Examination of the temporal and spatial dynamics of the gut microbiome in newborn piglets reveals distinct microbial communities in six intestinal segments

Abstract

Intestinal microbiota plays a crucial role in immune development and disease progression in mammals from birth onwards. The gastrointestinal tract of newborn mammals is rapidly colonized by microbes with tremendous biomass and diversity. Understanding how this complex of segmental communities evolves in different gastrointestinal sites over time has great biological significance and medical implications. However, most previous reports examining intestinal microbiota have focused on fecal samples, a strategy that overlooks the spatial microbial dynamics in different intestinal segments. Using intestinal digesta from six intestinal segments (duodenum, jejunum, ileum, cecum, colon and rectum) of newborn piglets, we herein conducted a large-scale 16S rRNA gene sequencing-based study to characterize the segmental dynamics of porcine gut microbiota at eight postnatal intervals (days 1, 7, 14, 21, 28, 35, 120 and 180). A total of 4,465 OTUs were obtained and showed that the six intestinal segments could be divided into three parts; in the duodenum-jejunum section, the most abundant genera included Lactobacillus and Bacteroides; in the ileum, Fusobacterium and Escherichia; and in the cecum-rectum section, Prevotella. Although the microbial communities of the piglets were similar among the six intestinal segments on postnatal day 1, they evolved and quickly differentiated at later intervals. An examination of time-dependent alterations in the dominant microbes revealed that the microbiome in the large intestine was very different from and much more stable than that in the small intestine. The gut microbiota in newborn piglets exhibited apparent temporal and spatial variations in different intestinal segments. The database of gut microbes in piglets could be a referable resource for future studies on mammalian gut microbiome development in early host growth phases.

Figure 1

Principal coordinate analysis (PCoA) of all 230 samples based on weighted UniFrac distances among different intestinal segments. (a) The samples in different intestinal segments are colored differentially (duodenum: red, ileum: orange, jejunum: dark read, cecum: dark green, colon: green; rectum: light green). (b) The samples in the small intestine (duodenum, ileum and jejunum) were colored in red, and those in the large intestine (cecum, colon and rectum) are colored in blue.

Figure 2

Weighted UniFrac PCoA of different growth stages. (a) PCoA of all 230 samples according to different growth stages; the points with different colors represent the different samples from postnatal days 1, 7, 14, 21, 28, 35, 120 and 180. (b,c) PCoA of the 113 samples in the small intestine (b) and the 117 samples in the large intestine (c). The colors represent the different time points; 1 day: blue, nursing (postnatal days 7, 14, 21, 28, and 35): red, weaning (postnatal day 120 and day 180): green, Each ‘arrow’, generated according to the centroid of the sampling points at each interval, illustrates the changing trend over time.

Figure 3

Bar plot of the microbial compositions of the top 20 genera among 230 samples. The horizontal axis represents the different samples; the vertical axis represents the relative abundance of the different genera. Different colors represent different bacterial genera.