Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows

Gut microbiome changed dramatically during pregnancy and played important roles in metabolic status and reproductive endocrinology in mammals. However, investigating the functional microbiota and metabolites to improve the reproductive performance and understanding the host–microbiota interaction ar...

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Main Authors: Qianhong Ye, Tingting Luo, Longshan Han, Yuwen Chen, Yifan Hu, Haoyi Jiang, Xiaojian Xu, Xianghua Yan
Format: Article
Language:English
Published: Cambridge University Press 2024-01-01
Series:Animal Nutriomics
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Online Access:https://www.cambridge.org/core/product/identifier/S2977377624000073/type/journal_article
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author Qianhong Ye
Tingting Luo
Longshan Han
Yuwen Chen
Yifan Hu
Haoyi Jiang
Xiaojian Xu
Xianghua Yan
author_facet Qianhong Ye
Tingting Luo
Longshan Han
Yuwen Chen
Yifan Hu
Haoyi Jiang
Xiaojian Xu
Xianghua Yan
author_sort Qianhong Ye
collection DOAJ
description Gut microbiome changed dramatically during pregnancy and played important roles in metabolic status and reproductive endocrinology in mammals. However, investigating the functional microbiota and metabolites to improve the reproductive performance and understanding the host–microbiota interaction are still arduous tasks. This study aims to reveal the dominant strains and metabolites that improve the reproductive performance. We analyzed the fecal microbiota composition and metabolic status of higher yield Chinese pig breed Meishan (MS) sows and lower yield but widespread raised hybrid pig breed Landrace × Yorkshire (L × Y) sows on days 28 and 100 of gestation. Results showed that MS sows had higher litter sizes and steroid hormone level but lower short-chain fatty acid level in feces. Fecal metabolomic analysis revealed that MS sows showed a different metabolic status compared with L × Y sows both at early and late pregnancy, which enriched with phenylpropanoid biosynthesis, bile secretion, steroid hormone biosynthesis, and plant secondary metabolite biosynthesis. In addition, 16S rDNA and internal transcribed spacer sequencing indicated that MS sows showed different structures of microbiota community and exhibited an increased bacterial α-diversity but non-differential fungal α-diversity than L × Y sows. Moreover, we found that the litter sizes and bacteria including Sphaerochaeta, Solibacillus, Oscillospira, Escherichia–Shigella, Prevotellaceae_UCG-001, dgA-11_gut_group, and Bacteroides, as well as fungi including Penicillium, Fusarium, Microascus, Elutherascus, and Heydenia both have positive association to the significant metabolites at the early pregnancy. Our findings revealed significant correlation between reproductive performance and gut microbiome and provided microbial and metabolic perspective to improve litter sizes and steroid hormones of sows.
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spelling doaj-art-9b0522256f654b37bafd58b338ea05e52025-08-20T03:03:11ZengCambridge University PressAnimal Nutriomics2977-37762977-37842024-01-01110.1017/anr.2024.7Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sowsQianhong Ye0https://orcid.org/0009-0002-7826-5458Tingting Luo1Longshan Han2Yuwen Chen3Yifan Hu4Haoyi Jiang5Xiaojian Xu6Xianghua Yan7https://orcid.org/0000-0003-2238-6218National Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety Technology, Wuhan, Hubei, ChinaGut microbiome changed dramatically during pregnancy and played important roles in metabolic status and reproductive endocrinology in mammals. However, investigating the functional microbiota and metabolites to improve the reproductive performance and understanding the host–microbiota interaction are still arduous tasks. This study aims to reveal the dominant strains and metabolites that improve the reproductive performance. We analyzed the fecal microbiota composition and metabolic status of higher yield Chinese pig breed Meishan (MS) sows and lower yield but widespread raised hybrid pig breed Landrace × Yorkshire (L × Y) sows on days 28 and 100 of gestation. Results showed that MS sows had higher litter sizes and steroid hormone level but lower short-chain fatty acid level in feces. Fecal metabolomic analysis revealed that MS sows showed a different metabolic status compared with L × Y sows both at early and late pregnancy, which enriched with phenylpropanoid biosynthesis, bile secretion, steroid hormone biosynthesis, and plant secondary metabolite biosynthesis. In addition, 16S rDNA and internal transcribed spacer sequencing indicated that MS sows showed different structures of microbiota community and exhibited an increased bacterial α-diversity but non-differential fungal α-diversity than L × Y sows. Moreover, we found that the litter sizes and bacteria including Sphaerochaeta, Solibacillus, Oscillospira, Escherichia–Shigella, Prevotellaceae_UCG-001, dgA-11_gut_group, and Bacteroides, as well as fungi including Penicillium, Fusarium, Microascus, Elutherascus, and Heydenia both have positive association to the significant metabolites at the early pregnancy. Our findings revealed significant correlation between reproductive performance and gut microbiome and provided microbial and metabolic perspective to improve litter sizes and steroid hormones of sows.https://www.cambridge.org/core/product/identifier/S2977377624000073/type/journal_articlelitter sizessteroid hormonesmicrobiotametabolomicssows
spellingShingle Qianhong Ye
Tingting Luo
Longshan Han
Yuwen Chen
Yifan Hu
Haoyi Jiang
Xiaojian Xu
Xianghua Yan
Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows
Animal Nutriomics
litter sizes
steroid hormones
microbiota
metabolomics
sows
title Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows
title_full Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows
title_fullStr Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows
title_full_unstemmed Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows
title_short Multi-omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows
title_sort multi omics analysis reveals the dominant intestinal microbial strains and metabolites related to the reproductive performance in pregnant sows
topic litter sizes
steroid hormones
microbiota
metabolomics
sows
url https://www.cambridge.org/core/product/identifier/S2977377624000073/type/journal_article
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AT longshanhan multiomicsanalysisrevealsthedominantintestinalmicrobialstrainsandmetabolitesrelatedtothereproductiveperformanceinpregnantsows
AT yuwenchen multiomicsanalysisrevealsthedominantintestinalmicrobialstrainsandmetabolitesrelatedtothereproductiveperformanceinpregnantsows
AT yifanhu multiomicsanalysisrevealsthedominantintestinalmicrobialstrainsandmetabolitesrelatedtothereproductiveperformanceinpregnantsows
AT haoyijiang multiomicsanalysisrevealsthedominantintestinalmicrobialstrainsandmetabolitesrelatedtothereproductiveperformanceinpregnantsows
AT xiaojianxu multiomicsanalysisrevealsthedominantintestinalmicrobialstrainsandmetabolitesrelatedtothereproductiveperformanceinpregnantsows
AT xianghuayan multiomicsanalysisrevealsthedominantintestinalmicrobialstrainsandmetabolitesrelatedtothereproductiveperformanceinpregnantsows