Gut microbial metabolism of dietary fibre protects against high energy feeding induced ovarian follicular atresia in a pig model

Zhuo, Yong; Cao, Meng; Gong, Yuechan; Tang, Lianchao; Jiang, Xin; Li, Yang; Yang, Min; Xu, Shengyu; Li, Jian; Che, Lianqiang; Lin, Yan; Feng, Bin; Fang, Zhengfeng; Wu, De

doi:10.1017/s0007114520002378

Cited by 21 publications

(37 citation statements)

References 78 publications

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“…Recently, a considerable amount of reference highlighted the contributions of the type, quantity, and composition of nutrients intake to host health and metabolism both on animals and human beings (1)(2)(3)(4). By contrast, there are fewer studies concerning the effects of feeding patterns on health and metabolism.…”

Section: Introductionmentioning

confidence: 99%

Metabolome-Microbiome Responses of Growing Pigs Induced by Time-Restricted Feeding

Wang

Xia

et al. 2021

Front. Vet. Sci.

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Time-restricted feeding (TRF) mode is a potential strategy in improving the health and production of farm animals. However, the effect of TRF on microbiota and their metabolism in the large intestine of the host remains unclear. Therefore, the present study aimed to investigate the responses of microbiome and metabolome induced by TRF based on a growing-pig model. Twelve crossbred growing barrows were randomly allotted into two groups with six replicates (1 pig/pen), namely, the free-access feeding group (FA) and TRF group. Pigs in the FA group were fed free access while the TRF group were fed free access within a regular time three times per day at 07:00–08:00, 12:00–13:00, and 18:00–19:00, respectively. Results showed that the concentrations of NH4-N, putrescine, cadaverine, spermidine, spermine, total biogenic amines, isobutyrate, butyrate, isovalerate, total SCFA, and lactate were increased while the pH value in the colonic digesta and the concentration of acetate was decreased in the TRF group. The Shannon index was significantly increased in the TRF group; however, no significant effects were found in the Fisher index, Simpson index, ACE index, Chao1 index, and observed species between the two groups. In the TRF group, the relative abundances of Prevotella 1 and Eubacterium ruminantium group were significantly increased while the relative abundances of Clostridium sensu sticto 1, Lactobacillus, and Eubacterium coprostanoligenes group were decreased compared with the FA group. PLS-DA analysis revealed an obvious and regular variation between the FA and TRF groups, further pathway enrichment analysis showed that these differential features were mainly enriched in pyrimidine metabolism, nicotinate and nicotinamide metabolism, glycerolipid metabolism, and fructose and mannose metabolism. In addition, Pearson's correlation analysis indicated that the changes in the microbial genera were correlated with the colonic metabolites. In conclusion, these results together indicated that although the overall microbial composition in the colon was not changed, TRF induced the gradient changes of the nutrients and metabolites which were correlated with certain microbial genera including Lactobacillus, Eubacterium_ruminantium group, Eubacterium coprostanoligenes group, Prevotella 1, and Clostridium sensu sticto 1. However, more studies are needed to understand the impacts of TRF on the health and metabolism of growing pigs.

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Section: Introductionmentioning

confidence: 99%

Metabolome-Microbiome Responses of Growing Pigs Induced by Time-Restricted Feeding

Wang

Xia

et al. 2021

Front. Vet. Sci.

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“…Along with the colonic contents, levels of acetate, propionate and butyrate SCFAs in faecal samples at 30 d of the experiment and at 19 d of the 2nd oestrous cycle were determined using a Varian CP-3800 gas chromatograph (manual injection, flame ionisation detector, 10 μL microinjector; Varian), as previously described [ 13 ]. Microbial diversity in faeces at 19 d of the 2nd oestrous cycle was measured using high-throughput pyrosequencing (16S rRNA analysis).…”

Section: Methodsmentioning

confidence: 99%

“…Additionally, SCFAs can be taken up by peripheral tissues such as the stomach, intestine, liver, adipocytes and skeletal muscle, making it difficult for them to reach threshold concentrations to activate downstream targets [ 11 , 12 ]. Peripheral tissues in turn detect metabolites and respond accordingly by secreting secondary metabolic hormones such as serotonin [ 13 ]. However, it remains unclear which metabolites or metabolic hormones are involved in controlling the reproductive functions of replacement gilts.…”

Section: Introductionmentioning

confidence: 99%

Microbial and metabolomic mechanisms mediating the effects of dietary inulin and cellulose supplementation on porcine oocyte and uterine development

