Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition.

IF 4 2区 生物学 Q2 MICROBIOLOGY Frontiers in Microbiology Pub Date : 2025-01-15 eCollection Date: 2024-01-01 DOI:10.3389/fmicb.2024.1441126
Bruno K Rodiño-Janeiro, Olfat Khannous-Lleiffe, Marc Pigrau, Jesse R Willis, Eloísa Salvo-Romero, Adoración Nieto, Elba Expósito, Marina Fortea, Cristina Pardo-Camacho, Mercé Albert-Bayo, Ana María González-Castro, Danila Guagnozzi, Cristina Martínez, Beatriz Lobo, María Vicario, Javier Santos, Toni Gabaldón, Carmen Alonso-Cotoner
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Abstract

Background/aims: Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress. However, whether this is associated with changes in the small bowel microbiota remains unknown. We have evaluated changes in the small intestinal microbiota in response to acute stress to better understand stress-induced intestinal barrier dysfunction.

Methods: Jejunal biopsies were obtained at baseline and 90 min after cold pain or sham stress. Autonomic (blood pressure and heart rate), hormonal (plasma cortisol and adrenocorticotropic hormone) and psychological (Subjective Stress Rating Scale) responses to cold pain and sham stress were monitored. Microbial DNA from the biopsies was analyzed using a 16S metabarcoding approach before and after cold pain stress and sham stress. Differences in diversity and relative abundance of microbial taxa were examined.

Results: Cold pain stress was associated with a significant decrease in alpha diversity (P = 0.015), which was more pronounced in females, along with significant sex differences in the abundance of specific taxa and the overall microbiota composition. Microbiota alterations significantly correlated with changes in psychological responses, hormones, and gene expression in the intestinal mucosal. Cold pain stress was also associated with activation of autonomic, hormonal and psychological response, with no differences between sexes.

Conclusions: Acute stress elicits rapid alterations in bacterial composition in the jejunum of healthy subjects and these changes are more pronounced in females. Our results may contribute to the understanding of female predominance in DGBI.

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急性应激触发人类小肠微生物群组成的性别依赖性快速改变。
背景/目的:肠脑相互作用消化障碍(DGBI)非常常见,主要发生在女性中,通常与肠屏障功能障碍、生态失调和应激有关。我们之前发现,在急性应激反应中,女性对肠道屏障功能障碍的易感性增加。然而,这是否与小肠微生物群的变化有关尚不清楚。我们评估了小肠微生物群对急性应激反应的变化,以更好地了解应激诱导的肠道屏障功能障碍。方法:在基线和冷痛或假应激后90min分别进行空肠活检。监测自主神经(血压和心率)、激素(血浆皮质醇和促肾上腺皮质激素)和心理(主观应激评定量表)对冷痛和假应激的反应。在冷痛应激和假应激前后,采用16S元条形码方法分析活检组织的微生物DNA。微生物分类群的多样性和相对丰度存在差异。结果:冷痛应激与α多样性的显著降低相关(P = 0.015),在雌性中更为明显,并且在特定分类群的丰度和总体微生物群组成上存在显著的性别差异。肠道菌群的改变与肠黏膜的心理反应、激素和基因表达的变化显著相关。冷痛压力还与自主神经、荷尔蒙和心理反应的激活有关,性别之间没有差异。结论:急性应激引起健康受试者空肠细菌组成的快速变化,这种变化在女性中更为明显。我们的结果可能有助于理解女性在DGBI中的优势。
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来源期刊
CiteScore
7.70
自引率
9.60%
发文量
4837
审稿时长
14 weeks
期刊介绍: Frontiers in Microbiology is a leading journal in its field, publishing rigorously peer-reviewed research across the entire spectrum of microbiology. Field Chief Editor Martin G. Klotz at Washington State University is supported by an outstanding Editorial Board of international researchers. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide.
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