Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces

Imke E Mulder; Bettina Schmidt; Chris R Stokes; Marie Lewis; Mick Bailey; Rustam I Aminov; James I Prosser; Bhupinder P Gill; John R Pluske; Claus-Dieter Mayer; Corran C Musk; Denise Kelly

doi:10.1186/1741-7007-7-79

Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces

Imke E Mulder, Bettina Schmidt, Chris R Stokes, Marie Lewis, Mick Bailey, Rustam I Aminov, James I Prosser, Bhupinder P Gill, John R Pluske, Claus-Dieter Mayer, Corran C Musk, Denise Kelly

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Abstract

Background: Early microbial colonization of the gut reduces the incidence of infectious, inflammatory and autoimmune diseases. Recent population studies reveal that childhood hygiene is a significant risk factor for development of inflammatory bowel disease, thereby reinforcing the hygiene hypothesis and the potential importance of microbial colonization during early life. The extent to which early-life environment impacts on microbial diversity of the adult gut and subsequent immune processes has not been comprehensively investigated thus far. We addressed this important question using the pig as a model to evaluate the impact of early-life environment on microbe/host gut interactions during development.

Results: Genetically-related piglets were housed in either indoor or outdoor environments or in experimental isolators. Analysis of over 3,000 16S rRNA sequences revealed major differences in mucosa-adherent microbial diversity in the ileum of adult pigs attributable to differences in early-life environment. Pigs housed in a natural outdoor environment showed a dominance of Firmicutes, in particular Lactobacillus, whereas animals housed in a hygienic indoor environment had reduced Lactobacillus and higher numbers of potentially pathogenic phylotypes. Our analysis revealed a strong negative correlation between the abundance of Firmicutes and pathogenic bacterial populations in the gut. These differences were exaggerated in animals housed in experimental isolators. Affymetrix microarray technology and Real-time Polymerase Chain Reaction revealed significant gut-specific gene responses also related to early-life environment. Significantly, indoor-housed pigs displayed increased expression of Type 1 interferon genes, Major Histocompatibility Complex class I and several chemokines. Gene Ontology and pathway analysis further confirmed these results.

Conclusion: Early-life environment significantly affects both microbial composition of the adult gut and mucosal innate immune function. We observed that a microbiota dominated by lactobacilli may function to maintain mucosal immune homeostasis and limit pathogen colonization.

Original language	English
Article number	79
Number of pages	20
Journal	BMC Biology
Volume	7
DOIs	https://doi.org/10.1186/1741-7007-7-79
Publication status	Published - 20 Nov 2009

Keywords

toll-like receptors
crohns-disease
intestinal microbiota
chemokine expression
hygiene hypothesis
gene-expression
dendritic cells
paneth cells
in-vitro
induction

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10.1186/1741-7007-7-79

BMC Developmental Biology 7
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@article{e92fc3ed206e419a8a00b319d4b29dd8,

title = "Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces",

abstract = "Background: Early microbial colonization of the gut reduces the incidence of infectious, inflammatory and autoimmune diseases. Recent population studies reveal that childhood hygiene is a significant risk factor for development of inflammatory bowel disease, thereby reinforcing the hygiene hypothesis and the potential importance of microbial colonization during early life. The extent to which early-life environment impacts on microbial diversity of the adult gut and subsequent immune processes has not been comprehensively investigated thus far. We addressed this important question using the pig as a model to evaluate the impact of early-life environment on microbe/host gut interactions during development. Results: Genetically-related piglets were housed in either indoor or outdoor environments or in experimental isolators. Analysis of over 3,000 16S rRNA sequences revealed major differences in mucosa-adherent microbial diversity in the ileum of adult pigs attributable to differences in early-life environment. Pigs housed in a natural outdoor environment showed a dominance of Firmicutes, in particular Lactobacillus, whereas animals housed in a hygienic indoor environment had reduced Lactobacillus and higher numbers of potentially pathogenic phylotypes. Our analysis revealed a strong negative correlation between the abundance of Firmicutes and pathogenic bacterial populations in the gut. These differences were exaggerated in animals housed in experimental isolators. Affymetrix microarray technology and Real-time Polymerase Chain Reaction revealed significant gut-specific gene responses also related to early-life environment. Significantly, indoor-housed pigs displayed increased expression of Type 1 interferon genes, Major Histocompatibility Complex class I and several chemokines. Gene Ontology and pathway analysis further confirmed these results. Conclusion: Early-life environment significantly affects both microbial composition of the adult gut and mucosal innate immune function. We observed that a microbiota dominated by lactobacilli may function to maintain mucosal immune homeostasis and limit pathogen colonization.",

keywords = "toll-like receptors, crohns-disease, intestinal microbiota, chemokine expression, hygiene hypothesis, gene-expression, dendritic cells, paneth cells, in-vitro, induction",

