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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. * Correspondence: firstname.lastname@example.org Zhaoyue Men, Meng Cao and Yuechan Gong contributed equally to this work. Animal Nutrition Institute, Sichuan Agricultural University, 211 Huimin Road, Wenjiang District, Chengdu 611130, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2022 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 2 of 16 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. Keywords: Dietary fiber, Gilts, Metabolomics, Microbiota, Oocyte maturation Background Indeed, DF is generally defined as a carbohydrate that Dietary fiber (DF) is often excluded from animal feed is neither absorbed nor hydrolysable by mammalian en- due to its anti-nutritional properties during nutrient di- dogenous digestive enzymes. Although DF is gradually gestion in monogastric nutrition [1, 2]. However, DF re- considered as an essential nutrient for normal gastro- portedly benefits swine production, including improving intestinal tract physiology and overall health of both hu- the welfare of gestating sows fed a restricted diet . In man and domestic animals, there have been different recent decades, the inclusion of DF in the diets of re- methods for the quantification of DF within feeds/foods placement gilts has received growing attention due to its for both animal and human nutrition [14, 15]. “Crude beneficial effects on reproductive performance. Gilts fed fiber” (CF) was one of the earliest parameters to describe a fiber-rich diet by adding high levels of sugar beet pulp the DF, and later the Van Soest method was introduced 19 d prior to breeding displayed greater embryo survival to classify the DF into neutral detergent fiber (NDF), (88.2%) at 28 d of pregnancy than controls (80.0%), while acid detergent fiber (ADF), and acid detergent lignin increasing the feeding level (from 1.8 × maintenance to (ADF) in animal nutrition . More recently, a simple 2.6 × maintenance), starch (+ 451 g/d) or protein (+ 158 classification of DF was introduced with enzymatic- g/d) did not improve embryonic survival . Further- gravimetric method, which allows the categorization of more, this beneficial effect of high DF prior to mating DF into “soluble” or “insoluble” based on the ability to on the survival of early embryos acted by improving the be fully dispersed with water . Soluble fiber has gen- quality of oocytes . However, feeding replacement erally a high affinity in the water, and is easily hydro- gilts a lupin-based high-fiber diet, but not a wheat bran- lyzed by the carbohydrate-active enzymes secreted by based diet, accelerated oocyte maturation , adding the microbiota in the gut, whereas insoluble fiber was complexity to the effects of DF on the reproductive out- less fermentable . Additionally, the DF benefits could comes of gilts. Most previous researches on the effects be attributed to its different physical characteristics such of fiber have explored high levels of fiber-rich ingredi- as water-holding capacity, viscosity, absorptive capacity, ents such as sugar beet pulp. However, other nutrients and faecal bulking capacity, as well as chemical charac- (e.g., vitamins) complicate the direct effects of DF. Add- teristic fermentability . Insoluble fibers (e.g. cellu- ing extracted forms of fiber such as inulin, cellulose and lose) usually related to water-holding capacity, pectin allows the direct evaluation of the effect of DF absorptive capacity, and faecal bulking capacity, while [7–10]. Recently, we investigated the effects of different soluble fibers (e.g. inulin) usually contributed to viscosity levels of DF intake on the ovarian follicle reserve of gilts and fermentability . This leads us to hypothesize that , but the optimal level of dietary fiber for oocyte mat- a combination of both soluble and insoluble fiber could uration and uterine development in gilts of mating age optimize the effects of DF. The objective of this study remains unknown. was to investigate the effects of different DF levels by As mentioned above, some of the beneficial effects of supplementing inulin and cellulose to the diets of grow- DF on reproductive performance have been elucidated, ing gilts on oocyte quality and uterine development. We but the underlying mechanism remains largely uncertain. also probed changes in microbial diversity, performed DF is usually mobilised by gut microbiota to generate metabolomic profiling based on 16S rRNA analysis, and short-chain fatty acids (SCFAs) such as acetate, propion- conducted untargeted metabolic pathway analysis. ate and butyrate . Additionally, SCFAs can be taken up by peripheral tissues such as the stomach, intestine, Materials and methods liver, adipocytes and skeletal muscle, making it difficult This trial was conducted at the research centre of Si- for them to reach threshold concentrations to activate chuan Agricultural University. Procedures were per- downstream targets [11, 12]. Peripheral tissues in turn formed in accordance with the National Research detect metabolites and respond accordingly by secreting Council Guide for the Care and Use of Laboratory Ani- secondary metabolic hormones such as serotonin . mals, and followed the regulations of the Animal Care However, it remains unclear which metabolites or meta- and Use Committee of Sichuan Agricultural University bolic hormones are involved in controlling the repro- (Approval No. 20174310). ductive functions of replacement gilts. Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 3 of 16 Animals, diets and experimental design contained 72.0% corn, 20.8% soybean meal, 2.5% fish- This was a companion trial of our recent study . meal, and 2.0% soybean meal to provide 3.4 Mcal/kg of Seventy-six Landrace × Yorkshire (LY) crossbred re- digestible energy, 16.9% of crude protein, and 1.08% of placement gilts of similar age (92.6 ± 0.6 d; mean ± SD) total lysine. The diet from 61 d to the end of experiment and body weight (33.8 ± 3.9 kg; mean ± SD) were used in contained 78.0% corn, 16.0% soybean meal, 2.0% fish- this study. Gilts were randomly allocated to 4 dietary meal, and 1.7% soybean meal to provide 3.4 Mcal/kg of treatment groups (n = 19); a basal diet without extra DF digestible energy, 14.7% of crude protein, and 0.86% of intake (DF 1.0), and 3 dietary groups with 3 different total lysine. The soluble and insoluble fibers in basal di- levels of extra DF intake. Basal diets were divided into 2 ets were analysed by enzymatic-gravimetric method with phases; 1 to 60 d (72.0% corn, 20.8% soybean) and 61 d minor modification . Briefly, feed samples (1.0 g) to the end of the experiment (78.0% corn, 16.0% soy- were treated with a 40-mL MES-TRIS buffer solution bean), respectively. The detailed diet formulation was (Sigma-Aldrich, Saint Louis, USA) on a stirrer. The shown in Table 1. The diet from 1 to 60 d of experiment heat-stable α-amylase solution (50 μL, A3306, Sigma- Aldrich) was added to the mixture