Multiomics integration identifies regulatory factors underlying reproductive disorders in geese

doi:10.1016/j.jia.2024.05.030

Journal of Integrative Agriculture

2026, Vol. 25

Issue (7): 2936-2949 DOI: 10.1016/j.jia.2024.05.030

Animal Science · Veterinary Medicine

Advanced Online Publication | Current Issue | Archive | Adv Search

Multiomics integration identifies regulatory factors underlying reproductive disorders in geese

Qingyuan Ouyang^{1, 2*}, Cong Lan^3*, Shenqiang Hu^{1, 2*}, Haizhou Gong⁴, Bincheng Tang^{1, 2}, Qingliang Chen^{1, 2}, Zhiyu He^{1, 2}, Junqi Wang^{1, 2}, Tanze Liu^{1, 2}, Shangmin Wang^{1, 2}, Xi Zhang^{1, 2}, Jiwei Hu^{1, 2}, Hua He^{1, 2}, Liang Li^{1, 2}, Hehe Liu^{1, 2}, Jiwen Wang^{1, 2#}

¹State Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China

²Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China

³Engineering Research Center of Animal Disease-Resistance Nutrition Biotechnology of Ministry of Education of China, Animal Nutrtition Institute, Sichuan Agricultural University, Chengdu 611130, China

⁴College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China

Highlights
● Multi-omic characterization of reproductive disorders (RD): Integrative ovarian anatomical, histological, and transcriptomic profiling reveals the underlying pathogenic mechanisms of RD in geese, establishing a foundational model for studying avian reproductive health.
● Bile acid metabolism as a core driver: Genetic mutations in bile acid metabolism genes disrupt circulating chenodeoxycholic acid (CDCA) levels, directly linking bile acid dysregulation to the pathogenesis of RD.
● CDCA-microbiota axis in RD progression: Elevated CDCA selectively promotes the proliferation of Romboutsia lituseburensis in the ileum, demonstrating a causal pathway from host metabolic alteration to gut microbiota dysbiosis and subsequent reproductive impairment.

Abstract
References

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摘要鹅是候鸟的后代，保留了其野生祖先独特的繁殖和脂质代谢特性。因此，与其他家禽相比，鹅的产蛋能力较低，并且对脂肪肝的易感性更高。最近的研究强调了脂质代谢紊乱对雌性生殖健康的影响。在此背景下，我们观察到某些鹅群体存在繁殖障碍（RD）和脂质代谢异常。本研究系统阐明了RD鹅和正常鹅在基因组学、转录组学、胆汁酸代谢组学和微生物组学等多个层次的差异，揭示了微生物在其中的关键作用。我们的研究对正常鹅和RD鹅的卵巢解剖、组织学和转录组进行了详细的检查。基因组分析定位了与胆汁酸代谢相关的基因突变，突显了它们在RD病因中的潜在作用。这些发现在随后的胆汁酸测定和回肠转录组分析得到了中得到了佐证，揭示了胆汁酸吸收的显著破坏、FXR的激活以及RD鹅血清鹅脱氧胆酸（CDCA）浓度的增加。值得注意的是，16S rRNA测序发现RD鹅回肠微生物群的beta多样性显著高于正常组。Wilcoxon秩和检验和LEfSe分析都突出了RD鹅中Romboutsia丰度的显著增加。CDCA补充的体外微生物培养实验证实了CDCA对Romboutsia lituseburensis（R. lituseburensis）增殖的影响。R. lituseburensis的灌胃实验阐明了其通过免疫介导途径参与初级卵泡减少的作用。总体而言，我们多方面的分析揭示了Romboutsia在鹅RD中复杂的参与机制，从基因、生理和微生物维度提供了见解。我们的研究结果不仅加深了对鹅RD病因的理解，还建议了通过靶向胆汁酸代谢和特定微生物组成分调节的潜在治疗途径。

Abstract

Geese, descendants of migratory birds, have preserved the distinct reproductive and lipid metabolism traits of their wild ancestors. Therefore, compared to other poultry, geese have lower egg production ability and greater susceptibility to fatty liver. Recent research underscores the impact of lipid metabolism disorders on female reproductive health. In this context, we observed reproductive disorders (RD) and lipid metabolism anomalies in certain geese populations. This study systematically elucidated the differences between RD and normal geese at various levels, including genomics, transcriptomics, bile acid metabolomics, and microbiomics, revealing the crucial role of microorganisms. Our study provides a thorough examination of the ovarian anatomical, histological, and transcriptomic profiles between normal and RD geese. Genomic analyses pinpoint mutations in genes associated with bile acid metabolism, highlighting their potential role in RD pathogenesis. The genomic discoveries are substantiated by precise bile acid assays and ileum transcriptome analyses, which expose a significant disruption in bile acid absorption, activation of FXR, and an increase in serum chenodeoxycholic acid (CDCA) concentrations within RD geese. Notably, 16S rRNA sequencing uncovers significantly greater beta diversity in the ileum microbiota of RD geese than in the normal group. Both Wilcoxon rank sum test and LEfSe analyses highlighted a marked increase in Romboutsia abundance in RD geese. Experimental cultivation of microbiota with CDCA supplementation confirms the impact of CDCA on Romboutsia lituseburensis proliferation. Gavage experiments with R. lituseburensis elucidate its involvement in primary follicle reduction via immune-mediated pathways. Collectively, our multifaceted analysis unravels the intricate involvement of Romboutsia in goose RD, offering insights from genetic, physiological, and microbial dimensions. Our findings not only deepen understanding of the etiology of RD in geese but also suggest potential avenues for therapeutic interventions targeting bile acid metabolism and modulation of specific microbiota components.

Keywords: goose bile acid gut microbiota reproduction dysfunction

Received: 10 April 2024 Accepted: 15 May 2024 Online: 14 June 2024

Fund: This research was supported by China Agriculture Research System of MOF and MARA (CARS-42-4) and Key Technology Support Program of Sichuan Province, China (2021YFYZ0014) for the financial support.

About author: Qingyuan Ouyang, E-mail: oyqy222@163.com; Cong Lan, E-mail: clarencelan7777@163.com; Shenqiang Hu, E-mail: sqhu2011@163.com; #Correspondence Jiwen Wang, Tel: +86-28-86293073, E-mail: wjw2886166@163.com * These authors contributed equally to this study.

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Qingyuan Ouyang, Cong Lan, Shenqiang Hu, Haizhou Gong, Bincheng Tang, Qingliang Chen, Zhiyu He, Junqi Wang, Tanze Liu, Shangmin Wang, Xi Zhang, Jiwei Hu, Hua He, Liang Li, Hehe Liu, Jiwen Wang. 2026. Multiomics integration identifies regulatory factors underlying reproductive disorders in geese. Journal of Integrative Agriculture, 25(7): 2936-2949.

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