LnDC_9hVgasjkGspbCD9bfuI5C8jdagU</recordid><startdate>20110701</startdate><enddate>20110701</enddate><creator>Sims, Ian M</creator><creator>Frese, Steven A</creator><creator>Walter, Jens</creator><creator>Loach, Diane</creator><creator>Wilson, Michelle</creator><creator>Appleyard, Kay</creator><creator>Eason, Jocelyn</creator><creator>Livingston, Megan</creator><creator>Baird, Margaret</creator><creator>Cook, Gregory</creator><creator>Tannock, Gerald W</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>SOI</scope><scope>5PM</scope></search><sort><creationdate>20110701</creationdate><title>Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23</title><author>Sims, Ian M ; Frese, Steven A ; Walter, Jens ; Loach, Diane ; Wilson, Michelle ; Appleyard, Kay ; Eason, Jocelyn ; Livingston, Megan ; Baird, Margaret ; Cook, Gregory ; Tannock, Gerald W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c488t-ac8b5e87044c5166d92dbfebcef56b09d37595ed14df7489410b094e95ba708b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>631/250/2152/569</topic><topic>631/326/2565/855</topic><topic>631/45/72/1205</topic><topic>692/698/2741/2135</topic><topic>Animals</topic><topic>Biofilms</topic><topic>Biomedical and Life Sciences</topic><topic>Chemical analysis</topic><topic>Colonization</topic><topic>Commensalism</topic><topic>Competition</topic><topic>Culture Media</topic><topic>Ecology</topic><topic>Evolutionary Biology</topic><topic>Fructans - biosynthesis</topic><topic>Fructans - chemistry</topic><topic>Gastrointestinal Contents - microbiology</topic><topic>Gastrointestinal tract</topic><topic>Genes, Bacterial</topic><topic>Hexosyltransferases - genetics</topic><topic>Lactobacillus reuteri</topic><topic>Lactobacillus reuteri - genetics</topic><topic>Lactobacillus reuteri - growth & development</topic><topic>Lactobacillus reuteri - metabolism</topic><topic>Life Sciences</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Microbial Ecology</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Mutagenesis, Insertional</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Original</topic><topic>original-article</topic><topic>Polysaccharides, Bacterial - biosynthesis</topic><topic>Polysaccharides, Bacterial - chemistry</topic><topic>Spleen - cytology</topic><topic>Spleen - immunology</topic><topic>Stomach - microbiology</topic><topic>Sucrose - metabolism</topic><topic>T-Lymphocytes, Regulatory - microbiology</topic><topic>Vertebrates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sims, Ian M</creatorcontrib><creatorcontrib>Frese, Steven A</creatorcontrib><creatorcontrib>Walter, Jens</creatorcontrib><creatorcontrib>Loach, Diane</creatorcontrib><creatorcontrib>Wilson, Michelle</creatorcontrib><creatorcontrib>Appleyard, Kay</creatorcontrib><creatorcontrib>Eason, Jocelyn</creatorcontrib><creatorcontrib>Livingston, Megan</creatorcontrib><creatorcontrib>Baird, Margaret</creatorcontrib><creatorcontrib>Cook, Gregory</creatorcontrib><creatorcontrib>Tannock, Gerald W</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</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>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Environmental Science Collection</collection><collection>Environment Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sims, Ian M</au><au>Frese, Steven A</au><au>Walter, Jens</au><au>Loach, Diane</au><au>Wilson, Michelle</au><au>Appleyard, Kay</au><au>Eason, Jocelyn</au><au>Livingston, Megan</au><au>Baird, Margaret</au><au>Cook, Gregory</au><au>Tannock, Gerald W</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2011-07-01</date><risdate>2011</risdate><volume>5</volume><issue>7</issue><spage>1115</spage><epage>1124</epage><pages>1115-1124</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>Lactobacillus reuteri
strain 100-23 together with a
Lactobacillus
-free mouse model, provides a system with which the molecular traits underpinning bacterial commensalism in vertebrates can be studied. A polysaccharide was extracted from sucrose-containing liquid cultures of strain 100-23. Chemical analysis showed that this exopolysaccharide was a levan (β-2, 6-linked fructan). Mutation of the fructosyl transferase (
ftf
) gene resulted in loss of exopolysaccharide production. The
ftf
mutant was able to colonise the murine gastrointestinal tract in the absence of competition, but colonisation was impaired in competition with the wild type. Biofilm formation by the mutant on the forestomach epithelial surface was not impaired and the matrix between cells was indistinguishable from that of the wild type in electron micrographs. Colonisation of the mouse gut by the wild-type strain led to increased proportions of regulatory T cells (Foxp3+) in the spleen, whereas colonisation by the
ftf
mutant did not. Survival of the mutant in sucrose-containing medium was markedly reduced relative to the wild type. Comparison of the genomic
ftf
loci of strain 100-23 with other
L. reuteri
strains suggested that the
ftf
gene was acquired by lateral gene transfer early in the evolution of the species and subsequently diversified at accelerated rates. Levan production by
L. reuteri
100-23 may represent a function acquired by the bacterial species for life in moderate to high-sucrose extra-gastrointestinal environments that has subsequently been diverted to novel uses, including immunomodulation, that aid in colonisation of the murine gut.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>21248858</pmid><doi>10.1038/ismej.2010.201</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 631/250/2152/569 631/326/2565/855 631/45/72/1205 692/698/2741/2135 Animals Biofilms Biomedical and Life Sciences Chemical analysis Colonization Commensalism Competition Culture Media Ecology Evolutionary Biology Fructans - biosynthesis Fructans - chemistry Gastrointestinal Contents - microbiology Gastrointestinal tract Genes, Bacterial Hexosyltransferases - genetics Lactobacillus reuteri Lactobacillus reuteri - genetics Lactobacillus reuteri - growth & development Lactobacillus reuteri - metabolism Life Sciences Mice Mice, Inbred BALB C Microbial Ecology Microbial Genetics and Genomics Microbiology Mutagenesis, Insertional Mutants Mutation Original original-article Polysaccharides, Bacterial - biosynthesis Polysaccharides, Bacterial - chemistry Spleen - cytology Spleen - immunology Stomach - microbiology Sucrose - metabolism T-Lymphocytes, Regulatory - microbiology Vertebrates |
title | Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23 |
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