Background:This study aimed to elucidate the molecular mechanisms of solid diet introduction initiating the cellular growth and maturation of rumen tissues and characterize the shared and unique biological processes u...Background:This study aimed to elucidate the molecular mechanisms of solid diet introduction initiating the cellular growth and maturation of rumen tissues and characterize the shared and unique biological processes upon different solid diet regimes.Methods:Twenty-four Hu lambs were randomly allocated to three groups fed following diets:goat milk powder only(M,n=8),goat milk powder+alfalfa hay(MH,n=8),and goat milk powder+concentrate starter(MC,n=8).At 42 days of age,the lambs were slaughtered.Ruminal fluid sample was collected for analysis of concentration of volatile fatty acid(VFA)and microbial crude protein(MCP).The sample of the rumen wall from the ventral sac was collected for analysis of rumen papilla morphology and transcriptomics.Results:Compared with the M group,MH and MC group had a higher concentration of VFA,MCP,rumen weight,and rumen papilla area.The transcriptomic results of rumen wall showed that there were 312 shared differentially expressed genes(DEGs)between in“MH vs.M”and“MC vs.M”,and 232 or 796 unique DEGs observed in“MH vs.M”or“MC vs.M”,respectively.The shared DEGs were most enriched in VFA absorption and metabolism,such as peroxisome proliferator-activated receptor(PPAR)signaling pathway,butanoate metabolism,and synthesis and degradation of ketone bodies.Additionally,a weighted gene co-expression network analysis identified M16(2,052 genes)and M18(579 genes)modules were positively correlated with VFA and rumen wall morphology.The M16 module was mainly related to metabolism pathway,while the M18 module was mainly associated with signaling transport.Moreover,hay specifically depressed expression of genes involved in cytokine production,immune response,and immunocyte activation,and concentrate starter mainly altered nutrient transport and metabolism,especially ion transport,amino acid,and fatty acid metabolism.Conclusions:The energy production during VFA metabolism may drive the rumen wall development directly.The hay introduction facilitated establishment of immune function,while the concentrate starter enhanced nutrient transport and metabolism,which are important biological processes required for rumen development.展开更多
The rumen is an important organ that enables ruminants to digest nutrients. However, the biological mechanism by which the microbiota and its derived fatty acids regulate rumen development is still unclear. In this st...The rumen is an important organ that enables ruminants to digest nutrients. However, the biological mechanism by which the microbiota and its derived fatty acids regulate rumen development is still unclear. In this study, 18 female Haimen goats were selected and slaughtered at d 30, 60, and 90 of age.Multi-omics analyses(rumen microbial sequencing, host transcriptome sequencing, and rumen epithelial metabolomics) were performed to investigate host-microbe interactions from preweaning to postweaning in a goat model. With increasing age, and after the introduction of solid feed, the increased abundances of Prevotella and Roseburia showed positive correlations with volatile fatty acid(VFA) levels and morphological parameters(P < 0.05). Epithelial transcriptomic analysis showed that the expression levels of hub genes, including 3-hydroxy-3-methylglutaryl-CoA synthase isoform 2(HMGCS2), enoyl-CoA hydratase, short chain 1(ECHS1), and peroxisome proliferator activated receptor gamma(PPARG), were positively associated with animal phenotype(P < 0.05). These hub genes were mainly correlated to VFA metabolism, oxidative phosphorylation, and the mammalian target of rapamycin(mTOR) and peroxisome proliferator activated receptor(PPAR) signaling pathways(P < 0.05). Moreover, the primary metabolites in the epithelium changed from glucose preweaning to(R)-3-hydroxybutyric acid(BHBA) and acetoacetic acid(ACAC) postweaning(P < 0.05). Diet and butyrate were the major factors shaping epithelial metabolomics in young ruminants(P < 0.05). Multi-omics analysis showed that the rumen microbiota and VFA were mainly associated with the epithelial transcriptome, and that alterations in gene expression influenced host metabolism. The “butanoate metabolism” pathway, which transcriptomic and metabolomic analyses identified as being upregulated with age, produces ketones that regulate the “oxidative phosphorylation” pathway, which could provide energy for the development of rumen papillae. Our findings reveal the changes that occur in the rumen microbiota, host transcriptome,and metabolome with age, and validate the role of microbiota-derived VFA in manipulating host gene expression and subsequent metabolism. This study provides insight into the molecular mechanisms of host-microbe interactions in goats and supplies a theoretical basis and guidance for precise nutritional regulation during the critical time window for rumen development of young ruminants.展开更多
基金This work was supported by the Project for Top Young Talents Program of College of Animal Science and Technology of Nanjing Agricultural University(DKQB201904)National Key Research and Development Plan(2018YFD0501900)+1 种基金Postgraduate Research&Practice Innovation Program of Jiangsu Province(KYCX20_0603)Science and Technology Project of Huzhou City of China(2017GY18).
