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

Research output: Contribution to journalArticle

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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 languageEnglish
Article number79
Number of pages20
JournalBMC Biology
Volume7
DOIs
Publication statusPublished - 20 Nov 2009

Keywords

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

Cite this

Mulder, I. E., Schmidt, B., Stokes, C. R., Lewis, M., Bailey, M., Aminov, R. I., ... Kelly, D. (2009). Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology, 7, [79]. https://doi.org/10.1186/1741-7007-7-79

Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. / Mulder, Imke E; Schmidt, Bettina; Stokes, Chris R; Lewis, Marie; Bailey, Mick; Aminov, Rustam I; Prosser, James I; Gill, Bhupinder P; Pluske, John R; Mayer, Claus-Dieter; Musk, Corran C; Kelly, Denise.

In: BMC Biology, Vol. 7, 79, 20.11.2009.

Research output: Contribution to journalArticle

Mulder, IE, Schmidt, B, Stokes, CR, Lewis, M, Bailey, M, Aminov, RI, Prosser, JI, Gill, BP, Pluske, JR, Mayer, C-D, Musk, CC & Kelly, D 2009, 'Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces', BMC Biology, vol. 7, 79. https://doi.org/10.1186/1741-7007-7-79
Mulder, Imke E ; Schmidt, Bettina ; Stokes, Chris R ; Lewis, Marie ; Bailey, Mick ; Aminov, Rustam I ; Prosser, James I ; Gill, Bhupinder P ; Pluske, John R ; Mayer, Claus-Dieter ; Musk, Corran C ; Kelly, Denise. / Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. In: BMC Biology. 2009 ; Vol. 7.
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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.",
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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

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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.

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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

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VL - 7

JO - BMC Biology

JF - BMC Biology

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ER -