Inheritance and Establishment of Gut Microbiota in Chickens

Abstract

In mammals, the microbiota can be transmitted from the placenta, uterus, and vagina of the mother to the infant. Unlike mammals, development of the avian embryo is a process isolated from the mother and thus in the avian embryo the gut microbial developmental process remains elusive. To explore the establishment and inheritance of the gut microbiome in the avian embryo, we used the chicken as the model organism to investigate the gut microbial composition in embryos, chicks, and maternal hens. We observed: (1) 28 phyla and 162 genera of microbes in embryos where the dominated genus was Halomonas (79%). (2) 65 genera were core microbiota in all stages with 42% and 62% gut microbial genera of embryo were found in maternal hen and chick, respectively. There was a moderate correlation (0.40) between the embryo and maternal, and 0.52 between the embryo and chick at the family level. (3) Gut microbes that are involved in substance metabolism, infectious disease, and environmental adaptation are enriched in embryos, chicks, and maternal hens, respectively. (4) 94% genera of gut microbial composition were similar among three different chicken breeds which were maintained under similar conditions. Our findings provide evidence to support the hypothesis that part of the microbial colonizers harbored in early embryos were inherited from maternal hens, and the gut microbial abundance and diversity were influenced by environmental factors and host genetic variation during development.

Keywords: 16S rRNA; chicken; establishment; gut microbiota; inheritance.

FIGURE 1

Aggregate microbiota characteristics of 4-day (E4) and 19-day (E19) embryos. (A) Dominant taxonomic groups of embryos by phylum. (B) Microbial beta diversity of embryos with a Non-metric Multidimensional Scaling (NMDS) plot showing how distant E4 and E19 communities were. (C) Microbial alpha diversity with a box plot exhibiting the community diversity (The Shannon estimator). (D) Heatmap of hierarchy cluster results for the statistical significant microbial OTUs of two groups at the genus level.

FIGURE 2

Phylogenetic tree of the taxa and differences in the microbial communities of different development stages. (A) Phylogenetic tree constructed from the 188 taxa. Colored blocks in the outermost circle indicate phyla, and in the inner circle indicate genera. The heatmap circles show relative abundance of embryos (E) E4 and E19; chicks (L) at 4 (L4), 21 (L21), and 42 days (L42) post hatch; and maternal hens (H). (B) The Venn diagram shows the microbes shared within different host development stages (see Supplementary Table S3 in the Supplementary Material). (C) Microbial composition structure of embryos, chicks, and maternal hens at the genus level.

FIGURE 3

The dynamic distribution of main core microbes within different host development stages including embryos (E) E4 and E19; chicks (L) at 4 (L4), 21 (L21), and 42 days (L42) post hatch; and maternal hens (H) based on microbial abundance. The boxes have lines at the lower quartile, median, and upper quartile values.

FIGURE 4

Significant differences in microbial metabolic pathways at different stages. Extended error bar plot indicates the difference in mean proportion of microbial metabolic pathways between the two groups along with the associated confidence interval of this effect size and the p-value of Welch’s t-test (p < 0.05). (A) Embryo vs. chick. (B) Embryo vs. maternal hen. (C) Chick vs. maternal hen.

FIGURE 5

Microbiota compositions for Beijing Fatty (B), Shiqiza (C), and Xianju (X) of chickens within different host development stages including embryos (E) E4 and E19; chicks (L) at 4 (L4), 21 (L21), and 42 days (L42) post hatch; and maternal hens (H).