Bacterial sensing underlies artificial sweetener-induced growth of gut Lactobacillus
Summary Disruption in stable establishment of commensal gut microbiota by early weaning is an important factor in susceptibility of young animals to enteric disorders. The artificial sweetener SUCRAM [consisting of neohesperidin dihydrochalcone (NHDC) and saccharin] included in piglets' feed re...
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| Veröffentlicht in: | Environmental microbiology 2016-07, Vol.18 (7), p.2159-2171 |
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| creator | Daly, Kristian Darby, Alistair C. Hall, Neil Wilkinson, Mark C. Pongchaikul, Pisut Bravo, David Shirazi-Beechey, Soraya P. |
| description | Summary
Disruption in stable establishment of commensal gut microbiota by early weaning is an important factor in susceptibility of young animals to enteric disorders. The artificial sweetener SUCRAM [consisting of neohesperidin dihydrochalcone (NHDC) and saccharin] included in piglets' feed reduces incidence of enteric disease. Pyrosequencing of pig caecal 16S rRNA gene amplicons identified 25 major families encompassing seven bacterial classes with Bacteroidia, Clostridia and Bacilli dominating the microbiota. There were significant shifts in microbial composition in pigs maintained on a diet containing SUCRAM, establishing SUCRAM as a major influence driving bacterial community dynamics. The most notable change was a significant increase of Lactobacillaceae population abundance, almost entirely due to a single phylotype, designated Lactobacillus 4228. The sweetener‐induced increase in Lactobacillaceae was observed in two different breeds of pigs signifying a general effect. We isolated Lactobacillus 4228, sequenced its genome and found it to be related to Lactobacillus amylovorus. In vitro analyses of Lactobacillus 4228 growth characteristics showed that presence of NHDC significantly reduces the lag phase of growth and enhances expression of specific sugar transporters, independently of NHDC metabolism. This study suggests that sensing of NHDC by a bacterial plasma membrane receptor underlies sweetener‐induced growth of a health promoting gut bacterium. |
| doi_str_mv | 10.1111/1462-2920.12942 |
| format | Article |
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Disruption in stable establishment of commensal gut microbiota by early weaning is an important factor in susceptibility of young animals to enteric disorders. The artificial sweetener SUCRAM [consisting of neohesperidin dihydrochalcone (NHDC) and saccharin] included in piglets' feed reduces incidence of enteric disease. Pyrosequencing of pig caecal 16S rRNA gene amplicons identified 25 major families encompassing seven bacterial classes with Bacteroidia, Clostridia and Bacilli dominating the microbiota. There were significant shifts in microbial composition in pigs maintained on a diet containing SUCRAM, establishing SUCRAM as a major influence driving bacterial community dynamics. The most notable change was a significant increase of Lactobacillaceae population abundance, almost entirely due to a single phylotype, designated Lactobacillus 4228. The sweetener‐induced increase in Lactobacillaceae was observed in two different breeds of pigs signifying a general effect. We isolated Lactobacillus 4228, sequenced its genome and found it to be related to Lactobacillus amylovorus. In vitro analyses of Lactobacillus 4228 growth characteristics showed that presence of NHDC significantly reduces the lag phase of growth and enhances expression of specific sugar transporters, independently of NHDC metabolism. This study suggests that sensing of NHDC by a bacterial plasma membrane receptor underlies sweetener‐induced growth of a health promoting gut bacterium.