Open Access Highly Accessed Research article

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

Imke E Mulder1, Bettina Schmidt1, Christopher R Stokes2, Marie Lewis2, Mick Bailey2, Rustam I Aminov1, James I Prosser3, Bhupinder P Gill4, John R Pluske5, Claus-Dieter Mayer6, Corran C Musk1 and Denise Kelly1*

Author Affiliations

1 Gut Immunology Group, University of Aberdeen, Rowett Institute of Nutrition and Health, Greenburn Road, Aberdeen AB21 9SB, UK

2 Veterinary Pathology, Infection & Immunity, Langford House, Langford, Bristol, BS40 5DU, UK

3 Institute of Biological and Environmental Sciences, University of Aberdeen, St Machar Drive, Aberdeen AB24 3UU, UK

4 Agricultural and Horticultural Development Board, Winterhill House, Snowdon Drive, Milton Keynes MK6 1AX, UK

5 School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia

6 Biomathematics & Statistics Scotland, University of Aberdeen, Rowett Institute of Nutrition and Health, Greenburn Road, Aberdeen AB21 9SB, UK

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BMC Biology 2009, 7:79  doi:10.1186/1741-7007-7-79

Published: 20 November 2009

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.