and then incubated in a 95–100 °C water bath for 15 min with continuous Table 1 Ingredients and nutrient compositions of basal diets (as agitation. The protease solution (P3910, Sigma-Aldrich) fed basis), g/kg were then added for 30 min at 60 °C. Additional 300 μL Ingredients, g/kg Phases of experiment amyloglucosidase solution (A9913, Sigma-Aldrich) was 1–60 d 61 d–slaughter added to the solution for 30 min at 60 °C after adjusting Corn 720 780 pH to 4.0–4.7. After hydrolysis, the insoluble fiber resi- Soybean (44%CP) 208 160 due was obtained by filtration on a crucible with acid Fish meal (65%CP) 25 20 washed wet and redistribute Celite (C8656, Sigma- Aldrich), and the filtrate was collected by adding 95% Soybean oil 20 17 ethanol prewarmed at 60 °C to form the SDF precipitate. L-Lys HCl (98%) 3 2 Total DF were calculated with sum of soluble fiber and DL-Met (99%) 1 0.4 insoluble fiber. The total DF in basal diets were 12.52% L-Thr (98%) 0.6 0.2 (d 1 to 60 of experiment) and 12.42% (d 61 to the end of L-Trp (98%) 0.1 0 experiment), respectively. DF 1.0 gilts were provided Choline chloride (50%) 1.5 1.5 with 1.6, 2.1, 2.5 and 2.8 kg/d of basal diet and estimated total DF intake from diets was 200.3, 262.9, 310.5 and Sodium chloride (feed grade, > 99.0%) 4 4 347.8 g/d from 1 to 30 d, 31 to 60 d, 61 to 120 d, and Limestone 6.2 5.9 121 d to the end of the experiment, respectively. During Monocalcium phosphate 8.6 7 each feeding phase, gilts were fed a basal diet supple- Vitamin-mineral premix 22 mented with 50% (DF 1.5), 75% (DF 1.75) and 100% (DF Total 1000 1000 2.0) extra DF compared with gilts in the DF 1.0 group Nutrient composition, g/kg (Fig. 1). Equal amounts of feed were provided to gilts twice daily at 08:00 and 14:30 h. Extracted DF inulin and Digestible energy, Mcal/kg 3.4 3.4 cellulose were composed of a 1:4 ratio, and this ratio Crude protein 169.1 147.2 was formulated as previously described [7, 8, 10]. All Total Lysine 10.8 8.6 gilts were individually housed in a pen (2.0 m × 0.8 m) in SID Lysine 9.8 7.8 Calcium 6.9 5.9 Total phosphorus 5.9 5.3 Soluble fiber 10.2 10.3 Insoluble fiber 115.0 113.9 Total dietary fiber 125.2 124.2 Provided the following per kilogram of basal diet: 8000 IU vitamin A; 800 IU vitamin D ; 30 IU vitamin E; 4 mg vitamin K; 0.16 mg biotin; 2 mg folacin; 25 Fig. 1 Schematic diagram of the experimental design. Two basal mg niacin; 20 mg pantothenic acid; 10 mg riboflavin; 2 mg thiamine; 1 mg diets were formulated during 1 to 60 d and 61 d to the end of the vitamin B ;20 μg vitamin B ; 16 mg copper as as copper sulfate; 0.25 mg 6 12 experiment. Gilts were fed a basal diet, or a basal diet with three iodine as potassium iodide; 125 mg iron as ferrous sulphate; 30 mg levels of extra dietary fiber (DF) during each phase. DF 1.0, basal diet manganese as manganese sulfate; 0.25 mg selenium as sodium selenite; 125 mg zinc as zinc sulfate without DF supplement, and DF 1.5, DF 1.75, and DF 2.0 were basal Total dietary fiber = soluble fiber + insoluble fiber, analyzed value according diets with an additional 50%, 75% and 100% DF, respectively. The to method AOAC 991.43 DF mixture comprised inulin and cellulose at a ratio of 1:4 Gilts were slaughtered at the 19th day of 3rd estrous cycle Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 4 of 16 a breeding facility with an environmental temperature collected under a stereo microscope (Olympus, Japan), maintained between 20 °C and 24 °C. Water was pro- and only those with uniform oocyte cytoplasm and at vided ad libitum. The onset of first puberty and the 2nd least 2 layers of cumulus cells were selected for culture oestrous cycle were carefully checked in order to collect and maturation in vitro. Follicular fluid was harvested by ovarian samples on 19 d of the 2nd oestrous cycle . centrifuging at 3000 × g at 4 °C and stored at − 20 °C for future analysis. The in vitro maturation medium was Sample collection based on TCM199 medium, which was supplemented Blood samples were collected from gilts at 2 h after the with 0.1% polyvinyl alcohol (Sigma), 10% porcine follicu- morning meal at both 30 d of the experiment and 19 d lar fluid (from COCs with a diameter ≥ 3 mm), 3.05 of the 2nd oestrous cycle. Blood samples were centri- mmol/L D-glucose (Sigma), 0.91 mmol/L sodium pyru- fuged at 3000 × g at 4 °C for 30 min to collect serum, vate (Sigma), 1× Penicillin-Streptomycin solution and stored at − 20 °C for future analysis. (Sigma), 0.57 mmol/L Cysteine (Sigma), 15 U/mL LH Faecal samples were randomly collected (n = 8 per (Prospec, Israel), 15 U/mL FSH (Prospec) and 10 ng/mL group) at 30 d of the experiment and at 19 d of the 2nd EGF (Prospec). Cumulus cell expansion was measured oestrous cycle. Defecation was promoted by rectal after 22 h of culture in vitro by determining the expan- stimulation and faeces were collected immediately, sion of cumulus cells surrounding oocytes using the fol- transferred into sterile tubes with a sterile cotton swab lowing scoring scheme: Score 0, no expansion of pre-wetted with ice-cold sterile phosphate-buffered sa- cumulus cells; Score 1, a slight expansion of the outer line (PBS, pH 7.2), immediately snap-frozen in liquid N , layer of cumulus cells; Score 2, expansion of the outer and stored at − 80 °C. All contacts with faeces were kept two-to-three layers of cumulus cells; Score 3, expansion sterile during the entire sampling procedure to avoid of 50% of cumulus cells; Score 4, full expansion of contamination. cumulus cells. Finally, evaluation of cumulus expansion Collection of reproductive organs was performed at 2 was calculated by the following equation: rate of cumu- time points. At 30 d of the experiment, 24 gilts (6 gilts lus expansion (%) =[ total scores of COCs per gilt / (the per group) were randomly chosen for harvesting bilateral number of COCs × 4)] × 100%. Next, cumulus cells ovaries 2 h after the morning meal under anaesthesia. were removed from COCs by gentle vortexing in 0.1% Cumulus-oocyte complex (COC) and follicular fluid hyaluronidase (Sigma) in TCM 199 after in vitro mat- samples were also collected from antral follicles (diam- uration for 44 h, and the maturation of oocytes to eter 1–3 mm) on the surface of ovaries, as previously de- metaphase II (MII) at 44 h of culture was evaluated scribed , snap-frozen, and stored at − 80 °C. At 19 d based on the presence of the first polar body as previ- of the 2nd oestrous cycle, another 24 gilts (6 gilts per ously described [18, 19]. group) were slaughtered for collecting ovarian, oviduct and uterine samples. Ovaries were washed with PBS pre- Analysis of SCFAs and microbiota warmed at 39 °C, maintained at 39 °C in TCM199 Along with the colonic contents, levels of acetate, propi- medium (Gibco, USA) containing 0.1% polyvinyl alcohol onate and butyrate SCFAs in faecal samples at 30 d of (Sigma, USA), and transported to the laboratory within the experiment and at 19 d of the 2nd oestrous cycle 1 h after sample collection. Uterus and oviduct