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.12942</identifier><identifier>PMID: 26058469</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animal Feed - analysis ; Animals ; Bacteria ; Bacteria - genetics ; Bacteria - isolation & purification ; Bacteria - metabolism ; Cecum - metabolism ; Cecum - microbiology ; Female ; Gastrointestinal Microbiome ; Intestinal Mucosa - metabolism ; Intestines - microbiology ; Lactobacillaceae ; Lactobacillus ; Lactobacillus - growth & development ; Lactobacillus - metabolism ; Lactobacillus amylovorus ; Male ; Saccharin - metabolism ; Sweetening Agents - metabolism ; Swine - metabolism ; Swine - microbiology ; Weaning</subject><ispartof>Environmental microbiology, 2016-07, Vol.18 (7), p.2159-2171</ispartof><rights>2015 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2015 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2016 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.12942$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.12942$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26058469$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Daly, Kristian</creatorcontrib><creatorcontrib>Darby, Alistair C.</creatorcontrib><creatorcontrib>Hall, Neil</creatorcontrib><creatorcontrib>Wilkinson, Mark C.</creatorcontrib><creatorcontrib>Pongchaikul, Pisut</creatorcontrib><creatorcontrib>Bravo, David</creatorcontrib><creatorcontrib>Shirazi-Beechey, Soraya P.</creatorcontrib><title>Bacterial sensing underlies artificial sweetener-induced growth of gut Lactobacillus</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Disruption in stable establishment of commensal gut microbiota by early weaning is an important factor in susceptibility of young animals to enteric disorders. The artificial sweetener SUCRAM [consisting of neohesperidin dihydrochalcone (NHDC) and saccharin] included in piglets' feed reduces incidence of enteric disease. Pyrosequencing of pig caecal 16S rRNA gene amplicons identified 25 major families encompassing seven bacterial classes with Bacteroidia, Clostridia and Bacilli dominating the microbiota. There were significant shifts in microbial composition in pigs maintained on a diet containing SUCRAM, establishing SUCRAM as a major influence driving bacterial community dynamics. The most notable change was a significant increase of Lactobacillaceae population abundance, almost entirely due to a single phylotype, designated Lactobacillus 4228. The sweetener‐induced increase in Lactobacillaceae was observed in two different breeds of pigs signifying a general effect. We isolated Lactobacillus 4228, sequenced its genome and found it to be related to Lactobacillus amylovorus. In vitro analyses of Lactobacillus 4228 growth characteristics showed that presence of NHDC significantly reduces the lag phase of growth and enhances expression of specific sugar transporters, independently of NHDC metabolism. This study suggests that sensing of NHDC by a bacterial plasma membrane receptor underlies sweetener‐induced growth of a health promoting gut bacterium.</description><subject>Animal Feed - analysis</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Bacteria - metabolism</subject><subject>Cecum - metabolism</subject><subject>Cecum - microbiology</subject><subject>Female</subject><subject>Gastrointestinal Microbiome</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestines - microbiology</subject><subject>Lactobacillaceae</subject><subject>Lactobacillus</subject><subject>Lactobacillus - growth & development</subject><subject>Lactobacillus - metabolism</subject><subject>Lactobacillus amylovorus</subject><subject>Male</subject><subject>Saccharin - metabolism</subject><subject>Sweetening Agents - metabolism</subject><subject>Swine - metabolism</subject><subject>Swine - microbiology</subject><subject>Weaning</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkbtPwzAQxi0E4j2zoUgsLAHbsR1nhIpHpfKQKILNcpxLMaQJ2IlK_3vctHRgwovv8ftOuvsQOiL4jIR3TpigMc1oSGnG6AbaXVc21zGhO2jP-3eMSZqkeBvtUIG5ZCLbReNLbVpwVleRh9rbehJ1dQGusuAj7VpbWtM3ZwAt1OBiWxedgSKauGbWvkVNGU26NhqFMU2uja2qzh-grVJXHg5X_z56vr4aD27j0cPNcHAxii0XlMZCEg2a4CyHBArO8xRLKKXkCaZlSYw2LGTUYElLLagmsoCcC1MKJguc8mQfnS7nfrrmqwPfqqn1BqpK19B0XhGJpUhlmuL_oDRlLCEkoCd_0Pemc3VYpKcYJ5LRQB2vqC6fQqE-nZ1qN1e_pw0AXwIzW8F83SdYLZxTC2_UwifVO6eu7oZ9EHTxUmd9C99rnXYfSgT7uHq5v1HX-OmVYfmoBskPmtaYhQ</recordid><startdate>201607</startdate><enddate>201607</enddate><creator>Daly, Kristian</creator><creator>Darby, Alistair C.</creator><creator>Hall, Neil</creator><creator>Wilkinson, Mark C.</creator><creator>Pongchaikul, Pisut</creator><creator>Bravo, David</creator><creator>Shirazi-Beechey, Soraya P.