Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota
Lactobacilli are gram-positive bacteria that are a subdominant element in the human gastrointestinal microbiota, and which are commonly used in the food industry. Some lactobacilli are considered probiotic, and have been associated with health benefits. However, there is very little culture-independ...
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creator | Riboulet-Bisson, Eliette Sturme, Mark H J Jeffery, Ian B O'Donnell, Michelle M Neville, B Anne Forde, Brian M Claesson, Marcus J Harris, Hugh Gardiner, Gillian E Casey, Patrick G Lawlor, Peadar G O'Toole, Paul W Ross, R Paul |
description | Lactobacilli are gram-positive bacteria that are a subdominant element in the human gastrointestinal microbiota, and which are commonly used in the food industry. Some lactobacilli are considered probiotic, and have been associated with health benefits. However, there is very little culture-independent information on how consumed probiotic microorganisms might affect the entire intestinal microbiota. We therefore studied the impact of the administration of Lactobacillus salivarius UCC118, a microorganism well characterized for its probiotic properties, on the composition of the intestinal microbiota in two model animals. UCC118 has anti-infective activity due to production of the bacteriocin Abp118, a broad-spectrum class IIb bacteriocin, which we hypothesized could impact the microbiota. Mice and pigs were administered wild-type (WT) L. salivarius UCC118 cells, or a mutant lacking bacteriocin production. The microbiota composition was determined by pyrosequencing of 16S rRNA gene amplicons from faeces. The data show that L. salivarius UCC118 administration had no significant effect on proportions of major phyla comprising the mouse microbiota, whether the strain was producing bacteriocin or not. However, L. salivarius UCC118 WT administration led to a significant decrease in Spirochaetes levels, the third major phylum in the untreated pig microbiota. In both pigs and mice, L. salivarius UCC118 administration had an effect on Firmicutes genus members. This effect was not observed when the mutant strain was administered, and was thus associated with bacteriocin production. Surprisingly, in both models, L. salivarius UCC118 administration and production of Abp118 had an effect on gram-negative microorganisms, even though Abp118 is normally not active in vitro against this group of microorganisms. Thus L. salivarius UCC118 administration has a significant but subtle impact on mouse and pig microbiota, by a mechanism that seems at least partially bacteriocin-dependent. |
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Some lactobacilli are considered probiotic, and have been associated with health benefits. However, there is very little culture-independent information on how consumed probiotic microorganisms might affect the entire intestinal microbiota. We therefore studied the impact of the administration of Lactobacillus salivarius UCC118, a microorganism well characterized for its probiotic properties, on the composition of the intestinal microbiota in two model animals. UCC118 has anti-infective activity due to production of the bacteriocin Abp118, a broad-spectrum class IIb bacteriocin, which we hypothesized could impact the microbiota. Mice and pigs were administered wild-type (WT) L. salivarius UCC118 cells, or a mutant lacking bacteriocin production. The microbiota composition was determined by pyrosequencing of 16S rRNA gene amplicons from faeces. The data show that L. salivarius UCC118 administration had no significant effect on proportions of major phyla comprising the mouse microbiota, whether the strain was producing bacteriocin or not. However, L. salivarius UCC118 WT administration led to a significant decrease in Spirochaetes levels, the third major phylum in the untreated pig microbiota. In both pigs and mice, L. salivarius UCC118 administration had an effect on Firmicutes genus members. This effect was not observed when the mutant strain was administered, and was thus associated with bacteriocin production. Surprisingly, in both models, L. salivarius UCC118 administration and production of Abp118 had an effect on gram-negative microorganisms, even though Abp118 is normally not active in vitro against this group of microorganisms. Thus L. salivarius UCC118 administration has a significant but subtle impact on mouse and pig microbiota, by a mechanism that seems at least partially bacteriocin-dependent.