samples were determined using a Varian CP-3800 gas chromato- were washed with ice-cooled PBS and dried with sterile graph (manual injection, flame ionisation detector, 10 μL tissue paper, and their weight and length in both direc- microinjector; Varian), as previously described . Mi- tions (left and right) were measured. crobial diversity in faeces at 19 d of the 2nd oestrous Colonic contents at the proximal section were quickly cycle was measured using high-throughput pyrosequenc- transferred to 1.5-mL sterile tubes, washed 3 times with ing (16S rRNA analysis). Detailed procedures were con- ice-cold PBS, and dried with sterile tissue paper. Both ducted as previously described , and they are colonic tissues and contents were snap-frozen in N and presented in the online supplementary methods. stored at − 80 °C. Oocyte maturation in vitro Measurement of serotonin and melatonin COCs collected from follicles with diameters between 3 The concentrations of serotonin (DLD Diagnostika mm and 6 mm at 19 d of the 2nd oestrous cycle were GmbH) and melatonin (IBL #RE54021) in serum and subjected to in vitro maturation to measure their oocyte follicular fluid samples were measured with their re- quality as previously described with minor modifications spective ELISA kits as recently described . Addition- . In brief, COCs were aspirated from large follicles ally, the serotonin content in proximal colon tissues was with a 10-mL syringe equipped with an 18-gauge needle normalised to tissue weight. on a sterile operating table. COCs were carefully Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 5 of 16 Gene expression experiment, 13 gilts remained per group from 31 d of Gene expression in ovarian COCs was investigated by the experiment. Additionally, 9 gilts (4, 2, 2 and 1 in DF real-time PCR. In brief, RNA was extracted with TRIzol 1.5, DF 1.75 and DF 2.0, respectively) were excluded reagent (TaKaRa, Dalian, China) for the synthesis of since they did not show oestrous at 240 days of age. In cDNA using a commercial reverse transcription kit this study, gilts in each treatment group could consume (TaKaRa) was used. A 7900HT Fast Real-Time PCR Sys- their provided feed; therefore, gilts in each group were tem (Thermo Fisher Scientific) with SYBR Green Real- expected to consume similar levels of digestible energy, Time PCR reagent (RR820A, TaKaRa) was used to meas- amino acids, minerals and vitamins, but with different ure mRNA levels. Primers for target genes were bone levels of DF intake. The estimated average daily DF in- morphogenetic protein 15 (BMP15) forward 5′-AGCT take was 284.28 g/d, 420.92 g/d, 494.91 g/d and 568.16 g/ TCCACCAACTGGGTTGG-3′ and reverse 5′-TCATCT d for DF 1.0, DF 1.5, DF 1.75 and DF 2.0 groups, re- GCATGTACAGGGCTG-3′, growth differentiation fac- spectively, throughout the experimental period. The tor 9 (GDF9) forward 5′-GGTATGGCTCTCCGGTTC average daily gain in body weight at 30 d of experiment ACAC-3′ and reverse 5′- CTTGGCAGGTACGCAGGA and at 19 d of the 2nd oestrous cycle were reported in a TGG-3′, β-actin, forward 5′-GGCCGCACCACTGGCA companion study , and were not affected by dietary TTGTCAT and reverse 5′- AGGTCCAGACGCAGGA treatment. –ΔΔCt TGGCG-3′. The threshold cycle (2 ) method was used to calculate relative gene expression. β-actin was Effects of DF intake level on oocyte quality and used as the housekeeping gene, and relative gene expres- reproductive organ development sion levels are expressed as fold changes relative to those As shown in Table 2, the number of COCs collected per in the DF 1.0 group. gilt ranged between 21.2 and 23.3, and the number of oocytes used for in vitro maturation ranged between Untargeted metabolomics 15.5 and 15.7, and these were not affected by DF intake Sera from 8 gilts per group were used for untargeted level (P > 0.05). The expansion rate of COCs was not af- metabolomics analysis. In each group, 2 serum samples fected by DF level (P > 0.05). The rate of oocytes with were randomly pooled as one sample, resulting in 4 rep- first polar bodies increased linearly with increasing DF licate samples for each group. The detailed procedures, level (P = 0.001), and was significantly higher for the DF including metabolite extraction, UHPLC-MS/MS ana- 1.75 diet than for the DF 1.0 diet (57.5% vs. 37.7%, lysis, database search, and data analysis are presented in P < 0.05). The mRNA expression levels of GDF-9 and the online supplementary materials. BMP-15, two markers of oocyte quality in ovarian COCs of gilts (Fig. 2a-d), were increased linearly with increas- Statistical analysis ing DF intake level at 30 d of the experiment and 19 d Raw data were checked using the Grubb’s test method. of the 2nd oestrous cycle. If |Xp - X|> λ (α, n) S, then Xp was considered an out- The effects of DF intake level on the development of lier. Measurement data were normally distributed after reproductive organs (uterus and oviduct) are shown in testing for homogeneity of variance and normal distribu- Table 3. The weight of the uterus (P = 0.059) and the tion using the Shapiro-Wilk method in SAS 9.4 (SAS In- relative weight of the uterus (P = 0.017) increased stitute Inc., Cary, NC, USA). As a completely linearly with increasing DF intake level. The relative randomised design, the statistical analyses were per- weight of the uterus in gilts increased from 5.44 g/kg formed through the mixed procedure of SAS 9.4 using BW in the DF 1.0 group to 6.21 g/kg BW in the DF 1.75 the following statistical model: Yij = μ + Ti + eij, where Y group (P < 0.05). The lengths of the left uterine horn is the analysed variable, μ is the overall mean, Ti is the (P = 0.044) and the right uterine horn (P = 0.001) were fixed effect of the ith treatment, and eij is the error term increased by DF intake level. Specifically, DF 1.75 gilts specific to the pig identified assigned to the ith treat- had a 19.8% greater oocyte maturation rate and a 48.9 ment. The linear and quadratic effects of increasing DF cm longer uterus length than DF 1.0 gilts (P < 0.05). levels on the analysed variable were determined by or- The weight of the left oviduct (P = 0.087) and the right thogonal polynomial contrast. Differences were consid- oviduct (P = 0.002) increased linearly with increasing DF ered statistically significant when P < 0.05 and a trend intake level. was considered significant when 0.05 ≤ P < 0.10. Effects of DF intake level on faecal microbial diversity at Results 19 d of the 2nd oestrous cycle Nutrient intake and number of gilts at each stage Total tags, unique tags, taxon tags, and operational taxo- Six gilts per group were removed from the experiment nomic units (OTUs) of faecal microbiota at 19 d of the after collection of their ovaries at 30 d of the 2nd oestrous cycle in the 4 dietary groups were Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 6 of 16 Table 2 Effects of DF intake level on oocyte maturation in gilts Items Treatments P-value DF 1.0 DF 1.5 DF 1.75 DF 2.0 Linear Quadratic No. of COCs