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.

Post‐natal co‐development of the microbiota and gut barrier function follows different paths in the small and large intestine in piglets

“…Fecal microbiota at PND21 was populated by Lactobacillus (Lactobacillacea), Ruminococcus (Ruminococcaceae), Prevotella (Prevotellaceae), and Rikenella (Rikenellaceae) 45 as observed in the colon at PND28 in our study. 3 This is contrast with our data where we observed a relative stability in the jejunum and ileum microbiota composition up to PND28 but more gradual changes with post-natal age in the colon. 44 Maradiaga et al considered only one time-point (PND21) but different locations (duodenum, jejunum, ileum, and colon).…”

“…Available data are either a time-course of fecal microbiota composition 44,45 or a region-specific description of the microbiota at one specific time-point. 3 The temporal and regional variations that we reported are in line with these published data. 3 The temporal and regional variations that we reported are in line with these published data.…”

“…Lactobacillus appeared in feces at PND7. 3 Similar differences were observed in our study. Similarly Chen et al observed a gradual change in fecal microbiota from PND1 to 21, with a high abundance of Proteobacteria in piglet feces at PND1, transient presence of Fusobacteria at PND3 and a predominance of Firmicutes and Bacteroidetes at PND7 and 21.…”

“…1 Although the small and large intestine originate from the primitive gut during embryonic development, they fulfill different functions, suggesting distinct spatiotemporal developmental differences in morphology and function. Apart from a recent study in piglets, 3 temporal and spatial variations of microbiota in different intestinal segments during the neonatal period are scarce. Indeed, germ-free animals harbor altered mucosa morphology and poorly developed gut immune system and barrier function.…”

Intraepithelial T cells diverge by intestinal location as pigs age

“…Drawing parallels to the current study, intestinal location gave greater dictation to IET community composition than age, though age still had significant influence. In pigs, distinct microbial communities exist between the small and large intestine (62) but also between the jejunum and the ileum of the small intestine (63). Similarly, we detected significant differences in overall IET community compositions not only between the small and large intestine but also between jejunum and ileum.…”