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Journal of Integrative Agriculture  2024, Vol. 23 Issue (6): 2033-2051    DOI: 10.1016/j.jia.2023.12.031
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Gut microbiome and serum metabolome analyses identify Bacteroides fragilis as regulators of serotonin content and PRL secretion in broody geese

Yu Zhang1, 2, Ning Zhou1, Jia Wu1, Lina Song1, Qiang Bao1, Kaiqi Weng1, Yang Zhang1, 2, Wanwipa Vongsangnak3, Guohong Chen1, 2, Qi Xu1, 2#

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

2Joint International Research Laboratory of Agriculture & Agri-Product Safety of Ministry of Education, Yangzhou University, Yangzhou 225009, China

3 Department of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand

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摘要  就巢行为是一种在家禽上常出现的母性行为,其受垂体分泌的催乳素的调控。这种就巢行为存在于大多数中国鹅品种中,并严重影响了母鹅的产蛋数量。大量研究表明动物行为受到特定肠道微生物与宿主之间通过脑--微生物轴的动态双向反馈的调节。然而,肠道微生物如何影响鹅就巢行为鲜有报道。在本研究中,我们检测了产蛋期与就巢期浙东白鹅相关激素水平,并进行了盲肠微生物宏基因组、16S rRNA与血清代谢组测序,以期鉴定出影响鹅就巢的关键肠道微生物,并阐明肠道微生物调控鹅催乳素分泌影响鹅就巢机制。

宏基因组与16S rRNA测序结果鉴定发现了产蛋鹅与就巢鹅存在十种丰度差异的关键菌群(P < 0.05),并确定了脆弱拟杆菌(Bacteroides fragilis)是鹅就巢的关键驱动因子。此外,血清代谢组发现产蛋鹅与就巢鹅之间存在313种差异代谢物,这些差异代谢物主要富集在色氨酸代谢途径中。Pearson相关分析表明,脆弱拟杆菌的丰度与就巢鹅中11种色氨酸代谢相关代谢物(如5-羟色胺等)的含量之间存在显著正相关,提示这些色氨酸代谢物可能由脆弱拟杆菌产生或驱动产生的。最后,我们检测了产蛋鹅与就巢鹅血清激素水平,发现脆弱拟杆菌的丰度与5-羟色胺含量呈正相关。此外,就巢鹅中垂体分泌的催乳素比产蛋鹅多,其也与脆弱拟杆菌的丰度高度相关。这一结果表明脆弱拟杆菌可能会促进垂体分泌更多的催乳素。综上所述,本研究发现脆弱拟杆菌为促进鹅就巢行为的关键驱动因子,脆弱拟杆菌可以通过提高血清中5-羟色胺水平来刺激垂体分泌催乳素,从而促进鹅就巢的行为发生。本研究为就巢行为的产生提供了新的视角,并为干预家禽就巢行为提供了新途径。



Abstract  

Broody behavior is regulated by hypothalamic prolactin secretion, which seriously affects egg production in poulty production.  Numerous studies have provided evidence that animal behavior is governed by dynamic bidirectional communication between specific gut bacteria and their host via the brain–gut–microbiome axis.  However, little research focused on how the gut microbiota influence broody behavior in poultry.  In this study, Zhedong white geese in laying and brooding phases were selected.  Ten differentially abundant bacteria in cecum were detected between brooding and laying geese through metagenomic analyses and 16S rRNA sequencing (P<0.05), and Bacteroides fragilis was specifically identified as a key driver species in the brooding geese.  Moverover, the serum metabolites were quantified, and the 313 differentially abundant metabolites were found between the two groups of different physiological geese.  They were primarily enriched in the tryptophan metabolism pathways.  Pearson correlation analyses revealed there was a significant positive correlation between Bfragilis abundance and the context of 11 tryptophan metabolism-related metabolites (such as serotonin, etc.) in broody geese, which hinted that those tryptophan metabolites might be produced or driven by Bfragilis.  Finally, the serum hormone levels were also measured.  We found there was a positive correlation between Bfragilis abundance and content of serotonin.  Besides, prolactin secreted by the pituitary gland was greater in brooding geese than that in laying geese, which was also highly correlated with Bfragilis abundance.  This result implied that Bfragilis could promote the secretion of prolactin by the pituitary gland.  Together, the current study findings provided the information on gut microbiota influencing broody behavior, Bfragilis produced or driven more serum serotonin, and stimulated the pituitary gland to secret more prolactin, which potentially offered a new enlightenment for the intervention of broody behavior in poultry.

Keywords:  Geese       Broody Behavior        Gut Microbiota        Serotonin        Prolactin   
Received: 07 February 2023   Accepted: 17 November 2023
Fund: This study was supported by the Modern Agro-industry Technology Research System, China (CARS-42-3), the “JBGS” Project of Seed Industry Revitalization in Jiangsu Province, China (JBGS (2021) 023) and the Project in Ministry of Agriculture and Rural Affairs of China (19211168).
About author:  Yu Zhang, E-mail: yuzhang@yzu.edu.cn; #Correspondence Qi Xu, E-mail: xuqi@yzu.edu.cn

Cite this article: 

Yu Zhang, Ning Zhou, Jia Wu, Lina Song, Qiang Bao, Kaiqi Weng, Yang Zhang, Wanwipa Vongsangnak, Guohong Chen, Qi Xu. 2024.

Gut microbiome and serum metabolome analyses identify Bacteroides fragilis as regulators of serotonin content and PRL secretion in broody geese . Journal of Integrative Agriculture, 23(6): 2033-2051.

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