collected per gilt 23.3 ± 1.4 21.2 ± 1.2 22.2 ± 0.9 22.5 ± 2.3 0.695 0.403 No. of oocytes for in vitro maturation 15.5 ± 0.2 15.7 ± 0.2 15.7 ± 0.2 15.5 ± 0.2 0.898 0.467 Expansion rate, % 86.9 ± 5.9 89.5 ± 3.5 91.5 ± 2.1 93.6 ± 3.3 0.232 0.876 c bc a ab Rate of oocytes with first polar body, % 37.7 ± 3.2 41.6 ± 3.0 57.5 ± 2.5 50.6 ± 2.3 0.001 0.568 a,b,c Data are expressed as means ± standard error (S.E.); DF, dietary fiber; n = 6; Means with different letters denote P < 0.05 1,721,847, 242,996, 1,478,851 and 31,092, respectively, at oestrous cycle are presented in Table 4. Two dominant the 97% identity level, revealed by 16S rRNA sequencing. phyla, Firmicutes and Bacteroidetes, accounted for ~ Microbiota alpha diversity was reflected by observed 85% of faecal microbiota. The relative abundance of the species, Shannon and Chao 1 indices. The observed spe- Firmicutes phylum decreased linearly (P < 0.001) or cies and Shannon indices were similar for DF 1.5 and quadratically (P= 0.003) with increasing DF intake level. DF 1.0 groups, but were lower than those of the DF 1.75 By contrast, the relative abundance of the Bacteroidetes and DF 2.0 groups (Fig. 3a and b, P < 0.05). The Chao 1 phylum increased linearly (P < 0.001) or quadratically index for the DF 1.5 group was lower than for the DF (P= 0.043) by increasing DF intake level. The relative 1.0, DF 1.75 and DF 2.0 groups (Fig. 3c, P < 0.05). abundance of the Proteobacteria phylum decreased As shown in the heatmap in Supplementary Fig. 1a linearly with increasing DF intake level (P = 0.002). The and b, we identified clear differences in the phylum and relative abundance of Tenericutes increased linearly with genus distributions of faecal microbiota with increasing increasing DF intake level (P = 0.002). The relative abun- DF intake level. The relative abundances of microbiota dance of the Actinobacteria and Planctomycetes phyla at the phylum level in faeces of gilts at 19 d of the 2nd decreased linearly (P < 0.001) or quadratically (P< 0.05) Fig. 2 Effects of DF intake level on gene expression of COCs in gilts. GDF-9, Growth differentiation factor-9; BMP-15, Bone morphogenetic protein 15; DF 1.0, basal diet without DF supplement; DF 1.5, DF 1.75, and DF 2.0, basal diets with an additional 50, 75 and 100% DF intake, respectively. a,b n = 6 per group. Columns with different letters denote P < 0.05 Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 7 of 16 Table 3 Effects of DF intake level on the development of reproductive tracts in gilts Items Treatments P-value DF 1.0 DF 1.5 DF 1.75 DF 2.0 Linear Quadratic BW at laughter, kg 146.7 ± 1.6 145.3 ± 1.8 145.8 ± 3.0 142.3 ± 1.7 0.209 0.549 Weight of uterus, kg 0.80 ± 0.02 0.82 ± 0.02 0.90 ± 0.03 0.84 ± 0.02 0.059 0.380 b ab a ab Relative weight of uterus, g/kg 5.44 ± 0.17 5.64 ± 0.16 6.21 ± 0.22 5.91 ± 0.14 0.017 0.548 b ab a ab Left uterine, cm 99.2 ± 4.3 107.3 ± 3.3 118.2 ± 5.3 109.2 ± 5.3 0.044 0.232 c bc a ab Right uterine, cm 91.8 ± 4.2 99.3 ± 3.1 121.7 ± 6.3 113.5 ± 6.0 0.001 0.660 Left oviduct, g 3.93 ± 0.25 4.02 ± 0.47 5.19 ± 0.36 4.64 ± 0.50 0.087 0.880 b b a ab Right oviduct, g 3.63 ± 0.22 4.12 ± 0.54 5.91 ± 0.30 4.97 ± 0.38 0.002 0.446 Left oviduct, cm 30.5 ± 0.9 33.3 ± 2.6 35.3 ± 1.0 33.8 ± 1.7 0.100 0.400 Right oviduct, cm 30.6 ± 1.1 32.7 ± 2.5 36.5 ± 1.2 33.2 ± 2.1 0.123 0.343 a,b Data are expressed as means ± S.E.; DF, dietary fiber; n = 6; Means with different letters denote P < 0.05 with increasing DF intake level. The relative abundance Effects of DF intake level on serum metabolomics at 19 of Cyanobacteria increased linearly (P < 0.001) or qua- d of the 2nd oestrous cycle. dratically (P= 0.01) with increasing DF intake level. As presented in Fig. 4, the principal component ana- The relative abundances of microbiota at the genus lysis (PCA) score plot of serum metabolomics data from level (> 0.1%) are presented in Table 5. Thirty of the 53 both positive (a) and negative (b) ionisation modes genera increased linearly or quadratically changed with showed a clear separation of metabolite communities be- increasing DF intake level (P < 0.05 or P < 0.01). The tween gilts in DF 1.0 and other groups, and differentially relative abundances of the genera Lactobacillus, Prevo- altered metabolites revealed significant changes in hier- tella_9, Rikenellaceae_RC9_gut_group, Alloprevotella, archical clustering (Supplementary Fig. 2a and b). The Prevotellaceae_UCG-003, Prevotella_7, dgA-11_gut_ numbers of differentially abundant metabolites identified group, Sphaerochaeta, Leeia, Erysipelotrichaceae_UCG- and annotated in serum samples between groups are 004, Catenibacterium, Fibrobacter and Faecalibacterium presented in Supplementary Table 1, revealing 92, 123 were elevated by increasing DF intake level (linear or and 171 differentially altered metabolites in DF 1.5, DF quadratic, P < 0.05). The relative abundances of the genera 1.75 and DF 2.0 gilts compared with DF 1.0 gilts. Streptococcus, Clostridium_sensu_stricto_1, Succinivibrio, In particular, we compared differentially abundant Eubacterium_coprostanoligenes_group, Ruminococcaceae_ serum metabolites identified in both positive and nega- NK4A214_group, Lachnospiraceae_XPB1014_group, Phas- tive ionisation modes between DF 1.0 and DF 1.75 gilts colarctobacterium, Escherichia-Shigella, Family_XIII_ (Table 6). In brief, a total of 41 (in positive ionisation AD3011_group, Turicibacter, Lachnospiraceae_AC2044_ mode) and 20 (in negative ionisation mode) serum me- group, Candidatus_Soleaferrea, Lachnospira, Blautia, tabolites were upregulated by 1.5–27.0 times in DF 1.75 Acidaminococcus, Romboutsia,and Lachnoclostridium de- gilts compared with DF 1.0 gilts (P < 0.05 or P < 0.01). creased with increasing DF intake level (linear or quadratic, A total of 25 (in positive ionisation mode) and 36 (in P<0.05). negative ionisation mode) serum metabolites were down-regulated in DF 1.75 gilts compared with DF 1.0 Fig. 3 Microbiota alpha-diversity in faeces of gilts fed different dietary fiber levels at 19 d of the 2nd oestrous cycle. a, Observed species. b, Shannon index. c, Chao 1 index. Gilts constituted the experimental units (n = 6). DF 1.0, basal diet without DF supplement; DF 1.5, DF 1.75 and DF a,b 2.0, basal diets with an additional 50%, 75% and 100% DF intake, respectively. Columns with different letters denote P < 0.05 Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 8 of 16 Table 4 Relative abundance of microbiota at the phyla level in faeces of gilts, % Items Treatments P-value 1.0 DF 1.5 DF 1.75DF 2.0 DF Linear Quadratic ab a bc c Firmicutes 44.22 ± 1.07 47.63 ± 1.89 40.34 ± 1.53 38.36 ± 0.80 < 0.001 0.003 bc c ab a Bacteroidetes 40.64 ± 1.16 38.81 ± 1.79 44.85 ± 1.78 46.51 ± 1.42 0.004 0.043 ab b a ab Spirochaetes 4.62 ± 0.65 3.29 ± 0.59 5.76 ± 0.63 5.60 ± 0.79 0.169 0.079 a ab b b Proteobacteria 4.08 ± 0.41 3.80 ± 0.26 3.00 ± 0.23 3.00 ± 0.24 0.002 0.629 Tenericutes 2.12 ± 0.13 2.26 ± 0.27 2.73 ± 0.22 2.69 ± 0.16 0.013 0.866 Euryarchaeota 2.15 ± 