Men

Cao

Gong

et al. 2022

J Animal Sci Biotechnol

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Background Dietary fiber (DF) is often eschewed in swine diet due to its anti-nutritional effects, but DF is attracting growing attention for its reproductive benefits. The objective of this study was to investigate the effects of DF intake level on oocyte maturation and uterine development, to determine the optimal DF intake for gilts, and gain microbial and metabolomic insight into the underlying mechanisms involved. Methods Seventy-six Landrace × Yorkshire (LY) crossbred replacement gilts of similar age (92.6 ± 0.6 d; mean ± standard deviation [SD]) and body weight (BW, 33.8 ± 3.9 kg; mean ± SD) were randomly allocated to 4 dietary treatment groups (n = 19); a basal diet without extra DF intake (DF 1.0), and 3 dietary groups ingesting an extra 50% (DF 1.5), 75% (DF 1.75), and 100% (DF 2.0) dietary fiber mixture consisting of inulin and cellulose (1:4). Oocyte maturation and uterine development were assessed on 19 d of the 2nd oestrous cycle. Microbial diversity of faecal samples was analysed by high-throughput pyrosequencing (16S rRNA) and blood samples were subjected to untargeted metabolomics. Results The rates of oocytes showing first polar bodies after in vitro maturation for 44 h and uterine development increased linearly with increasing DF intake; DF 1.75 gilts had a 19.8% faster oocyte maturation rate and a 48.9 cm longer uterus than DF 1.0 gilts (P < 0.05). Among the top 10 microbiota components at the phylum level, 8 increased linearly with increasing DF level, and the relative abundance of 30 of 53 microbiota components at the genus level (> 0.1%) increased linearly or quadratically with increasing DF intake. Untargeted metabolic analysis revealed significant changes in serum metabolites that were closely associated with microbiota, including serotonin, a gut-derived signal that stimulates oocyte maturation. Conclusions The findings provide evidence of the benefits of increased DF intake by supplementing inulin and cellulose on oocyte maturation and uterine development in gilts, and new microbial and metabolomic insight into the mechanisms mediating the effects of DF on reproductive performance of replacement gilts.

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“…The area of the HE-stained sections was estimated with Image-Pro Plus for Windows 6.0 (Media Cybernetics, Maryland, MD, USA). The number of follicles at each stage was normalized by the area of HE-stained ovarian tissue in the sections and is presented as the number of follicles per cm 2 as previously described [ 18 ].…”

Section: Methodsmentioning

confidence: 99%

Beneficial effects of a decreased meal frequency on nutrient utilization, secretion of luteinizing hormones and ovarian follicular development in gilts

Hua

Zhao

Mao

et al. 2021

J Animal Sci Biotechnol

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Background Replacement gilts are typically fed ad libitum, whereas emerging evidence from human and rodent studies has revealed that time-restricted access to food has health benefits. The objective of this study was to investigate the effect of meal frequency on the metabolic status and ovarian follicular development in gilts. Methods A total of 36 gilts (Landrace × Yorkshire) with an age of 150±3 d and a body weight of 77.6±3.8 kg were randomly allocated into one of three groups (n = 12 in each group), and based on the group allocation, the gilts were fed at a frequency of one meal (T1), two meals (T2), or six meals per day (T6) for 14 consecutive weeks. The effects of the meal frequency on growth preference, nutrient utilization, short-chain fatty acid production by gut microbial, the post-meal dynamics in the metabolic status, reproductive hormone secretions, and ovarian follicular development in the gilts were measured. Results The gilts in the T1 group presented a higher average daily gain (+ 48 g/d, P < 0.05) and a higher body weight (+ 4.9 kg, P < 0.05) than those in the T6 group. The meal frequency had no effect on the apparent digestibility of dry matter, crude protein, ether extract, ash, and gross energy, with the exception that the T1 gilts exhibited a greater NDF digestibility than the T6 gilts (P < 0.05). The nitrogen balance analysis revealed that the T1 gilts presented decreased urine excretion of nitrogen (− 8.17 g/d, P < 0.05) and higher nitrogen retention (+ 9.81 g/d, P < 0.05), and thus exhibited higher nitrogen utilization than the T6 gilts. The time-course dynamics of glucose, α-amino nitrogen, urea, lactate, and insulin levels in serum revealed that the T1 group exhibited higher utilization of nutrients after a meal than the T2 or T6 gilts. The T1 gilts also had a higher acetate content and SCFAs in feces than the T6 gilts (P < 0.05). The age, body weight and backfat thickness of the gilts at first estrous expression were not affected by the meal frequency, but the gilts in the T1 group had higher levels of serum luteinizing hormone on the 18th day of the 3rd estrus cycle and 17β-estradiol, a larger number of growing follicles and corpora lutea, and higher mRNA expression levels of genes related to follicular development on the 19th day of the 3rd estrus cycle. Conclusions The current findings revealed the benefits of a lower meal frequency equal feed intake on nutrient utilization and reproductive function in replacement gilts, and thus provide new insights into the nutritional strategy for replacement gilts, and the dietary pattern for other mammals, such as humans.

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Gut microbial metabolism of dietary fibre protects against high energy feeding induced ovarian follicular atresia in a pig model

Cited by 21 publications

References 78 publications

Metabolome-Microbiome Responses of Growing Pigs Induced by Time-Restricted Feeding

Metabolome-Microbiome Responses of Growing Pigs Induced by Time-Restricted Feeding

Microbial and metabolomic mechanisms mediating the effects of dietary inulin and cellulose supplementation on porcine oocyte and uterine development

Beneficial effects of a decreased meal frequency on nutrient utilization, secretion of luteinizing hormones and ovarian follicular development in gilts

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