Cargando…

Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine

Escherichia coli is a single species consisting of many biotypes, some of which are commensal colonizers of mammals and others that cause disease. Humans are colonized on average with five commensal biotypes, and it is widely thought that the commensals serve as a barrier to infection by pathogens....

Descripción completa

Detalles Bibliográficos
Autores principales: Maltby, Rosalie, Leatham-Jensen, Mary P., Gibson, Terri, Cohen, Paul S., Conway, Tyrrell
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3547972/
https://www.ncbi.nlm.nih.gov/pubmed/23349773
http://dx.doi.org/10.1371/journal.pone.0053957
_version_ 1782256269049987072
author Maltby, Rosalie
Leatham-Jensen, Mary P.
Gibson, Terri
Cohen, Paul S.
Conway, Tyrrell
author_facet Maltby, Rosalie
Leatham-Jensen, Mary P.
Gibson, Terri
Cohen, Paul S.
Conway, Tyrrell
author_sort Maltby, Rosalie
collection PubMed
description Escherichia coli is a single species consisting of many biotypes, some of which are commensal colonizers of mammals and others that cause disease. Humans are colonized on average with five commensal biotypes, and it is widely thought that the commensals serve as a barrier to infection by pathogens. Previous studies showed that a combination of three pre-colonized commensal E. coli strains prevents colonization of E. coli O157:H7 in a mouse model (Leatham, et al., 2010, Infect Immun 77: 2876–7886). The commensal biotypes included E. coli HS, which is known to successfully colonize humans at high doses with no adverse effects, and E. coli Nissle 1917, a human commensal strain that is used in Europe as a preventative of traveler's diarrhea. We hypothesized that commensal biotypes could exert colonization resistance by consuming nutrients needed by E. coli O157:H7 to colonize, thus preventing this first step in infection. Here we report that to colonize streptomycin-treated mice E. coli HS consumes six of the twelve sugars tested and E. coli Nissle 1917 uses a complementary yet divergent set of seven sugars to colonize, thus establishing a nutritional basis for the ability of E. coli HS and Nissle 1917 to occupy distinct niches in the mouse intestine. Together these two commensals use the five sugars previously determined to be most important for colonization of E. coli EDL933, an O157:H7 strain. As predicted, the two commensals prevented E. coli EDL933 colonization. The results support a model in which invading pathogenic E. coli must compete with the gut microbiota to obtain the nutrients needed to colonize and establish infection; accordingly, the outcome of the challenge is determined by the aggregate capacity of the native microbiota to consume the nutrients required by the pathogen.
format Online
Article
Text
id pubmed-3547972
institution National Center for Biotechnology Information
language English
publishDate 2013
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-35479722013-01-24 Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine Maltby, Rosalie Leatham-Jensen, Mary P. Gibson, Terri Cohen, Paul S. Conway, Tyrrell PLoS One Research Article Escherichia coli is a single species consisting of many biotypes, some of which are commensal colonizers of mammals and others that cause disease. Humans are colonized on average with five commensal biotypes, and it is widely thought that the commensals serve as a barrier to infection by pathogens. Previous studies showed that a combination of three pre-colonized commensal E. coli strains prevents colonization of E. coli O157:H7 in a mouse model (Leatham, et al., 2010, Infect Immun 77: 2876–7886). The commensal biotypes included E. coli HS, which is known to successfully colonize humans at high doses with no adverse effects, and E. coli Nissle 1917, a human commensal strain that is used in Europe as a preventative of traveler's diarrhea. We hypothesized that commensal biotypes could exert colonization resistance by consuming nutrients needed by E. coli O157:H7 to colonize, thus preventing this first step in infection. Here we report that to colonize streptomycin-treated mice E. coli HS consumes six of the twelve sugars tested and E. coli Nissle 1917 uses a complementary yet divergent set of seven sugars to colonize, thus establishing a nutritional basis for the ability of E. coli HS and Nissle 1917 to occupy distinct niches in the mouse intestine. Together these two commensals use the five sugars previously determined to be most important for colonization of E. coli EDL933, an O157:H7 strain. As predicted, the two commensals prevented E. coli EDL933 colonization. The results support a model in which invading pathogenic E. coli must compete with the gut microbiota to obtain the nutrients needed to colonize and establish infection; accordingly, the outcome of the challenge is determined by the aggregate capacity of the native microbiota to consume the nutrients required by the pathogen. Public Library of Science 2013-01-17 /pmc/articles/PMC3547972/ /pubmed/23349773 http://dx.doi.org/10.1371/journal.pone.0053957 Text en © 2013 Maltby et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Maltby, Rosalie
Leatham-Jensen, Mary P.
Gibson, Terri
Cohen, Paul S.
Conway, Tyrrell
Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine
title Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine
title_full Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine
title_fullStr Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine
title_full_unstemmed Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine
title_short Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine
title_sort nutritional basis for colonization resistance by human commensal escherichia coli strains hs and nissle 1917 against e. coli o157:h7 in the mouse intestine
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3547972/
https://www.ncbi.nlm.nih.gov/pubmed/23349773
http://dx.doi.org/10.1371/journal.pone.0053957
work_keys_str_mv AT maltbyrosalie nutritionalbasisforcolonizationresistancebyhumancommensalescherichiacolistrainshsandnissle1917againstecolio157h7inthemouseintestine
AT leathamjensenmaryp nutritionalbasisforcolonizationresistancebyhumancommensalescherichiacolistrainshsandnissle1917againstecolio157h7inthemouseintestine
AT gibsonterri nutritionalbasisforcolonizationresistancebyhumancommensalescherichiacolistrainshsandnissle1917againstecolio157h7inthemouseintestine
AT cohenpauls nutritionalbasisforcolonizationresistancebyhumancommensalescherichiacolistrainshsandnissle1917againstecolio157h7inthemouseintestine
AT conwaytyrrell nutritionalbasisforcolonizationresistancebyhumancommensalescherichiacolistrainshsandnissle1917againstecolio157h7inthemouseintestine