0.32 2.72 ± 0.79 1.38 ± 0.38 1.97 ± 0.29 0.385 0.778 a b b b Actinobacteria 0.87 ± 0.55 0.22 ± 0.01 0.18 ± 0.02 0.23 ± 0.03 < 0.001 0.008 b b a ab Lentisphaerae 0.74 ± 0.05 0.67 ± 0.07 1.02 ± 0.08 0.82 ± 0.07 0.062 0.840 ab a b b Planctomycetes 0.13 ± 0.04 0.26 ± 0.09 0.09 ± 0.02 0.05 ± 0.01 0.017 0.002 bc c ab a Cyanobacteria 0.17 ± 0.02 0.15 ± 0.02 0.25 ± 0.04 0.34 ± 0.05 < 0.001 0.010 b c a a Others 0.25 ± 0.03 0.18 ± 0.01 0.41 ± 0.02 0.47 ± 0.05 < 0.001 < 0.001 a,b Data are expressed as means ± S.E.; DF, dietary fiber; n = 6; Means with different letters denote P < 0.05 gilts (P < 0.05 or P < 0.01). Enrichment of these metab- Melatonin concentrations in follicular fluid increased olites resulted in changes in multiple biological pathways linearly with increasing DF intake level at 30 d of the ex- (Fig. 5), including the serotonergic pathway, the PPAR periment and at 19 d of the 2nd oestrous cycle (Supple- signalling pathway, Parkinson’s disease, carbohydrate di- mentary Fig. 3). gestion and absorption, arachidonic acid metabolism, Linear regression analysis results between butyrate protein digestion and absorption, propanoate metabol- concentration in colon chyme and serotonin in serum, ism, inflammatory mediator regulation of TRP channels, follicular fluid, and colon tissues are presented in cholesterol metabolism, bile secretion, pyrimidine me- Table 9. A positive linear association was observed be- tabolism, oxidative phosphorylation, fatty acid biosyn- tween butyrate concentration in colon chyme and sero- thesis, nicotinate and nicotinamide metabolism, tonin in serum, follicular fluid and colon tissues neuroactive ligand-receptor interaction, and metabolic (P < 0.01, Table 9). pathways under positive ionisation mode (Fig. 5a), and sphingolipid metabolism, alanine, aspartate and glutam- Discussion ate metabolism, lysine degradation, folate biosynthesis, DF is an anti-nutritional factor that exerts negative ef- metabolic pathways, arginine and proline metabolism, fects on nutrient digestion, and sometimes diminishes beta-alanine metabolism, purine metabolism, glutathione growth performance . However, basal diet supple- metabolism, ABC transporters, and bile secretion under mented with graded amounts of DF from a 33 kg phase negative ionisation mode (Fig. 5b). did not negatively impact growth performance and the The effects of DF intake level on concentrations age at puberty in gilts . Oocyte maturation, a param- of SCFAs in faeces and colon chyme of gilts are eter reflecting the quality of oocytes, is a determining shown in Table 7. The concentrations of acetate, factor influencing early embryo development [21, 22]. propionate and butyrate in faeces of gilts on 30 d of Previous research revealed that the beneficial effects of the experiment were linearly increased by DF intake fiber-rich ingredients on early embryonic survival could level (P<0.05 or P < 0.01, Table 7). The concen- be attributed to enhanced oocyte maturation in gilts [5, trations of propionate and butyrate in chyme in the 6]. Consistently, results from our recent studies demon- colons of gilts at 19 d of the 2nd oestrous cycle strated that DF could improve the survival rate of imma- were linearly increased by DF intake level (P < 0.05, ture oocytes, thereby improving the ovarian reservation Table 7). of replacement gilts [7, 13]. The current findings, The effects of DF intake level on serotonin concentra- coupled with the results of a companion study , tions in the serum and follicular fluid in gilts are pre- proved beneficial effects of DF on both the number and sented in Table 8. The serum serotonin concentrations quality of oocytes in growing gilts. The quality of re- on 30 d of the experiment increased linearly with in- placement gilts not only plays an important role in pu- creasing DF intake level (P = 0.001, Table 8). The eleva- bertal maturation, but also influences the lifetime tion in DF intake level resulted in a linear increase in fertility of sows . The successful reproductive serotonin in serum (P < 0.001, Table 8) and in follicular process of sows requires a continuous supply of mature fluid (P = 0.032, Table 8). oocytes and the secretion of reproductive hormones such Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 9 of 16 Table 5 Relative abundance of the top 53 microbiota at the genus level ,% Items Treatments P-value 1.0 DF 1.5 DF 1.75 DF 2.0 DF Linear Quadratic Prevotellaceae_NK3B31_group 6.33 ± 0.37 6.70 ± 0.80 6.34 ± 0.65 7.10 ± 1.04 0.440 0.895 c bc a ab Lactobacillus 2.21 ± 0.16 2.60 ± 0.46 4.98 ± 1.10 3.81 ± 0.32 < 0.001 0.660 ab b a a Prevotella_9 3.46 ± 0.54 2.52 ± 0.30 4.77 ± 0.73 5.14 ± 0.92 0.025 0.034 Treponema_2 4.23 ± 0.63 2.98 ± 0.57 4.94 ± 0.58 4.78 ± 0.79 0.368 0.119 bc c ab a Rikenellaceae_RC9_gut_group 4.33 ± 0.31 3.95 ± 0.33 5.61 ± 0.34 5.80 ± 0.40 0.001 0.045 b a b b Streptococcus 3.83 ± 0.28 5.90 ± 0.56 3.50 ± 0.50 2.87 ± 0.29 0.027 < 0.001 Methanobrevibacter 2.05 ± 0.32 2.66 ± 0.79 1.34 ± 0.38 1.89 ± 0.28 0.413 0.726 Ruminococcaceae_UCG-005 2.61 ± 0.27 3.16 ± 0.37 2.17 ± 0.23 2.15 ± 0.21 0.069 0.079 a a b b Clostridium_sensu_stricto_1 2.46 ± 0.29 2.68 ± 0.16 1.85 ± 0.10 1.49 ± 0.11 < 0.001 0.001 Parabacteroides 2.32 ± 0.26 2.24 ± 0.26 2.27 ± 0.24 2.15 ± 0.18 0.620 0.895 a ab c bc Succinivibrio 1.98 ± 0.30 1.61 ± 0.17 1.00 ± 0.12 1.11 ± 0.15 < 0.001 0.845 Megasphaera 1.88 ± 0.36 1.85 ± 0.69 0.87 ± 0.17 1.30 ± 0.50 0.089 0.838 Ruminococcaceae_UCG-002 2.42 ± 0.21 2.36 ± 0.21 2.30 ± 0.12 2.46 ± 0.24 0.989 0.571 a a b b Eubacterium_coprostanoligenes_group 2.06 ± 0.08 2.42 ± 0.22 1.58 ± 0.15 1.51 ± 0.08 0.001 0.001 Prevotellaceae_UCG-001 1.54 ± 0.37 1.24 ± 0.22 1.27 ± 0.34 1.67 ± 0.38 0.934 0.212 ab a b b Ruminococcaceae_NK4A214_group 1.43 ± 0.08 1.50 ± 0.12 1.18 ± 0.10 1.16 ± 0.06 0.008 0.169 Oscillospira 1.42 ± 0.08 1.32 ± 0.09 1.42 ± 0.14 1.41 ± 0.07 0.944 0.532 Ruminococcaceae_UCG-014 1.36 ± 0.14 1.31 ± 0.12 1.12 ± 0.12 1.18 ± 0.11 0.149 0.922 Alloprevotella 1.34 ± 0.13 1.28 ± 0.24 1.69 ± 0.14 1.92 ± 0.20 0.027 0.188 bc c a ab Prevotellaceae_UCG-003 1.28 ± 0.09 1.25 ± 0.20 1.97 ± 0.15 1.88 ± 0.17 0.002 0.382 Lachnospiraceae_XPB1014_group 1.12 ± 0.11 1.13 ± 0.08 0.94 ± 0.08 0.85 ± 0.06 0.011 0.191 Prevotella_1 1.00 ± 0.09 0.77 ± 0.10 0.79 ± 0.14 0.96 ± 0.14 0.680 0.095 Ruminococcus_1 0.98 ± 0.08 1.03 ± 0.16 0.82 ± 0.09 0.88 ± 0.10 0.271 0.710 a a b b Phascolarctobacterium 0.87 ± 0.09 1.10 ± 0.16 0.60 ± 0.06 0.57 ± 0.03 < 0.001 0.010 Prevotella_2 0.81 ± 0.08 0.66 ± 0.10 1.01 ± 0.12 1.04 ± 0.09 0.055 0.080 Ruminococcaceae_UCG-010 0.71 ± 0.04 0.67 ± 0.08 0.76 ± 0.03 0.81 ± 0.05 0.147 0.256 Prevotella_7 0.66 ± 0.13 0.36 ± 0.06 0.78 ± 0.15 0.89 ± 0.21 0.154 0.010 Christensenellaceae_R-7_group 0.60 ± 0.06 0.68 ± 0.06 0.50 ± 0.04 0.52 ± 0.04 0.093 0.168 a ab c bc Escherichia-Shigella 0.56 ± 0.22 0.37 ± 0.09 0.15 ± 0.02 0.23 ± 0.05 < 0.001 0.304 dgA-11_gut_group 0.52 ± 0.08 0.52 ± 0.07 0.68 ± 0.06 0.82 ± 0.12 0.008 0.179 a ab b ab Family_XIII_AD3011_group 0.50 ± 0.03 0.48 ± 0.05 0.39 ± 0.02 0.43 ± 