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0031113</identifier><identifier>PMID: 22363561</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Analysis ; Animal models ; Animals ; Antibiotics ; Bacteria ; Bacterial Adhesion - drug effects ; Bacteriocins - administration & dosage ; Bacteriocins - pharmacology ; Biology ; Cell culture ; E coli ; Escherichia coli ; Feces - microbiology ; Feeding Behavior - drug effects ; Female ; Food ; Food industry ; Food processing industry ; Gastrointestinal Transit - drug effects ; Gene expression ; Gram-positive bacteria ; Health insurance ; Health sciences ; Hogs ; Humans ; Infections ; Intestinal microflora ; Intestinal Mucosa - drug effects ; Intestinal Mucosa - microbiology ; Intestine ; Intestines - drug effects ; Intestines - microbiology ; Lactobacilli ; Lactobacillus ; Lactobacillus plantarum ; Listeria ; Medicine ; Metagenome - drug effects ; Mice ; Mice, Inbred BALB C ; Microbial Viability - drug effects ; Microbiota (Symbiotic organisms) ; Microorganisms ; Models, Animal ; Mutation - genetics ; Permeability ; Phylogenetics ; Pigs ; Probiotics ; Probiotics - administration & dosage ; Probiotics - pharmacology ; rRNA 16S ; Salmonella ; Studies ; Suidae ; Sus scrofa - growth & development ; Sus scrofa - microbiology ; Swine ; Time Factors ; Weight Gain - drug effects</subject><ispartof>PloS one, 2012-02, Vol.7 (2), p.e31113</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Riboulet-Bisson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Riboulet-Bisson et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c782t-ea10cb2e2577864f26de7158a2dd9920a9ba488612a6828a90808057acd13f243</citedby><cites>FETCH-LOGICAL-c782t-ea10cb2e2577864f26de7158a2dd9920a9ba488612a6828a90808057acd13f243</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/PMC3281923/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3281923/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22363561$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Riboulet-Bisson, Eliette</creatorcontrib><creatorcontrib>Sturme, Mark H J</creatorcontrib><creatorcontrib>Jeffery, Ian B</creatorcontrib><creatorcontrib>O'Donnell, Michelle M</creatorcontrib><creatorcontrib>Neville, B Anne</creatorcontrib><creatorcontrib>Forde, Brian M</creatorcontrib><creatorcontrib>Claesson, Marcus J</creatorcontrib><creatorcontrib>Harris, Hugh</creatorcontrib><creatorcontrib>Gardiner, Gillian E</creatorcontrib><creatorcontrib>Casey, Patrick G</creatorcontrib><creatorcontrib>Lawlor, Peadar G</creatorcontrib><creatorcontrib>O'Toole, Paul W</creatorcontrib><creatorcontrib>Ross, R Paul</creatorcontrib><title>Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Lactobacilli are gram-positive bacteria that are a subdominant element in the human gastrointestinal microbiota, and which are commonly used in the food industry. Some lactobacilli are considered probiotic, and have been associated with health benefits. However, there is very little culture-independent information on how consumed probiotic microorganisms might affect the entire intestinal microbiota. We therefore studied the impact of the administration of Lactobacillus salivarius UCC118, a microorganism well characterized for its probiotic properties, on the composition of the intestinal microbiota in two model animals. UCC118 has anti-infective activity due to production of the bacteriocin Abp118, a broad-spectrum class IIb bacteriocin, which we hypothesized could impact the microbiota. Mice and pigs were administered wild-type (WT) L. salivarius UCC118 cells, or a mutant lacking bacteriocin production. The microbiota composition was determined by pyrosequencing of 16S rRNA gene amplicons from faeces. The data show that L. salivarius UCC118 administration had no significant effect on proportions of major phyla comprising the mouse microbiota, whether the strain was producing bacteriocin or not. However, L. salivarius UCC118 WT administration led to a significant decrease in Spirochaetes levels, the third major phylum in the untreated pig microbiota. In both pigs and mice, L. salivarius UCC118 administration had an effect on Firmicutes genus members. This effect was not observed when the mutant strain was administered, and was thus associated with bacteriocin production. Surprisingly, in both models, L. salivarius UCC118 administration and production of Abp118 had an effect on gram-negative microorganisms, even though Abp118 is normally not active in vitro against this group of microorganisms. Thus L. salivarius UCC118 administration has a significant but subtle impact on mouse and pig microbiota, by a mechanism that seems at least partially bacteriocin-dependent.</description><subject>Acids</subject><subject>Analysis</subject><subject>Animal models</subject><subject>Animals</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Bacterial Adhesion - drug effects</subject><subject>Bacteriocins - administration & dosage</subject><subject>Bacteriocins - pharmacology</subject><subject>Biology</subject><subject>Cell culture</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Feces - microbiology</subject><subject>Feeding Behavior - drug effects</subject><subject>Female</subject><subject>Food</subject><subject>Food industry</subject><subject>Food processing industry</subject><subject>Gastrointestinal Transit - drug effects</subject><subject>Gene expression</subject><subject>Gram-positive bacteria</subject><subject>Health insurance</subject><subject>Health sciences</subject><subject>Hogs</subject><subject>Humans</subject><subject>Infections</subject><subject>Intestinal microflora</subject><subject>Intestinal Mucosa - drug effects</subject><subject>Intestinal Mucosa - microbiology</subject><subject>Intestine</subject><subject>Intestines - drug effects</subject><subject>Intestines - microbiology</subject><subject>Lactobacilli</subject><subject>Lactobacillus</subject><subject>Lactobacillus plantarum</subject><subject>Listeria</subject><subject>Medicine</subject><subject>Metagenome - drug effects</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbial Viability - drug effects</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Models, Animal</subject><subject>Mutation - genetics</subject><subject>Permeability</subject><subject>Phylogenetics</subject><subject>Pigs</subject><subject>Probiotics</subject><subject>Probiotics - administration & dosage</subject><subject>Probiotics - pharmacology</subject><subject>rRNA 16S</subject><subject>Salmonella</subject><subject>Studies</subject><subject>Suidae</subject><subject>Sus scrofa - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</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>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content 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>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Riboulet-Bisson, Eliette</au><au>Sturme, Mark H J</au><au>Jeffery, Ian B</au><au>O'Donnell, Michelle M</au><au>Neville, B Anne</au><au>Forde, Brian M</au><au>Claesson, Marcus J</au><au>Harris, Hugh</au><au>Gardiner, Gillian E</au><au>Casey, Patrick G</au><au>Lawlor, Peadar G</au><au>O'Toole, Paul W</au><au>Ross, R Paul</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-02-17</date><risdate>2012</risdate><volume>7</volume><issue>2</issue><spage>e31113</spage><pages>e31113-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Lactobacilli are gram-positive bacteria that are a subdominant element in the human gastrointestinal microbiota, and which are commonly used in the food industry. Some lactobacilli are considered probiotic, and have been associated with health benefits. However, there is very little culture-independent information on how consumed probiotic microorganisms might affect the entire intestinal microbiota. We therefore studied the impact of the administration of Lactobacillus salivarius UCC118, a microorganism well characterized for its probiotic properties, on the composition of the intestinal microbiota in two model animals. UCC118 has anti-infective activity due to production of the bacteriocin Abp118, a broad-spectrum class IIb bacteriocin, which we hypothesized could impact the microbiota. Mice and pigs were administered wild-type (WT) L. salivarius UCC118 cells, or a mutant lacking bacteriocin production. The microbiota composition was determined by pyrosequencing of 16S rRNA gene amplicons from faeces. The data show that L. salivarius UCC118 administration had no significant effect on proportions of major phyla comprising the mouse microbiota, whether the strain was producing bacteriocin or not. However, L. salivarius UCC118 WT administration led to a significant decrease in Spirochaetes levels, the third major phylum in the untreated pig microbiota. In both pigs and mice, L. salivarius UCC118 administration had an effect on Firmicutes genus members. This effect was not observed when the mutant strain was administered, and was thus associated with bacteriocin production. Surprisingly, in both models, L. salivarius UCC118 administration and production of Abp118 had an effect on gram-negative microorganisms, even though Abp118 is normally not active in vitro against this group of microorganisms. Thus L. salivarius UCC118 administration has a significant but subtle impact on mouse and pig microbiota, by a mechanism that seems at least partially bacteriocin-dependent.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22363561</pmid><doi>10.1371/journal.pone.0031113</doi><tpages>e31113</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2012-02, Vol.7 (2), p.e31113 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1323570865 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
subjects | Acids Analysis Animal models Animals Antibiotics Bacteria Bacterial Adhesion - drug effects Bacteriocins - administration & dosage Bacteriocins - pharmacology Biology Cell culture E coli Escherichia coli Feces - microbiology Feeding Behavior - drug effects Female Food Food industry Food processing industry Gastrointestinal Transit - drug effects Gene expression Gram-positive bacteria Health insurance Health sciences Hogs Humans Infections Intestinal microflora Intestinal Mucosa - drug effects Intestinal Mucosa - microbiology Intestine Intestines - drug effects Intestines - microbiology Lactobacilli Lactobacillus Lactobacillus plantarum Listeria Medicine Metagenome - drug effects Mice Mice, Inbred BALB C Microbial Viability - drug effects Microbiota (Symbiotic organisms) Microorganisms Models, Animal Mutation - genetics Permeability Phylogenetics Pigs Probiotics Probiotics - administration & dosage Probiotics - pharmacology rRNA 16S Salmonella Studies Suidae Sus scrofa - growth & development Sus scrofa - microbiology Swine Time Factors Weight Gain - drug effects |
title | Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota |
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