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Differential Effects of Breed and Nursing on Early-Life Colonic Microbiota and Immune Status as Revealed in a Cross-Fostering Piglet Model.

ABSTRACT: Nursing mother and breed can differently regulate early-life microbiota succession in pigs. However, it remains unclear whether they affect gastrointestinal microbiota and immune status, which are critical for early-life gut health. Here, an interspecific cross-fostering piglet model was employed by fostering neonatal Yorkshire and Meishan piglets to the same or another breed of sows. Jejunal and colonic microbiotas and mucosal immune parameters were analyzed at postnatal days 14 (preweaning) and 49 (postweaning). Nursing mother affected 10 genera in the colon and 3 minor genera in the jejunum. At day 14, Meishan sow-nursed piglets had lower Streptococcus suis and higher Cloacibacillus counts in the colonic digesta and larger amounts of interleukin 10 and Foxp3-positive cells in the colonic mucosa than did Yorkshire sow-nursed piglets. At day 49, nursing mother had no significant effects on cytokine expression. Breed effects were observed; Meishan piglets had lower relative abundances of Prevotella and lower gene expression of tumor necrosis factor alpha (TNF-?) than those of Yorkshire piglets at days 14 and 49. Collectively, nursing mother mainly affected preweaning colonic microbiota and immune status, while breed effects persisted after weaning. Piglets nursed by Meishan sows had different microbiota compositions and inflammatory cytokine profiles in the colon compared with those of piglets nursed by Yorkshire sows. These results highlight the different role of nursing mother and breed in affecting early gut microenvironment.IMPORTANCE Early-life gut microbiota and immune status are pivotal for postnatal growth. By using an interspecific cross-fostering piglet model, we find that change in nursing mother transiently reshapes preweaning colon microbiota and immune status, while breed shows persistent effects both pre- and postweaning. Piglets nursed by Meishan sows had lower Streptococcus suis counts and higher anti-inflammatory cytokine expression. These results highlight the significance of nursing mother in regulating early-life gut health.

SUBMITTER: Mu C

PROVIDER: S-EPMC6495758 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Differential Effects of Breed and Nursing on Early-Life Colonic Microbiota and Immune Status as Revealed in a Cross-Fostering Piglet Model.

Mu Chunlong C Bian Gaorui G Su Yong Y Zhu Weiyun W

Applied and environmental microbiology 20190418 9

Nursing mother and breed can differently regulate early-life microbiota succession in pigs. However, it remains unclear whether they affect gastrointestinal microbiota and immune status, which are critical for early-life gut health. Here, an interspecific cross-fostering piglet model was employed by fostering neonatal Yorkshire and Meishan piglets to the same or another breed of sows. Jejunal and colonic microbiotas and mucosal immune parameters were analyzed at postnatal days 14 (preweaning) an ...[more]

PMID: 30824438

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Project description:BackgroundDiarrhea is a major cause of reduced growth and mortality in piglets during the suckling and weaning periods and poses a major threat to the global pig industry. Diarrhea and gut dysbiosis may in part be prevented via improved early postnatal microbial colonization of the gut. To secure better postnatal gut colonization, we hypothesized that transplantation of colonic or gastric content from healthy donors to newborn recipients would prevent diarrhea in the recipients in the post-weaning period. Our objective was to examine the impact of transplanting colonic or gastric content on health and growth parameters and paraclinical parameters in recipient single-housed piglets exposed to a weaning transition and challenged with enterotoxigenic Escherichia coli (ETEC).MethodsSeventy-two 1-day-old piglets were randomized to four groups: colonic microbiota transplantation (CMT, n = 18), colonic content filtrate transplantation (CcFT, n = 18), gastric microbiota transplantation (GMT, n = 18), or saline (CON, n = 18). Inoculations were given on d 2 and 3 of life, and all piglets were milk-fed until weaning (d 20) and shortly after challenged with ETEC (d 24). We assessed growth, diarrhea prevalence, ETEC concentration, organ weight, blood parameters, small intestinal morphology and histology, gut mucosal function, and microbiota composition and diversity.ResultsEpisodes of diarrhea were seen in all groups during both the milk- and the solid-feeding phase, possibly due to stress associated with single housing. However, CcFT showed lower diarrhea prevalence on d 27, 28, and 29 compared to CON (all P < 0.05). CcFT also showed a lower ETEC prevalence on d 27 (P < 0.05). CMT showed a higher alpha diversity and a difference in beta diversity compared to CON (P < 0.05). Growth and other paraclinical endpoints were similar across groups.ConclusionIn conclusion, only CcFT reduced ETEC-related post-weaning diarrhea. However, the protective effect was marginal, suggesting that higher doses, more effective modalities of administration, longer treatment periods, and better donor quality should be explored by future research to optimize the protective effects of transplantation.