0.02 0.018 0.734 Terrisporobacter 0.53 ± 0.05 0.52 ± 0.04 0.67 ± 0.08 0.53 ± 0.04 0.541 0.492 b b a a Sphaerochaeta 0.39 ± 0.03 0.31 ± 0.03 0.76 ± 0.10 0.79 ± 0.04 < 0.001 0.001 a a ab b Turicibacter 0.33 ± 0.06 0.33 ± 0.02 0.23 ± 0.02 0.21 ± 0.02 0.001 0.212 a a b b Lachnospiraceae_AC2044_group 0.34 ± 0.02 0.29 ± 0.01 0.18 ± 0.02 0.19 ± 0.01 < 0.001 0.764 b b a ab Leeia 0.23 ± 0.04 0.21 ± 0.08 0.68 ± 0.27 0.51 ± 0.08 0.002 0.534 Mitsuokella 0.25 ± 0.04 0.28 ± 0.09 0.33 ± 0.13 0.25 ± 0.04 0.794 0.368 a a b b Candidatus_Soleaferrea 0.22 ± 0.01 0.25 ± 0.03 0.13 ± 0.01 0.16 ± 0.01 < 0.001 0.207 a b b b Lachnospira 0.20 ± 0.03 0.19 ± 0.01 0.14 ± 0.01 0.14 ± 0.01 < 0.001 0.404 a ab b b Blautia 0.21 ± 0.11 0.10 ± 0.01 0.09 ± 0.02 0.07 ± 0.01 < 0.001 0.526 a a b ab Acidaminococcus 0.18 ± 0.05 0.17 ± 0.08 0.04 ± 0.01 0.08 ± 0.03 0.003 0.896 Ruminococcaceae_UCG-009 0.16 ± 0.01 0.15 ± 0.02 0.18 ± 0.02 0.17 ± 0.01 0.444 0.511 a a b b Romboutsia 0.15 ± 0.03 0.14 ± 0.01 0.08 ± 0.01 0.08 ± 0.01 < 0.001 0.366 Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 10 of 16 Table 5 Relative abundance of the top 53 microbiota at the genus level ,% (Continued) Items Treatments P-value 1.0 DF 1.5 DF 1.75 DF 2.0 DF Linear Quadratic ab b ab a Erysipelotrichaceae_UCG-004 0.14 ± 0.02 0.12 ± 0.01 0.18 ± 0.02 0.19 ± 0.02 0.024 0.064 a b a a Catenibacterium 0.14 ± 0.03 0.05 ± 0.01 0.19 ± 0.06 0.25 ± 0.06 0.019 < 0.001 Bifidobacterium 0.13 ± 0.01 0.11 ± 0.01 0.09 ± 0.02 0.14 ± 0.03 0.904 0.107 Dialister 0.12 ± 0.05 0.08 ± 0.02 0.20 ± 0.07 0.21 ± 0.08 0.061 0.058 Fibrobacter 0.12 ± 0.02 0.06 ± 0.01 0.18 ± 0.02 0.25 ± 0.05 < 0.001 < 0.001 Lachnoclostridium 0.12 ± 0.02 0.12 ± 0.02 0.07 ± 0.01 0.06 ± 0.01 < 0.001 0.075 Thalassospira 0.10 ± 0.01 0.20 ± 0.12 0.13 ± 0.01 0.12 ± 0.01 0.571 0.044 Acetitomaculum 0.10 ± 0.02 0.09 ± 0.02 0.12 ± 0.02 0.13 ± 0.03 0.178 0.457 Campylobacter 0.08 ± 0.01 0.11 ± 0.04 0.09 ± 0.02 0.10 ± 0.02 0.751 0.595 bc c a ab Faecalibacterium 0.08 ± 0.01 0.07 ± 0.01 0.15 ± 0.02 0.12 ± 0.01 0.004 0.475 a,b Data are expressed as means ± S.E.; DF, dietary fiber; n = 6; Means with different letters denote P < 0.05 as oestrogen and progesterone from granulosa cells, which DF consists of nondigestible carbohydrates that are re- is largely determined by the number and quality of oocytes sistant to digestion and absorption in the porcine gastro- in ovaries [24–26]. Therefore, DF consumption during the intestinal tract. Hence their metabolism requires replacement phase may exert a benefit on the lifetime fertil- microbiota harboured in the gut. Indeed, microbial me- ity of sows, although this needs further validation. tabolism of DF is the key process mediating the benefi- Interestingly, our results implied that uterine develop- cial effects of DF on gastrointestinal health and disease ment was also significantly promoted by DF intake level. resistance [17, 29]. DF significantly alters the gut micro- To date, very few data are available on the nutrient- bial diversity of hosts, by stimulating the growth of fiber- dependent regulation of the uterus in gilts. Recent evi- degrading microbiota, and this alternation in gut micro- dence found that dietary energy density and lysine level bial diversity in turn impacts gut microbial ecology, host had no effect on uterine development . Weaver et al. physiology, and health [17, 29]. In order to investigate observed a 118 g heavier uterine weight on 19 d of the the role of microbiota in the regulation of oocyte matur- oestrous cycle in gilts fed a fiber-rich diet compared with ation by dietary fiber, we explored microbial diversity by a low-fiber diet . The development of uterus at mat- 16S rRNA sequencing. In the present study, the Ob- ing plays an important role in regulating early embryonic served_species, Shannon index, and Chao1 index of DF survival, since foetus would die if uterine endometrial 1.5 gilts were lower than those of DF 1.75 and DF 2.0 lumen epithelium was insufficient to provide support to groups, indicating that DF intake level altered the alpha foetus development . Therefore, replacement gilts diversity of microbiota in the gut. With increasing DF fed a high DF diet during their rearing phase could intake level, the relative abundance of 13 microbiota benefit from subsequent improved fertility. genera were significantly increased, among which Fig. 4 Principal component analysis of the metabolites identified in positive and negative ionisation modes. DF 1.0, basal diet without DF supplement; DF 1.5, DF 1.75 and DF 2.0, basal diets with an additional 50%, 75% and 100% DF intake, respectively. QC, quality control samples Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 11 of 16 Table 6 Differentially abundant serum metabolites between DF 1.0 and DF 1.75 gilts identified in positive and negative ionisation 1,2 modes Name Fold change P-value Name Fold change P-value Positive ionisation Negative ionisation (2S)-1-Hydroxy-3-(pentadecanoyloxy)- 18.966 0.047 Sinapyl alcohol 27.041 0.044 2-propanyl (15Z)-15-tetracosenoate 3-(2,4-Cyclopentadien-1-ylidene)- 5.594 0.003 Cuauhtemone 13.210 < 0.001 5alpha-androstan-17beta-ol Oxandrolone 5.563 0.013 Cholic acid glucuronide 8.250 0.025 2,6-Di-tert-butyl-1,4-benzoquinone 5.028 0.005 GLIMEPIRIDE, CIS- 5.853 < 0.001 19-Nortestosterone 4.993 0.007 Olivoretin D 5.543 0.013 3-Beta-fluoro-5-beta-pregnan-20-one 4.670 0.002 Deoxycholic acid 4.117 0.001 p-Cymene 4.148 0.008 Avasimibe 3.204 0.026 Geroquinol 3.979 0.006 Taurochenodeoxycholic acid 3.100 0.044 Hypaphorine 3.902 < 0.001 p-Dimethylinamyl benzoate 3.077 < 0.001 Jasmonal 3.766 0.007 Chaksine 3.026 0.003 Ibuprofen 3.680 0.002 Tenivastatin 2.962 0.009 3-Beta,17-beta-diacetoxy-5α-androstane 3.057 0.007 Mupirocin 2.918 0.047 Oleandomycin 2′-O-phosphate 2.998 0.041 Ubiquinone Q4 2.219 0.025 Ionene 2.869 0.049 Sunitinib 2.185 0.011 Diaziquone 2.858 < 0.001 (3alpha)-3-Hydroxycholan-24-oic acid 2.054 0.042 1-Piperideine 2.857 0.004 Ifetroban 2.038 0.010 Myxalamid A 2.801 0.045 Maleimide 1.918 0.012 Genistein 2.584 0.011 5-HT 1.855 0.003 7-Ketodeoxycholic acid 2.434 0.023 Uldazepam 1.814 0.018 1-O-[4-(1H-indol-3-yl)butanoyl] 2.335 0.001 Indole-3-carboxilic acid-O-sulphate 1.690 0.019 -beta-D-glucopyranose Linagliptin 2.278 0.017 6α-Prostaglandin I1 0.566 0.011 (KDO)2-lipid IVA 2.096 0.045 3-Hydroxydecanoic acid 0.548 0.021 4-Aminobenzoic acid 2.089 0.043 14,18-Dihydroxy-12-oxo-9,13,15-octadecatrienoic acid 0.542 < 0.001 Spermidine 1.964 0.026 Cromoglicic acid 0.531 < 0.001 Hexoprenaline 1.902 0.005 Nemonapride (JAN) 0.526 0.044 Manumycin 1.899 0.041 Epithienamycin F 0.519 0.010 N-Lactoyl ethanolamine phosphate 1.888 0.002 10-Undecenoic acid 0.508 0.010 Perphenazine enantate 1.862 0.003 Prunin 0.502 0.010 5-HIAA 1.856 0.002 Leucodelphinidin 0.497 0.001 TU4153400 1.831 0.036 MFCD00065806 0.496 0.015 1-Octadecanoyl-2-[(15Z)- 1.855 0.044 4,6,8-Trihydroxy-7-methoxy-3-methyl-3,4-dihydroisochromen-1-one 0.494 0.029 tetracosenoyl]-sn-glycero-3-phosphocholine Bikhaconitine 1.850 0.007 ARAMITE 