author = "Mulder, {Imke E} and Bettina Schmidt and Stokes, {Chris R} and Marie Lewis and Mick Bailey and Aminov, {Rustam I} and Prosser, {James I} and Gill, {Bhupinder P} and Pluske, {John R} and Claus-Dieter Mayer and Musk, {Corran C} and Denise Kelly",

year = "2009",

month = nov,

day = "20",

doi = "10.1186/1741-7007-7-79",

language = "English",

volume = "7",

journal = "BMC Biology",

issn = "1741-7007",

publisher = "BioMed Central",

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TY - JOUR

T1 - Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces

AU - Mulder, Imke E

AU - Schmidt, Bettina

AU - Stokes, Chris R

AU - Lewis, Marie

AU - Bailey, Mick

AU - Aminov, Rustam I

AU - Prosser, James I

AU - Gill, Bhupinder P

AU - Pluske, John R

AU - Mayer, Claus-Dieter

AU - Musk, Corran C

AU - Kelly, Denise

PY - 2009/11/20

Y1 - 2009/11/20

N2 - Background: Early microbial colonization of the gut reduces the incidence of infectious, inflammatory and autoimmune diseases. Recent population studies reveal that childhood hygiene is a significant risk factor for development of inflammatory bowel disease, thereby reinforcing the hygiene hypothesis and the potential importance of microbial colonization during early life. The extent to which early-life environment impacts on microbial diversity of the adult gut and subsequent immune processes has not been comprehensively investigated thus far. We addressed this important question using the pig as a model to evaluate the impact of early-life environment on microbe/host gut interactions during development. Results: Genetically-related piglets were housed in either indoor or outdoor environments or in experimental isolators. Analysis of over 3,000 16S rRNA sequences revealed major differences in mucosa-adherent microbial diversity in the ileum of adult pigs attributable to differences in early-life environment. Pigs housed in a natural outdoor environment showed a dominance of Firmicutes, in particular Lactobacillus, whereas animals housed in a hygienic indoor environment had reduced Lactobacillus and higher numbers of potentially pathogenic phylotypes. Our analysis revealed a strong negative correlation between the abundance of Firmicutes and pathogenic bacterial populations in the gut. These differences were exaggerated in animals housed in experimental isolators. Affymetrix microarray technology and Real-time Polymerase Chain Reaction revealed significant gut-specific gene responses also related to early-life environment. Significantly, indoor-housed pigs displayed increased expression of Type 1 interferon genes, Major Histocompatibility Complex class I and several chemokines. Gene Ontology and pathway analysis further confirmed these results. Conclusion: Early-life environment significantly affects both microbial composition of the adult gut and mucosal innate immune function. We observed that a microbiota dominated by lactobacilli may function to maintain mucosal immune homeostasis and limit pathogen colonization.

AB - Background: Early microbial colonization of the gut reduces the incidence of infectious, inflammatory and autoimmune diseases. Recent population studies reveal that childhood hygiene is a significant risk factor for development of inflammatory bowel disease, thereby reinforcing the hygiene hypothesis and the potential importance of microbial colonization during early life. The extent to which early-life environment impacts on microbial diversity of the adult gut and subsequent immune processes has not been comprehensively investigated thus far. We addressed this important question using the pig as a model to evaluate the impact of early-life environment on microbe/host gut interactions during development. Results: Genetically-related piglets were housed in either indoor or outdoor environments or in experimental isolators. Analysis of over 3,000 16S rRNA sequences revealed major differences in mucosa-adherent microbial diversity in the ileum of adult pigs attributable to differences in early-life environment. Pigs housed in a natural outdoor environment showed a dominance of Firmicutes, in particular Lactobacillus, whereas animals housed in a hygienic indoor environment had reduced Lactobacillus and higher numbers of potentially pathogenic phylotypes. Our analysis revealed a strong negative correlation between the abundance of Firmicutes and pathogenic bacterial populations in the gut. These differences were exaggerated in animals housed in experimental isolators. Affymetrix microarray technology and Real-time Polymerase Chain Reaction revealed significant gut-specific gene responses also related to early-life environment. Significantly, indoor-housed pigs displayed increased expression of Type 1 interferon genes, Major Histocompatibility Complex class I and several chemokines. Gene Ontology and pathway analysis further confirmed these results. Conclusion: Early-life environment significantly affects both microbial composition of the adult gut and mucosal innate immune function. We observed that a microbiota dominated by lactobacilli may function to maintain mucosal immune homeostasis and limit pathogen colonization.

KW - toll-like receptors

KW - crohns-disease

KW - intestinal microbiota

KW - chemokine expression

KW - hygiene hypothesis

KW - gene-expression

KW - dendritic cells

KW - paneth cells

KW - in-vitro

KW - induction

U2 - 10.1186/1741-7007-7-79

DO - 10.1186/1741-7007-7-79

M3 - Article

SN - 1741-7007

VL - 7

JO - BMC Biology

JF - BMC Biology

M1 - 79

ER -

Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces

Abstract

Keywords

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