Abstract

The objective of this study was to elucidate the impacts of irregular eating patterns on gut microbiota and transcriptomic responses in a pig model with different feeding regimens. The experiment involved 24 growing pigs (Duroc × Landrace × Large White, 48 days of age) which were randomly allocated to one of three feeding patterns: one-meal (M1), three-meals (M3), or five-meals (M5) per day with the same daily feed intake. The results showed that different feeding frequencies had no significant effects on the microbial composition of ileal digesta, colonic digesta, colon mucosa, as well as the concentration of SCFAs in colonic digesta. Mucosa transcriptomic profiling data showed the pathways related to vitamin metabolism were enriched in the ileum and colon of pigs in the pairwise comparison between M3 and M1 groups. On the other hand, the pathways related to lipid metabolism were enriched in the ileum and colon of pigs in the pairwise comparison between M5 and M1 groups. Lastly, the pathways related to protein metabolism were enriched in the colon in the pairwise comparison between M3 and M1 groups, M5 and M1 groups, M5 and M3 groups, while the ileum was not enriched. Differentially expressed genes (DEG) related to metabolism showed that carbohydrate transport was suppressed in the ileum and enhanced in the colon in M5 and M3 groups compared with the M1 group. Compared with the M3 group, carbohydrate transport in the ileum was enhanced in the M5 group, while in the colon was inhibited. With the increase of feeding frequency, the catabolism, biosynthesis, and transport of lipid in the ileum were suppressed, while those in the colon were enhanced. Compared with the M1 group, amino acid transport in the ileum and colon in the M3 group was enhanced. Amino acid catabolism in the ileum in the M5 group was enhanced compared with M1 and M3 groups. In summary, different feeding frequencies affected the transport of carbohydrate, lipid, and amino acid in the ileum and colon, and affected the catabolism and biosynthesis of lipid in the ileum and colon with a low impact on intestinal microbiota.

Highlights

  • With the pace of life accelerated, eating habits become increasingly diverse, such as skipping breakfast and/or late-night eating, increasing the risk of obesity and metabolic diseases, which have attracted the attention of those in the public health field, and effective medicine or approaches are needed to prevent and treat [1, 2]

  • At the biological process level, most of the DEGs in the colon mucosa were significantly represented in the term of regulation of system process in the pairwise comparison between M3 and M1 groups, the term of negative regulation of molecular function in the pairwise comparison between M5 and M1 groups, and the terms of circulatory system development, animal organ morphogenesis, and anatomical structure formation involved in morphogenesis in the pairwise comparison between M5 and M3 groups

  • High-throughput sequencing technology was adapted to investigate the effects of different feeding frequencies per day on gene expression in ileum mucosa and colon mucosa, the microbial composition of ileal digesta, colonic digesta, and colon mucosa, as well as the microbial metabolites of colonic digesta of growing pigs

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Summary

Introduction

With the pace of life accelerated, eating habits become increasingly diverse, such as skipping breakfast and/or late-night eating, increasing the risk of obesity and metabolic diseases, which have attracted the attention of those in the public health field, and effective medicine or approaches are needed to prevent and treat [1, 2]. As a part of the strategies to reduce energy intake (diets, drugs, and bariatric surgery) [3] and to increase energy output (exercise and non-exercise movement) [4], meal timing and frequency have an important impact on weight control and weight loss [5, 6]. Researchers are looking for a simple solution to weight loss and decrease their metabolic diseases, and they have recently increased in popularity of low overall feed intake, research on the effects of irregular eating patterns on weight control and metabolism under the condition of an equal amount of feed intake is scarce. Our previous study found different feeding frequencies significantly affected the growth performance of growing pigs with the same feed intake, indicating that meal frequency as a strategy had an important impact on weight control [7]. The underlying mechanism of feeding frequency affecting nutrient digestion and absorption and the possible role of intestine microbiota is unknown

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