</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope></search><sort><creationdate>201607</creationdate><title>Bacterial sensing underlies artificial sweetener-induced growth of gut Lactobacillus</title><author>Daly, Kristian ; Darby, Alistair C. ; Hall, Neil ; Wilkinson, Mark C. ; Pongchaikul, Pisut ; Bravo, David ; Shirazi-Beechey, Soraya P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-i5622-681aea109be3ed55b708ef885302ff1cac4f882c082fa62a18deb56cf648d0753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animal Feed - analysis</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacteria - genetics</topic><topic>Bacteria - isolation & purification</topic><topic>Bacteria - metabolism</topic><topic>Cecum - metabolism</topic><topic>Cecum - microbiology</topic><topic>Female</topic><topic>Gastrointestinal Microbiome</topic><topic>Intestinal Mucosa - metabolism</topic><topic>Intestines - microbiology</topic><topic>Lactobacillaceae</topic><topic>Lactobacillus</topic><topic>Lactobacillus - growth & development</topic><topic>Lactobacillus - metabolism</topic><topic>Lactobacillus amylovorus</topic><topic>Male</topic><topic>Saccharin - metabolism</topic><topic>Sweetening Agents - metabolism</topic><topic>Swine - metabolism</topic><topic>Swine - microbiology</topic><topic>Weaning</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Daly, Kristian</creatorcontrib><creatorcontrib>Darby, Alistair C.</creatorcontrib><creatorcontrib>Hall, Neil</creatorcontrib><creatorcontrib>Wilkinson, Mark C.</creatorcontrib><creatorcontrib>Pongchaikul, Pisut</creatorcontrib><creatorcontrib>Bravo, David</creatorcontrib><creatorcontrib>Shirazi-Beechey, Soraya P.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Daly, Kristian</au><au>Darby, Alistair C.</au><au>Hall, Neil</au><au>Wilkinson, Mark C.</au><au>Pongchaikul, Pisut</au><au>Bravo, David</au><au>Shirazi-Beechey, Soraya P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bacterial sensing underlies artificial sweetener-induced growth of gut Lactobacillus</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2016-07</date><risdate>2016</risdate><volume>18</volume><issue>7</issue><spage>2159</spage><epage>2171</epage><pages>2159-2171</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Disruption in stable establishment of commensal gut microbiota by early weaning is an important factor in susceptibility of young animals to enteric disorders. The artificial sweetener SUCRAM [consisting of neohesperidin dihydrochalcone (NHDC) and saccharin] included in piglets' feed reduces incidence of enteric disease. Pyrosequencing of pig caecal 16S rRNA gene amplicons identified 25 major families encompassing seven bacterial classes with Bacteroidia, Clostridia and Bacilli dominating the microbiota. There were significant shifts in microbial composition in pigs maintained on a diet containing SUCRAM, establishing SUCRAM as a major influence driving bacterial community dynamics. The most notable change was a significant increase of Lactobacillaceae population abundance, almost entirely due to a single phylotype, designated Lactobacillus 4228. The sweetener‐induced increase in Lactobacillaceae was observed in two different breeds of pigs signifying a general effect. We isolated Lactobacillus 4228, sequenced its genome and found it to be related to Lactobacillus amylovorus. In vitro analyses of Lactobacillus 4228 growth characteristics showed that presence of NHDC significantly reduces the lag phase of growth and enhances expression of specific sugar transporters, independently of NHDC metabolism. This study suggests that sensing of NHDC by a bacterial plasma membrane receptor underlies sweetener‐induced growth of a health promoting gut bacterium.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>26058469</pmid><doi>10.1111/1462-2920.12942</doi><tpages>13</tpages></addata></record> |
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| subjects | Animal Feed - analysis Animals Bacteria Bacteria - genetics Bacteria - isolation & purification Bacteria - metabolism Cecum - metabolism Cecum - microbiology Female Gastrointestinal Microbiome Intestinal Mucosa - metabolism Intestines - microbiology Lactobacillaceae Lactobacillus Lactobacillus - growth & development Lactobacillus - metabolism Lactobacillus amylovorus Male Saccharin - metabolism Sweetening Agents - metabolism Swine - metabolism Swine - microbiology Weaning |
| title | Bacterial sensing underlies artificial sweetener-induced growth of gut Lactobacillus |
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