0.485 0.024 Cediranib 1.797 0.002 Uridine 0.480 0.013 Callystatin A 1.782 0.017 N-Palmitoyl-L-phenylalanine 0.463 0.014 Decoside 1.690 0.005 Cidofovir anhydrous 0.460 0.004 5-methyltetrahydropteroyltri- 1.677 0.012 3-Indoxyl sulphate 0.448 0.002 L-Glutamic acid 2-(2-Carboxyethyl)-4-methyl- 1.640 0.012 Butoctamide semisuccinate 0.447 0.009 5-Pentyl-3-furoic acid Trans-Anethole 1.637 0.021 Kukoamine A 0.443 0.001 Saccharocin 1.541 0.002 Pyrophosphoric Acid 0.433 0.033 5-Phospho-beta-D-ribosylamine 1.540 0.009 4-Phenolsulfonic acid 0.429 0.046 Dehydrocholic acid 1.50 0.013 Geranyl phosphate 0.412 0.043 Tritoqualine 0.634 0.008 Caftaric acid 0.412 0.008 Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 12 of 16 Table 6 Differentially abundant serum metabolites between DF 1.0 and DF 1.75 gilts identified in positive and negative ionisation 1,2 modes (Continued) Name Fold change P-value Name Fold change P-value Benzoyl cyanide 0.628 < 0.001 Disulfaton 0.396 0.023 Ocaperidone 0.622 0.012 4-(1,2-Dihydroxy-2-propanyl)-1-methyl-1,2-cyclohexanediol 0.388 0.021 Monomethyl phosphate 0.621 0.002 Hydrogen bromide 0.363 < 0.001 MFCD00056202 0.619 0.019 (2-Hydroxy-2-oxido-1,3,2-dioxaphospholan-4-yl) methyl palmitate 0.316 0.004 Minosaminomycin 0.589 0.037 Chloralodol 0.228 < 0.001 Trametinib 0.557 0.003 Caprylic acid 0.199 0.024 Premithramycin A3’ 0.550 0.004 1,3-Nonanediol acetate 0.187 0.039 Alpha,alpha’-trehalose 6-mycolate 0.546 0.005 Retosiban 0.170 < 0.001 1-stearoyl-2-arachidonoyl- 0.521 0.033 3-Hydroxytridecanoic acid 0.155 0.009 sn-glycero-3-phosphoserine Phytosphingosine 0.521 0.016 Difluprednate 0.126 < 0.001 Depe 0.484 0.006 Leukotriene B4 0.075 < 0.001 Azithromycin 0.462 0.001 Pentachlorophenol 0.071 < 0.001 1-Stearoyl-2-docosahexanoyl- 0.461 0.037 3,4,15-Triacetoxy-12,13-epoxytrichothec-9-en-8-yl 3-methylbutanoate 0.055 < 0.001 sn-glycero-3-phosphocholine Benzyl succinate 0.458 0.003 Nobiletin 0.029 < 0.001 Ascidiacyclamide 0.457 0.005 1,2-Dioleoyl-sn-glycero-3-phospho- 0.436 0.011 N,N-dimethylethanolamine 12-Deoxyoligomycin A 0.433 0.011 Terminalin 0.420 0.036 Digitoxin 0.415 0.028 Uroporphyrinogen IV 0.362 0.009 Vilazodone 0.361 0.001 N,N-Bis(2-hydroxyethyl) 0.334 0.002 dodecanamide 1-Eicosyl-2-docosanoyl-sn-glycero-3- 0.307 0.042 phosphocholine Emblicanin A 0.275 0.007 Phytolaccoside B 0.221 0.025 Serum samples collected on 19 d of the 2nd oestrous cycle. Metabolites with VIP > 1, P-value < 0.05, fold change ≥ 1.5 or fold change ≤ 0.65 were considered differential metabolites Fig. 5 KEGG pathway analysis of differential metabolites identified in positive and negative ionisation modes between DF 1.0 and DF 1.75 groups. DF 1.0, basal diet without DF supplement; DF 1.75, basal diet with an additional 75% DF intake. DF, dietary fiber Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 13 of 16 Table 7 Effects of DF intake level on the concentrations (μmol/g) of short-chain fatty acids in faeces and colon chyme of gilts Items Treatments P-value 1.0 DF 1.5 DF 1.75 DF 2.0 DF Linear Quadratic Faeces at 30 d of experiment b b ab a Acetate 40.1 ± 2.6 41.5 ± 2.9 47.6 ± 1.7 51.4 ± 2.7 0.002 0.231 b ab a a Propionate 14.2 ± 1.6 15.5 ± 1.4 19.2 ± 0.8 19.4 ± 1.1 0.003 0.709 Butyrate 8.4 ± 0.8 9.8 ± 1.2 11.4 ± 1.1 12.1 ± 0.7 0.010 0.843 Chyme in colon at 19 d of the 2nd oestrous cycle Acetate 58.9 ± 2.9 56.8 ± 4.8 63.7 ± 3.0 62.6 ± 3.0 0.324 0.604 Propionate 25.8 ± 1.1 24.8 ± 1.9 29.8 ± 1.2 31.8 ± 3.5 0.046 0.218 b ab ab a Butyrate 11.6 ± 0.4 12.5 ± 1.3 13.1 ± 0.8 15.4 ± 1.0 0.012 0.263 a,b Faeces tested at 30 d of the experiment, n = 8; Chyme colon data, n = 6; Data are expressed as means ± S.E.; DF, dietary fiber; Means with different letters denote P < 0.05 Lactobacillus, Faecalibacterium, Prevotella_9, Alloprevo- metabolites. Compared with gilts in the DF 1.0 group, tella, Prevotellaceae_UCG-003, Prevotella_7, Fibrobacter, the total number of metabolites that differed from those Sphaerochaeta and Erysipelotrichaceae_UCG-004 are in DF 1.5, DF 1.75 and DF 2.0 groups was 92, 123 and able to mobilise DF to produce SCFAs. Studies con- 171, respectively, indicating a dose-dependent regulation ducted on zebrafish revealed that the probiotic Lacto- of DF intake level on serum metabolites. However, oo- bacillus rhamnosus exerted beneficial effects on cyte quality reached a peak in DF 1.75 gilts, implying an oocyte development [30, 31]. Additionally, Faecalibac- optimal DF intake level for replacement gilts, but the terium was implicated to play a role in the pathogen- reason why a further increase in DF intake level resulted esis of polycystic ovary syndrome (PCOS) in human in no further improvement in reproductive traits com- [32–34]. On the other hand, 17 microbiota genera pared with DF 1.75 gilts remains unclear and awaits fur- significantly decreased with increasing DF intake level, ther investigation. including Streptococcus and Escherichia-Shigella, We further explored the differential metabolites be- which are pathogenic bacteria. A recent study re- tween DF 1.0 and DF 1.75 groups. Interestingly, KEGG vealed that an elevation in Bacteroides vulgatus was pathway analysis revealed that some of those metabolites an important factor leading to PCOS in human . were gut-derived. For example, the serotonergic pathway Furthermore, studies conducted on humans revealed derived from tryptophan metabolism in enterochromaf- that the diversity of the gut microbiota is closely cor- fin cells of the gastrointestinal tract, in which tryptophan related with the morbidity of PCOS, in particular for is converted to serotonin (also known as 5-HT) by the those with obesity [34–36]. However, it remains un- enzyme tryptophan hydroxylase 1 encoded by the TPH1 clear how the microbiota influences ovarian develop- gene . It has been revealed that metabolites pro- ment in domestic animals such as pigs. duced by the gut microbiota, such as SCFAs, bile acids, We conducted serum metabolomics analysis to ex- cholate, deoxycholate and p-aminobenzoate, can up- plore the potential mechanism mediating the effects of regulate TPH1 gene expression and thereby stimulate DF on oocytes in gilts. The untargeted metabolomics serotonin secretion . Over 95% of serotonin is gut- analysis revealed significant changes in serum derived, and serotonin is believed to be a gut-derived Table 8 Effects of dietary fiber intake level on serotonin concentration in serum, follicular fluid and colon tissues of gilts Treatments P-value 1.0 DF 1.5 DF 1.75 DF 2.0 DF Linear Quadratic At 30 d of experiment b ab a a Serum, ng/mL 1422.1 ± 86.6 1713.4 ± 1115.3 2069.1 ± 133.8 1879.5 ± 105.5 0.001 0.226 FF, pg/mL 209.8 ± 16.0 259.9 ± 24.9 286.1 ± 16.8 304.5 ± 32.1 < 0.001 0.356 At 19 d of the 2rd oestrous cycle c b ab a Serum, ng/mL 646.8 ± 42.4 847.3 ± 32.2 1026.8 ± 68.5 1141.0 ± 51.9 < 0.001 0.598 FF, pg/mL 112.7 ± 10.0 124.8 ± 27.8 179.6 ± 35.8 180.1 ± 13.1 0.032 0.724 b b a a Colons, ng/mg 2.84 ± 0.28 3.05 ± 0.24 4.58 ± 0.20 4.11 ± 0.09 < 0.001 0.928 a,b Data are expressed