Intestinal Immune Development Is Accompanied by Temporal Deviation in Microbiota Composition of Newly Hatched Pigeon Squabs.

Abstract

ABSTRACTIdentifying the interaction between intestinal mucosal immune system development and commensal microbiota colonization in neonates is of paramount importance for understanding how early life events affect resistance to disease later in life. However, knowledge about this interaction during the early posthatch development period in altrices is limited. To fill this gap, samples of intestinal content and tissue were collected from newly hatched pigeon squabs at four time points (days 0, 7, 14, and 21) for microbial community analysis and genome-wide transcriptome profiling, respectively. We show that the first week after hatching seems to be the critical window for ileal microbiota colonization and that a potentially stable microbiota has not yet been well established at 21 days of age. Regional transcriptome differences revealed that the jejunum rather than the ileum plays a crucial role in immunity at both the innate and adaptive levels. In the ileum, temporal deviation in innate immune-related genes mainly occurs in the first week of life and is accompanied by a temporal change in microbiota composition, indicating that the ileal innate mucosal immune system development regulated by microbial colonization occurs mainly in this period. Furthermore, we provide evidence that colonization by Escherichia and Lactobacillus within the first week of life is likely one of the causative factors for the induction of proinflammatory cytokine expression in the ileum. We also demonstrate that cellular adaptive immune responses mediated by Th17 cells following commensal-induced proinflammatory cytokine production in the ileum begin as early as the first week posthatch, but this cellular immunity seems to be less effective in terms of maintaining the inflammatory response balance. Because the induction of high levels of mucosal secretory IgA (SIgA) seems to take approximately 3 weeks, we favor the idea that humoral adaptive immunity might be less active, at least, during the first 2 weeks of life. Our data may help to explain the phenomenon of the occurrence of intestinal infections mainly in the ileum of pigeon squabs during the early posthatch period.IMPORTANCE The pigeon (Columba livia), an altricial bird, is one of the most economically important farmed poultry for table purposes. Identifying the interaction between intestinal mucosal immune system development and commensal microbiota colonization in neonates is of paramount importance for understanding how early life events affect resistance to disease and potential productivity later in life. However, knowledge about this interaction during the early posthatch development period in altricial birds is limited. The study described herein is the first to try to provide insights into this interaction. Our data provide evidence on the mutual relationship between intestinal mucosal immune system development and commensal microbiota colonization in pigeon squabs and may help to explain the phenomenon of the occurrence of intestinal infections mainly in the ileum of pigeon squabs during the early posthatch period.