文摘Background:This study aimed to elucidate the molecular mechanisms of solid diet introduction initiating the cellular growth and maturation of rumen tissues and characterize the shared and unique biological processes upon different solid diet regimes.Methods:Twenty-four Hu lambs were randomly allocated to three groups fed following diets:goat milk powder only(M,n=8),goat milk powder+alfalfa hay(MH,n=8),and goat milk powder+concentrate starter(MC,n=8).At 42 days of age,the lambs were slaughtered.Ruminal fluid sample was collected for analysis of concentration of volatile fatty acid(VFA)and microbial crude protein(MCP).The sample of the rumen wall from the ventral sac was collected for analysis of rumen papilla morphology and transcriptomics.Results:Compared with the M group,MH and MC group had a higher concentration of VFA,MCP,rumen weight,and rumen papilla area.The transcriptomic results of rumen wall showed that there were 312 shared differentially expressed genes(DEGs)between in“MH vs.M”and“MC vs.M”,and 232 or 796 unique DEGs observed in“MH vs.M”or“MC vs.M”,respectively.The shared DEGs were most enriched in VFA absorption and metabolism,such as peroxisome proliferator-activated receptor(PPAR)signaling pathway,butanoate metabolism,and synthesis and degradation of ketone bodies.Additionally,a weighted gene co-expression network analysis identified M16(2,052 genes)and M18(579 genes)modules were positively correlated with VFA and rumen wall morphology.The M16 module was mainly related to metabolism pathway,while the M18 module was mainly associated with signaling transport.Moreover,hay specifically depressed expression of genes involved in cytokine production,immune response,and immunocyte activation,and concentrate starter mainly altered nutrient transport and metabolism,especially ion transport,amino acid,and fatty acid metabolism.Conclusions:The energy production during VFA metabolism may drive the rumen wall development directly.The hay introduction facilitated establishment of immune function,while the concentrate starter enhanced nutrient transport and metabolism,which are important biological processes required for rumen development.
基金funded by grants from National Natural Science Foundation of China(31872385)Foshan Postdoctoral Sustentation Fund(BKS209151)+1 种基金the Inner Mongolia Science and Technology Key Project(2021SZD0014)the National Key R&D Program Projects(2018YFD0501902)。
文摘The rumen is an important organ that enables ruminants to digest nutrients. However, the biological mechanism by which the microbiota and its derived fatty acids regulate rumen development is still unclear. In this study, 18 female Haimen goats were selected and slaughtered at d 30, 60, and 90 of age.Multi-omics analyses(rumen microbial sequencing, host transcriptome sequencing, and rumen epithelial metabolomics) were performed to investigate host-microbe interactions from preweaning to postweaning in a goat model. With increasing age, and after the introduction of solid feed, the increased abundances of Prevotella and Roseburia showed positive correlations with volatile fatty acid(VFA) levels and morphological parameters(P < 0.05). Epithelial transcriptomic analysis showed that the expression levels of hub genes, including 3-hydroxy-3-methylglutaryl-CoA synthase isoform 2(HMGCS2), enoyl-CoA hydratase, short chain 1(ECHS1), and peroxisome proliferator activated receptor gamma(PPARG), were positively associated with animal phenotype(P < 0.05). These hub genes were mainly correlated to VFA metabolism, oxidative phosphorylation, and the mammalian target of rapamycin(mTOR) and peroxisome proliferator activated receptor(PPAR) signaling pathways(P < 0.05). Moreover, the primary metabolites in the epithelium changed from glucose preweaning to(R)-3-hydroxybutyric acid(BHBA) and acetoacetic acid(ACAC) postweaning(P < 0.05). Diet and butyrate were the major factors shaping epithelial metabolomics in young ruminants(P < 0.05). Multi-omics analysis showed that the rumen microbiota and VFA were mainly associated with the epithelial transcriptome, and that alterations in gene expression influenced host metabolism. The “butanoate metabolism” pathway, which transcriptomic and metabolomic analyses identified as being upregulated with age, produces ketones that regulate the “oxidative phosphorylation” pathway, which could provide energy for the development of rumen papillae. Our findings reveal the changes that occur in the rumen microbiota, host transcriptome,and metabolome with age, and validate the role of microbiota-derived VFA in manipulating host gene expression and subsequent metabolism. This study provides insight into the molecular mechanisms of host-microbe interactions in goats and supplies a theoretical basis and guidance for precise nutritional regulation during the critical time window for rumen development of young ruminants.
