Multi-omics analysis reveals gut microbiota-ovary axis contributed to the follicular development difference between Meishan and Landrace × Yorkshire sows

Journal of Animal Science and Biotechnology

Research

Xianghua Yan¹  Juncheng Huang¹  Shuyi Zhou¹  Wenxia Qin¹  Yimei Tang¹  Yuwen Chen¹  Libao Ma¹  Baoyang Xu¹ 

[1] State Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural University, 430070, Wuhan, Hubei, China;The Cooperative Innovation Center for Sustainable Pig Production, 430070, Wuhan, Hubei, China;Hubei Provincial Engineering Laboratory for Pig Precision Feeding and Feed Safety, 430070, Wuhan, Hubei, China;

关键词: Follicular development;    Granulosa cells apoptosis;    Gut microbiota;    Short-chain fatty acids;    Sows;   

DOI  :  10.1186/s40104-023-00865-w

 received in 2022-11-04, accepted in 2023-03-09,  发布年份 2023

来源: Springer

【 摘 要 】

BackgroundThe mechanism by which Meishan (MS) sows are superior to white crossbred sows in ovarian follicle development remains unclear. Given gut microbiota could regulate female ovarian function and reproductive capacity, this study aimed to determine the role of gut microbiota-ovary axis on follicular development in sows.MethodsWe compared the ovarian follicular development, gut microbiota, plasma metabolome, and follicular fluid metabolome between MS and Landrace × Yorkshire (L × Y) sows. A H2O2-induced cell apoptosis model was used to evaluate the effects of multi-omics identified metabolites on the apoptosis of porcine ovarian granulosa cells in vitro.ResultsCompared with L × Y sows, MS sows have greater ovary weight and improved follicular development, including the greater counts of large follicles of diameter ≥ 5 mm, secondary follicles, and antral follicles, but lesser atretic follicles. The ovarian granulosa cells in MS sows had alleviated apoptosis, which was indicated by the increased BCL-2, decreased caspases-3, and decreased cleaved caspases-3 than in L × Y sows. The ovarian follicular fluid of MS sows had higher concentrations of estradiol, progesterone, follicle-stimulating hormone, luteinizing hormone, and insulin like growth factor 1 than L × Y sows. Gut microbiota of MS sows formed a distinct cluster and had improved alpha diversity, including increased Shannon and decreased Simpson than those of L × Y sows. Corresponding to the enhanced function of carbohydrate metabolism and elevated short-chain fatty acids (SCFAs) in feces, the differential metabolites in plasma between MS and L × Y sows are also mainly enriched in pathways of fatty acid metabolism. There were significant correlations among SCFAs with follicular development, ovarian granulosa cells apoptosis, and follicular fluid hormones, respectively. Noteworthily, compared with L × Y sows, MS sows had higher follicular fluid SCFAs concentrations which could ameliorate H2O2-induced porcine granulosa cells apoptosis in vitro.ConclusionMS sows have more secondary and antral follicles, but fewer atretic follicles and apoptotic ovarian granulosa cells, as well as harbored a distinctive gut microbiota than L × Y sows. Gut microbiota may participate in regulating ovarian follicular development via SCFAs affecting granulosa cells apoptosis in sows.

【 授权许可】

CC BY   
© The Author(s) 2023

【 图 表 】

Fig. 2

41116_2023_36_Article_IEq753.gif

41116_2023_36_Article_IEq413.gif

41116_2023_36_Article_IEq337.gif

41116_2023_36_Article_IEq238.gif

41116_2023_36_Article_IEq119.gif

Fig. 4