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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.

SUBMITTER: Mulder IE

PROVIDER: S-EPMC2785767 | biostudies-literature | 2009

REPOSITORIES: biostudies-literature

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

Mulder Imke E IE Schmidt Bettina B Stokes Christopher R CR Lewis Marie M Bailey Mick M Aminov Rustam I RI Prosser James I JI Gill Bhupinder P BP Pluske John R JR Mayer Claus-Dieter CD Musk Corran C CC Kelly Denise D

BMC biology 20091120

<h4>Background</h4>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 proc ...[more]

PMID: 19930542

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Project description:Deep aquifers (up to 2km deep) contain massive volumes of water harboring large and diverse microbial communities at high pressure. Aquifers are home to microbial ecosystems that participate in physicochemical balances. These microorganisms can positively or negatively interfere with subsurface (i) energy storage (CH4 and H2), (ii) CO2 sequestration; and (iii) resource (water, rare metals) exploitation. The aquifer studied here (720m deep, 37°C, 88bar) is naturally oligotrophic, with a total organic carbon content of <1mg.L-1 and a phosphate content of 0.02mg.L-1. The influence of natural gas storage locally generates different pressures and formation water displacements, but it also releases organic molecules such as monoaromatic hydrocarbons at the gas/water interface. The hydrocarbon biodegradation ability of the indigenous microbial community was evaluated in this work. The in situ microbial community was dominated by sulfate-reducing (e.g., Sva0485 lineage, Thermodesulfovibriona, Desulfotomaculum, Desulfomonile, and Desulfovibrio), fermentative (e.g., Peptococcaceae SCADC1_2_3, Anaerolineae lineage and Pelotomaculum), and homoacetogenic bacteria ("Candidatus Acetothermia") with a few archaeal representatives (e.g., Methanomassiliicoccaceae, Methanobacteriaceae, and members of the Bathyarcheia class), suggesting a role of H2 in microenvironment functioning. Monoaromatic hydrocarbon biodegradation is carried out by sulfate reducers and favored by concentrated biomass and slightly acidic conditions, which suggests that biodegradation should preferably occur in biofilms present on the surfaces of aquifer rock, rather than by planktonic bacteria. A simplified bacterial community, which was able to degrade monoaromatic hydrocarbons at atmospheric pressure over several months, was selected for incubation experiments at in situ pressure (i.e., 90bar). These showed that the abundance of various bacterial genera was altered, while taxonomic diversity was mostly unchanged. The candidate phylum Acetothermia was characteristic of the community incubated at 90bar. This work suggests that even if pressures on the order of 90bar do not seem to select for obligate piezophilic organisms, modifications of the thermodynamic equilibria could favor different microbial assemblages from those observed at atmospheric pressure.

Dataset Information

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

Publications

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

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