Early-life environmental variation affects intestinal microbiota and immune development in new-born piglets

PLoS One. 2014 Jun 18;9(6):e100040. doi: 10.1371/journal.pone.0100040. eCollection 2014.

Abstract

Background: Early-life environmental variation affects gut microbial colonization and immune competence development; however, the timing and additional specifics of these processes are unknown. The impact of early-life environmental variations, as experienced under real life circumstances, on gut microbial colonization and immune development has not been studied extensively so far. We designed a study to investigate environmental variation, experienced early after birth, to gut microbial colonization and intestinal immune development.

Methodology/principal findings: To investigate effects of early-life environmental changes, the piglets of 16 piglet litters were divided into 3 groups per litter and experimentally treated on day 4 after birth. During the course of the experiment, the piglets were kept with their mother sow. Group 1 was not treated, group 2 was treated with an antibiotic, and group 3 was treated with an antibiotic and simultaneously exposed to several routine, but stressful management procedures, including docking, clipping and weighing. Thereafter, treatment effects were measured at day 8 after birth in 16 piglets per treatment group by community-scale analysis of gut microbiota and genome-wide intestinal transcriptome profiling. We observed that the applied antibiotic treatment affected the composition and diversity of gut microbiota and reduced the expression of a large number of immune-related processes. The effect of management procedures on top of the use of an antibiotic was limited.

Conclusions/significance: We provide direct evidence that different early-life conditions, specifically focusing on antibiotic treatment and exposure to stress, affect gut microbial colonization and intestinal immune development. This reinforces the notion that the early phase of life is critical for intestinal immune development, also under regular production circumstances.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Anti-Bacterial Agents / pharmacology
  • Bacterial Typing Techniques
  • Biodiversity
  • Cytokines / genetics
  • Cytokines / immunology*
  • Disaccharides / pharmacology
  • Environment
  • Heterocyclic Compounds / pharmacology
  • Immunity, Innate*
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / microbiology*
  • Microbiota / drug effects
  • Microbiota / immunology*
  • Principal Component Analysis
  • Stress, Physiological
  • Swine
  • Toll-Like Receptors / genetics
  • Toll-Like Receptors / immunology*
  • Transcriptome

Substances

  • Anti-Bacterial Agents
  • Cytokines
  • Disaccharides
  • Heterocyclic Compounds
  • Toll-Like Receptors
  • tulathromycin

Grants and funding

D.S., S.A.V., J.M.J.R., and M.A.S. were supported by the funding of Dutch Ministry of Economic Affairs, Central Veterinary Institute and Wageningen Livestock Research. J.Z. was supported by a fellowship of the China Scholarship Programme, and J.Z., L.Z. and H.S. were partly supported by the European Union through the Interplay project, Grant agreement no. 227549). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.