Abstract
Administration of all-trans retinoic acid (ATRA) to pregnant sows improves developmental defects of Hoxa1–/– fetal pigs, and this study aimed to explore the influence of maternal ATRA administration during pregnancy on gut microbiota of neonatal piglets. Samples of jejunal and ileal meconium of neonatal piglets before suckling were collected including 5 Hoxa1–/– and 20 non-Hoxa1–/– (Hoxa1+/+ and Hoxa1+/−) neonatal piglets from the control group and 5 Hoxa1–/– and 7 non-Hoxa1–/– neonatal piglets from the experimental group. Results indicated that Hoxa1 mutation shaped the bacterial composition of the jejunum and ileum of neonatal piglets and Hoxa1–/– neonatal piglets had significantly higher diversity and species richness, higher relative abundance of phylum Bacteroidetes, lower relative abundances of phylum Firmicutes and genus Lactobacillus, and lower ratio of Firmicutes to Bacteroidetes than non-Hoxa1–/– neonatal piglets. After maternal ATRA administration, Hoxa1–/– neonatal piglets had significantly higher diversity and species richness, higher relative abundances of two bacterial phyla (Bacteroidetes and Proteobacteria), and lower relative abundances of phylum Firmicutes and genus Lactobacillus in the jejunum than non-Hoxa1–/– neonatal piglets. Hoxa1–/– neonatal piglets delivered by sows with maternal ATRA administration had lower diversity and species richness and higher relative abundance of phylum Firmicutes in the jejunum than Hoxa1–/– neonatal piglets born by sows with no maternal ATRA administration. Non-Hoxa1–/– neonatal piglets delivered by sows with maternal ATRA administration had higher diversity and species richness and significantly lower relative abundances of phyla Firmicutes and Actinobacteria and genus Lactobacillus in the ileum than non-Hoxa1–/– neonatal piglets born by sows with no maternal ATRA administration. Hoxa1 mutation decreased the expression of bacterial genes involved in ABC transporters, purine metabolism, and aminoacyl-tRNA biosynthesis and increased the expression of bacterial genes involved in two-component system, starch and sucrose metabolism, and arginine and proline metabolism. Maternal ATRA administration decreased the expression of bacterial genes involved in arginine and proline metabolism, peptidoglycan biosynthesis, and fatty acid biosynthesis. Hoxa1 mutation resulted in bacterial dysbiosis of the small intestine of Hoaxa1–/– neonatal piglets, and maternal ATRA administration restored the bacterial dysbiosis of Hoxa1–/– neonatal piglets and altered the bacterial composition of the small intestine of non-Hoxa1–/– neonatal piglets.
Highlights
Gut microbiota is integral to feed digestion, nutrient absorption and metabolism, immune response, and gastrointestinal development (Morgavi et al, 2015), and the colonization of intestinal microbiota during early life could further influence the subsequent microbiota of adult host (Ben Salem et al, 2005)
The data in our study indicated that decreasing the number and alpha diversity of small intestinal bacterial community is beneficial to the neonatal piglets, because Hoxa1−/− neonatal piglets delivered by sows with all-trans retinoic acid (ATRA) administration during pregnancy had lower number and alpha diversity of small intestinal bacterial community, heavier birth live weight, and less symptom with dyspnea than Hoxa1−/− neonatal piglets born by sows with no ATRA administration
It is reported that the composition of intestinal bacterial communities in human and other mammals after suckling is mainly dominated by the phyla Firmicutes and Bacteroidetes, followed by the phyla Proteobacteria, Actinobacteria, and Verrucomicrobia (Gill et al, 2006; Duncan et al, 2008; Ley et al, 2008); the compositions of bacteria in the meconium of fetal bovine and lamb delivered by cesarean section were primarily composed of the phyla Proteobacteria and Firmicutes instead of Firmicutes and Bacteroidetes (Bi et al, 2021; Husso et al, 2021), and data in our study indicated that Firmicutes and Proteobacteria were the most abundant phyla in the meconium of vaginal-delivered neonatal piglets before suckling
Summary
Gut microbiota is integral to feed digestion, nutrient absorption and metabolism, immune response, and gastrointestinal development (Morgavi et al, 2015), and the colonization of intestinal microbiota during early life could further influence the subsequent microbiota of adult host (Ben Salem et al, 2005). Many studies demonstrated that the intestine of prenatal animals really has microorganism (Alipour et al, 2018; Stinson et al, 2019; Hummel et al, 2020; Bi et al, 2021; Husso et al, 2021), and at present, no literature on the differences in intestinal microbiota composition between mutant and wild-type fetuses is found, but for postnatal individuals, there are differences in gut microbiota between mutant and wild-type host, for example, nucleotide-binding oligomerization domain-containing protein 2 (NOD2) mutation caused Crohn’s disease (CD) (Hampe et al, 2001; Ogura et al, 2001) and Crohn’s disease individuals had lower bacterial diversity than healthy controls (Joossens et al, 2011). Our previous studies demonstrated that maternal administration with ATRA at the level of 4 mg/kg body weight on 14 dpc had the best effects in repairing ear defects of Hoxa1−/− fetal pigs, and the aims of this study are (1) to find out if maternal administration with ATRA can alter the intestinal bacterial compositions of Hoxa1−/− and non-Hoxa1−/− fetal piglets and (2) to compare the differences in intestinal bacterial compositions of neonate piglets between Hoxa1−/− and nonHoxa1−/− genotypes
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