Project description:Dietary protein sources have the potential to affect the colon microbiome of piglets that will subsequently have a large impact on metabolic capabilities and hindgut health. This study explored the effects of different protein sources on the growth performance, diarrhea rate, apparent ileal digestibility (AID) of crude protein (CP), colonic mucin chemotypes, colonic microbiome, and microbial metabolites of piglets. Twenty-four piglets were randomly divided into four groups that received isoenergetic and isonitrogenous diets containing either Palbio 50 RD (P50), Soyppt-50% (S50), concentrated degossypolized cottonseed protein (CDCP), or fish meal (FM) as the sole protein source. The experimental diets did not affect the estimated daily gain (EDG), but P50 increased fecal score compared with S50 and CDCP. CDCP increased, but P50 reduced AID of CP in comparison to FM and S50. S50 and CDCP increased the amount of mixed neutral-acidic mucins relative to P50. Venn analysis identified unique OTUs in the P50 (13), CDCP (74), FM (39), and S50 (31) groups. The protein sources did not change the colonic bacterial richness or diversity. High Escherichia abundance in the P50 and FM, great abundant of Lactobacillus in the CDCP, and high Gemmiger abundance in the S50 were found. The CDCP tended to elevate valeric acid and branched chain fatty acid (BCFA) concentrations compared with the other diets. The P50 and FM groups had greater ammonia nitrogen and methylamine contents than the S50 and CDCP groups. There was a positive correlation between the Escherichia and ammonia nitrogen, the Lactobacillus and short chain fatty acid (SCFA), and a negative correlation between the Gemmige and BCFA. These findings suggested short-term feeding of different protein sources did not affect the piglets' growth, but P50 increased the diarrhea rate. Potential pathogenic bacteria and detrimental metabolites appeared in the colons of piglets fed P50 and FM, whereas, beneficial effects were conferred upon piglets fed CDCP and S50, thus indicating that available plant proteins (cotton seed, soy) added to the diets of piglets enhanced colon health by reducing protein fermentation.

Project description:The main purpose of the present study was to assess the effect of soluble and insoluble fiber on colonic bacteria and intestinal barrier function in a piglet model. A total of 24 piglets (25 ± 1 d old; 7.50 ± 0.31 kg) were randomly allotted to 4 treatments: basal diet (control, CON), 1% insoluble dietary fiber (IDF) diet, 1% soluble dietary fiber (SDF) diet, and 0.5% insoluble fiber + 0.5% soluble dietary fiber (MDF) diet. The trial lasted 28 days. SDF-fed piglets showed a higher (P < 0.05) bacterial a-diversity (observed_species, chao1, and ACE) and a higher relative abundance of Proteobacteria and Actinobacteria, Solobacterium, Succinivibrio, Blautia, and Atopobium in colonic digesta than CON, IDF, and MDF groups (P < 0.05). At the same time, Bacteroidetes, Euryarchaeota, Phascolarctobacterium, Coprococcus_1, and Prevotella_1 were significantly increased in the IDF group when compared with CON, SDF, and MDF groups (P < 0.05). Furthermore, Bacteroidetes and Enterobacteriaceae, Selenomonas, Phascolarctobacterium, and Alloprevotella(P < 0.05) were significantly higher in the MDF group than those in the other three groups (P < 0.05). SDF diet increased the concentrations of short-chain fatty acid (SCFA) in colonic digesta (P < 0.05) when compared with the CON group and enhanced weight index of the colon (P < 0.05) than the CON and IDF groups. Furthermore, compared with the CON group, SDF, IDF, and MDF diets all upregulated the mRNA expressions of claudin-1 (CLDN-1) in colonic mucosa (P < 0.05), SDF and IDF diets upregulated the mRNA expressions of mucin 2 (MUC2) (P < 0.05), SDF diet increased mRNA expressions of zonula occludens 1 (ZO-1) and occludin (OCLN), while the IDF group enhanced the secretory immunoglobulin A (sIgA) concentrations (P < 0.05), respectively. IDF and MDF diets decreased expressions of TNF-α(P < 0.05). We concluded that the influence of soluble fiber on colonic microbiota was more extensive than that of insoluble fiber. Moreover, soluble fiber could more effectively improve colonic barrier function by upregulating gene expressions of the gut barrier.

Project description:Probiotics can improve animal growth performance and intestinal health. Bacillus species, Lactobacillus species, Bifidobacterium species, yeast etc. are the common types of probiotics. However, understanding the effects of probiotics on the immune status and gut microbiota of weaning piglets and how the probiotics exert their impact are still limited. This study aimed to investigate the effects of Bacillus amyloliquefaciens 40 (BA40) on the performance, immune status and gut microbiota of piglets. A total of 12 litters of newborn piglets were randomly divided into 3 groups. Piglets in control group were orally dosed with phosphate buffered saline; BA40 group and probiotics group were orally gavaged with resuspension BA40 and a probiotics product, respectively. The results showed that BA40 treatment significantly decreased (P < 0.05) the diarrhea incidence (from d 5 to 40), diamine oxidase, D-lactate, interleukin (IL)-1β and interferon-γ concentrations compared with control group and probiotics group. Meanwhile BA40 dramatically increased the total antioxidant capacity, IL-10 and secretory immunoglobulin-A concentrations in contrast to control group. For the microbial composition, BA40 modulated the microbiota by improving the abundance of Bacteroides, Phascolarctobacterium (producing short-chain fatty acids) and Desulfovibrio and reducing the proliferation of pathogens (Streptococcus, Tyzzerella, Vellionella and paraeggerthella). Meanwhile, a metabolic function prediction explained that carbohydrate metabolism and amino acid metabolism enriched in BA40 group in contrast to control group and probiotics group. For correlation analysis, the results demonstrated that BA40-enriched Phascolarctobacterium and Desulfovibrio provide insights into strategies for elevating the health status and performance of weaned piglets. Altogether, BA40 exerted stronger ability in decreasing diarrhea incidence and improved antioxidant activity, gut barrier function and immune status of piglets than the other treatments. Our study provided the experimental and theoretical basis for the application of BA40 in pig production.

Dataset Information

Differential Effects of Breed and Nursing on Early-Life Colonic Microbiota and Immune Status as Revealed in a Cross-Fostering Piglet Model.

Publications

Differential Effects of Breed and Nursing on Early-Life Colonic Microbiota and Immune Status as Revealed in a Cross-Fostering Piglet Model.

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