Biogeographical distribution of gut microbiome composition and function is partially recapitulated by fecal transplantation into germ-free mice

Julianne C Yang, Venu Lagishetty, Ezinne Aja, Nerea Arias-Jayo, Candace Chang, Megan Hauer, William Katzka, Yi Zhou, Farzaneh Sedighian, Carolina Koletic, Fengting Liang, Tien S Dong, Jamilla Situ, Ryan Troutman, Heidi Buri, Shrikant Bhute, Carra A Simpson, Jonathan Braun, Noam Jacob, Jonathan P Jacobs
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Abstract

Fecal microbiota transplantation has been vital for establishing whether host phenotypes can be conferred through the microbiome. However, whether the existing microbial ecology along the mouse gastrointestinal tract can be recapitulated in germ-free mice colonized with stool remains unknown. We first identified microbes and their predicted functions specific to each of six intestinal regions in three cohorts of specific pathogen-free mice spanning two facilities. Of these region-specific microbes, the health-linked genus Akkermansia was consistently enriched in the lumen of the small intestine compared to the colon. Predictive functional modeling on 16S rRNA gene amplicon sequencing data recapitulated in shotgun sequencing data revealed increased microbial central metabolism, lipolytic fermentation, and cross-feeding in the small intestine, whereas butyrate synthesis was colon-enriched. Neuroactive compound metabolism also demonstrated regional specificity, including small intestine-enriched gamma-aminobutyric acid degradation and colon-enriched tryptophan degradation. Specifically, the jejunum and ileum stood out as sites with high predicted metabolic and neuromodulation activity. Differences between luminal and mucosal microbiomes within each site of the gastrointestinal tract were largely facility-specific, though there were a few consistent patterns in microbial metabolism in specific pathogen-free mice. These included luminal enrichment of central metabolism and cross-feeding within both the small intestine and the colon, and mucosal enrichment of butyrate synthesis within the colon. Across three cohorts of germ-free mice colonized with mice or human stool, compositional and functional region specificity were inconsistently reproduced. These results underscore the importance of investigating the spatial variation of the gut microbiome to better understand its impact on host physiology.
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将粪便移植到无菌小鼠体内可部分重现肠道微生物组组成和功能的生物地理分布
粪便微生物群移植对于确定宿主表型是否可通过微生物群遗传至关重要。然而,小鼠胃肠道现有的微生物生态是否能在无菌小鼠的粪便定植中重现仍是未知数。我们首先在跨越两个设施的三组特异性无病原体小鼠中确定了六个肠道区域的特异性微生物及其预测功能。在这些区域特异性微生物中,与结肠相比,与健康相关的 Akkermansia 属在小肠腔内持续富集。16S rRNA 基因扩增子测序数据的预测功能建模再现了霰弹枪测序数据,显示小肠中微生物中心代谢、脂肪分解发酵和交叉采食增加,而丁酸合成则富集于结肠。神经活性化合物代谢也表现出区域特异性,包括小肠富含的γ-氨基丁酸降解和结肠富含的色氨酸降解。具体而言,空肠和回肠是预测代谢和神经调节活性较高的部位。胃肠道每个部位的管腔和粘膜微生物组之间的差异主要是设施特异性的,但特定无病原体小鼠的微生物代谢有一些一致的模式。这些模式包括小肠和结肠的管腔富集中心代谢和交叉摄食,以及结肠粘膜富集丁酸合成。在用小鼠或人类粪便定植的三组无菌小鼠中,成分和功能区特异性的再现并不一致。这些结果强调了研究肠道微生物组的空间变化以更好地了解其对宿主生理影响的重要性。
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