Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats

Abstract Background Preweaned rumen development is vital for animal health and efficient fermentation. In this study, we integrated ruminal transcriptomic and metagenomic data to explore the dynamics of rumen functions, microbial colonization, and their functional interactions during the first 8 wee...

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Main Authors: Xiangyu Pan, Zongjun Li, Bibo Li, Chen Zhao, Yu Wang, Yulin Chen, Yu Jiang
Format: Article
Language:English
Published: BMC 2021-04-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-021-07595-1
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author Xiangyu Pan
Zongjun Li
Bibo Li
Chen Zhao
Yu Wang
Yulin Chen
Yu Jiang
author_facet Xiangyu Pan
Zongjun Li
Bibo Li
Chen Zhao
Yu Wang
Yulin Chen
Yu Jiang
author_sort Xiangyu Pan
collection DOAJ
description Abstract Background Preweaned rumen development is vital for animal health and efficient fermentation. In this study, we integrated ruminal transcriptomic and metagenomic data to explore the dynamics of rumen functions, microbial colonization, and their functional interactions during the first 8 weeks of life in goats. Results The dynamic rumen transcriptomic and microbial profiles both exhibited two distinct phases during early rumen development. The differentially expressed genes of the rumen transcriptome between the two phases showed that the immune-related response was enriched in the first phase and nutrient-related metabolism was enriched in the second phase, whereas the differentially expressed genes of the rumen microbiome were enriched in bacteriocin biosynthesis and glycolysis/gluconeogenesis activities. The developmental shift in the rumen transcriptome (at d 21) was earlier than the feed stimulus (at d 25) and the shift in the rumen microbiome (at d 42). Additionally, 15 temporal dynamic rumen gene modules and 20 microbial modules were revealed by coexpression network analysis. Functional correlations between the rumen and its microbiome were primarily involved in rumen pH homeostasis, nitrogen metabolism and the immune response. Rumen gene modules associated with the microbial alpha diversity index were also enriched in the immune response process. Conclusions The present study touched the critical developmental process of rumen functions, microbial colonization and their functional interactions during preweaned development. Taken together, these results demonstrated that rumen development at the first phase is more likely a programmed process rather than stimulation from feed and the microbiome, while the shift of rumen metagenomes was likely regulated by both the diet and host. The intensive functional correlations between rumen genes and the microbiome demonstrated that synergistic processes occurred between them during early rumen development.
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spelling doaj.art-c8c0e2efa9444552ae780eeaaad2f23f2022-12-21T19:41:16ZengBMCBMC Genomics1471-21642021-04-0122111510.1186/s12864-021-07595-1Dynamics of rumen gene expression, microbiome colonization, and their interplay in goatsXiangyu Pan0Zongjun Li1Bibo Li2Chen Zhao3Yu Wang4Yulin Chen5Yu Jiang6Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityAbstract Background Preweaned rumen development is vital for animal health and efficient fermentation. In this study, we integrated ruminal transcriptomic and metagenomic data to explore the dynamics of rumen functions, microbial colonization, and their functional interactions during the first 8 weeks of life in goats. Results The dynamic rumen transcriptomic and microbial profiles both exhibited two distinct phases during early rumen development. The differentially expressed genes of the rumen transcriptome between the two phases showed that the immune-related response was enriched in the first phase and nutrient-related metabolism was enriched in the second phase, whereas the differentially expressed genes of the rumen microbiome were enriched in bacteriocin biosynthesis and glycolysis/gluconeogenesis activities. The developmental shift in the rumen transcriptome (at d 21) was earlier than the feed stimulus (at d 25) and the shift in the rumen microbiome (at d 42). Additionally, 15 temporal dynamic rumen gene modules and 20 microbial modules were revealed by coexpression network analysis. Functional correlations between the rumen and its microbiome were primarily involved in rumen pH homeostasis, nitrogen metabolism and the immune response. Rumen gene modules associated with the microbial alpha diversity index were also enriched in the immune response process. Conclusions The present study touched the critical developmental process of rumen functions, microbial colonization and their functional interactions during preweaned development. Taken together, these results demonstrated that rumen development at the first phase is more likely a programmed process rather than stimulation from feed and the microbiome, while the shift of rumen metagenomes was likely regulated by both the diet and host. The intensive functional correlations between rumen genes and the microbiome demonstrated that synergistic processes occurred between them during early rumen development.https://doi.org/10.1186/s12864-021-07595-1Rumen developmentRumen transcriptomeMicrobiomeRumen-microbial crosstalk
spellingShingle Xiangyu Pan
Zongjun Li
Bibo Li
Chen Zhao
Yu Wang
Yulin Chen
Yu Jiang
Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats
BMC Genomics
Rumen development
Rumen transcriptome
Microbiome
Rumen-microbial crosstalk
title Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats
title_full Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats
title_fullStr Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats
title_full_unstemmed Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats
title_short Dynamics of rumen gene expression, microbiome colonization, and their interplay in goats
title_sort dynamics of rumen gene expression microbiome colonization and their interplay in goats
topic Rumen development
Rumen transcriptome
Microbiome
Rumen-microbial crosstalk
url https://doi.org/10.1186/s12864-021-07595-1
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AT chenzhao dynamicsofrumengeneexpressionmicrobiomecolonizationandtheirinterplayingoats
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