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The role of gut microbiota in mediating tissue injury through the promotion of proteolysis and heme bioavailability in the small intestine

ABSTRACT: Background: Excessive meat intake is considered to be associated with multiple intestinal injuries. However, the specific mechanism is still controversial. Results: It was found that pork diet (typical meat diet) only induced small intestinal injury in specific-pathogen free (SPF) mice but not in germ-free (GF) mice, highlighting the indispensable role of gut microbiota in intestinal health. ELISA and RT-qPCR indicated that the intestinal tissue in GF mice had lower levels of heme and Hmox1 compared with the SPF mice, suggesting the low bioavailability of myoglobin without symbiotic microbes. High throughput sequencing showed that dietary myoglobin and heme effected intestinal flora diversity, with Lactobacillus, Muribaculaceae and Bifidobacterium being enriched by myoglobin. Additionally, the enrichment of protease and peptidase by myoglobin demonstrated the regulated proteolytic capacity of small intestinal microbiota. In contrast with hemoglobin, the degradation of myoglobin and subsequent heme release must be initiated by gastric digestion and ultimately enhanced by gut microbes under a simulated condition. Peptidomics revealed the peptide-shortening role of gut microbes in digestion. Both the inhibition of gastric digestion by esomeprazole and clearance of gut microbes by amoxicillin hindered heme absorption in mice that were orally administered with myoglobin. Moreover, the incubation of human intestinal epithelial cells (INT 407) with microbial hydrolysate of myoglobin and peptide-heme mixture induced the accumulation of intracellular iron and cell death which were found to be dependent on heme carrier and PEPT1. Inhibitor screening indicated that although utilization and metabolism of free heme was independent of endocytosis, F-actin-mediated endocytosis inhibited the bioavailability of peptide-heme mixture and downregulated ferritin. Conclusions: These findings describe the direct role of small intestinal microbes in host digestion and give a new insight into the underlying mechanism of bioavailability of dietary myoglobin.

ORGANISM(S): Mus musculus (mouse)

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PROVIDER: S-BSST1056 | biostudies-other |

SECONDARY ACCESSION(S): PRJNA948118

REPOSITORIES: biostudies-other

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Project description:BackgroundIntestinal disorder is an important factor contributing to growth lag and high rates of morbidity and mortality of piglets with intrauterine growth retardation (IUGR). Resveratrol (RSV) and its derivative pterostilbene (PT) are natural stilbenes possessing various bioactivities, such as antioxidative and anti-inflammatory effects. This study compared the protective potential of RSV and PT on the intestinal redox status and gut microbiota in weanling piglets with IUGR.MethodsEighteen male piglets of normal body weight (NBW) and 54 same-sex IUGR piglets were chosen according to their birth and weaning weights. The NBW piglets accepted a basal diet, while the IUGR piglets were allotted to one of three groups according to their body weight at weaning and received a basal diet, an RSV-supplemented diet (300 mg/kg), or a PT-supplemented diet (300 mg/kg), respectively.ResultsCompared with IUGR piglets, both RSV and PT improved the IUGR-associated decrease in jejunal villus height and increases in plasma diamine oxidase activity and D-lactate level and jejunal apoptosis of piglets (P < 0.05). Administering RSV and PT also enhanced jejunal superoxide dismutase activity and the mRNA and protein expression of superoxide dismutase 2 of IUGR piglets by promoting nuclear factor erythroid 2-related factor 2 (Nrf2) nuclear translocation (P < 0.05). Comparatively, PT was more effective than RSV in elevating the villus height/crypt depth ratio and occludin mRNA and protein levels in the jejunum of IUGR piglets (P < 0.05). PT was also superior to RSV in increasing Nrf2 nuclear translocation and inhibiting malondialdehyde accumulation in the jejunum of IUGR piglets (P < 0.05). Additionally, RSV modulated the composition of cecal microbiota of IUGR piglets, as evidenced by increasing the prevalence of the phylum Bacteroidetes and the genera Prevotella, Faecalibacterium, and Parabacteroides and inhibiting the growth of the phylum Proteobacteria and its genera Escherichia and Actinobacillus (P < 0.05). Moreover, RSV significantly increased the butyrate concentration in the cecum of IUGR piglets (P < 0.05).ConclusionPT is more potent than RSV to prevent intestinal oxidative stress, while RSV has a stronger capacity to regulate gut microbiota compared to PT.

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The role of gut microbiota in mediating tissue injury through the promotion of proteolysis and heme bioavailability in the small intestine

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