as means ± S.E.; means with different letters denote P < 0.05. DF, dietary fiber; FF, follicular fluid; n =6 Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 14 of 16 Table 9 Linear regression between butyric acid (x, μmol/g) and . Liver-derived bile acids in mammals are usually con- serotonin in different tissues sidered primary acids, and most are re-absorbed via entero- Items b b R P-value hepatic circulation. However, a small fraction of this pool 0 1 (roughly 5%) is able to escape reabsorption in the ileum Serotonin and undergoes bacterial transformation in the colon, giving Serum, ng/mL 24.705 67.739 0.624 < 0.001 rise to secondary bile acids. In this study, the secondary bile Follicular fluid, pg/mL −118.494 20.362 0.697 < 0.001 acids deoxycholic acid and taurochenodeoxycholic acid Colon, ng/mg 1.266 0.181 0.281 0.008 were increased in DF 1.75 gilts compared with DF 1.0 gilts. The linear regression model is y = b + b × x, where b denotes serum 0 1 0 Tauroursodeoxycholic acid was shown to facilitate DNA serotonin concentrations when the butyrate concentration in colonic content damage repair and improve early embryo development in was 0 μmol/g, and b denotes the serotonin increment when the colonic butyrate content was increased to 1 μmol/g pigs  and other mammals . Additionally, DF intake also altered levels of other metabolites, including spermi- metabolic signal [38, 39]. In order to validate the effect dine , 4-aminobenzoic acid and ibuprofen that of DF intake level on serotonin secretion, we measured are known to influence oocyte quality or reproductive func- the serum concentration of serotonin, and revealed a lin- tion. However, we cannot exclude the possibility that these ear effect of DF intake on serum serotonin level. Con- differentially abundant metabolites might act as primary sistently, the serotonin level in follicular fluid was also signals to trigger secondary metabolic signals that influence elevated by DF intake level. Serotonin receptors such as oocyte and uterine development. 5-hydroxytryptamine (HTR)1D, 5-HTR2 and 5-HTR7 are expressed in porcine ovarian tissues . Injection of Conclusion serotonin into crustaceans [40–42] and fish  resulted The current study provides evidence showing that in- in improved ovarian follicular development and oocyte creased DF intake exerts profound beneficial effects on maturation. Serotonergic signalling in mammalian ovar- oocyte maturation and uterine development in gilts. ian follicles and oocytes might play important roles in Notably, feeding replacement gilts additional intake of oocyte or early embryo survival . Deletion of the 419.5 g/d DF in the form of inulin and cellulose at a 1:4 rate-limiting enzyme-encoding gene Tph1 resulted in el- ratio on a corn-soybean meal based diet could optimize evated embryo death from 3.6% in wild-type to 80–89% the oocyte and uterine development. We also observed in mice lacking Tph1 . Therefore, serotonin might that DF might increase the SCFA-producing microbe be one of the potential regulators mediating the effects and gut-derived metabolites (such as serotonin) to exert of DF on oocyte maturation in gilts. Additionally, sero- the benefit on the oocyte quality and uterine develop- tonin serves as the sole precursor of melatonin via the ment of replacement gilts, and thereby providing new rate-limiting enzyme arylalkylamine-N-acetyltransferase microbial and metabolomic insight into the mechanisms (AANAT), the expression of which can be up-regulated mediating the effects of DF. The findings could help de- by the microbial metabolite butyrate in duodenal tissue velop optimal nutritional strategies for replacement gilts, and Caco-2 cells . To clarify, we observed a dose- as well as dietary patterns for other mammals, including dependent effect of DF on the concentration of mela- humans. tonin in follicular fluids. Several lines of evidence have Abbreviations demonstrated that melatonin can promote the develop- DF: Dietary fiber; LY: Landrace × Yorkshire; SD: Standard deviation; mental competence of porcine oocytes [47–49]. Thus, SCFAs: Short-chain fatty acids; CF: Crude fiber; NDF: Neutral detergent fiber; COC: Cumulus-oocyte complex; ELISA: Enzyme-linked immunosorbent assay; the serotonin-melatonin pathway appears to be involved BMP15: Bone morphogenetic protein 15; GDF9: Growth differentiation factor in the control of oocyte maturation following DF intake. 9; PCA: Principal component analysis; PCOS: Polycystic ovary syndrome; In addition, sphingolipid metabolism differed between TPH1: Enzyme tryptophan hydroxylase 1; AANAT: Arylalkylamine-N- acetyltransferase gilts in DF 1.0 and DF 1.75 groups. Sphingolipids are lipids with a set of aliphatic amino alcohols that play an Supplementary Information important role in cell recognition and signal transduc- The online version contains supplementary material available at https://doi. tion . Ceramides are early products of sphingolipid org/10.1186/s40104-021-00657-0. synthetic pathways involved in the control of hepatic gluconeogenesis induced by the microbiota-bile acid Additional file 1. Supplementary figures. pathway , and they impair porcine oocyte quality via regulation of mitochondrial oxidative stress and apoptosis Acknowledgements The authors wish to thank the laboratory staff for their ongoing assistance. [52, 53]. Bile acids, steroid acids primarily produced by the liver, are secreted into the gut lumen upon feeding to assist Authors’ contributions the absorption of nutrients such as lipids and vitamins, glu- MC, DW and YZ designed and supervised the experiments. MC, YG, LH, LT, cose homeostasis, and regulation of energy expenditure XJ and JL conducted the animal trial and performed data collection. ZM, LC, Men et al. Journal of Animal Science and Biotechnology (2022) 13:14 Page 15 of 16 YL and ZF conducted statistical analyses. ZM and YZ analysed microbial 16S ovarian follicular atresia in a pig model. Br J Nutr. 2021;125(1):38–49. https:// rRNA and metabolomics data. YZ and ZM wrote and revised the manuscript. doi.org/10.1017/S0007114520002378. All authors read and approved the final manuscript. 14. Englyst HN, Cummings JH. Improved method for measurement of dietary fiber as non-starch polysaccharides in plant foods. J Assoc Off Anal Chem. 1988;71(4):808–14. Funding 15. Van Soest PJWR. Determination of lignin and cellulose in acid-detergent This study was supported by the Sichuan Science and Technology Program fiber with permanganate. J Association Off Anal Chem. 1968;4(51):780–5. (2021YJ0287), and National Natural Science Foundation of China, PR China https://doi.org/10.1093/jaoac/51.4.780. (31772616). The funding sources played no role in study design or the 16. Mudgil D, Barak S. 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Journal of Animal Science and Biotechnology – Springer Journals
Published: Jan 13, 2022
Keywords: Dietary fiber; Gilts; Metabolomics; Microbiota; Oocyte maturation
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