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Ecological memory of prior nutrient exposure in the human gut microbiome
The ISME Journal ( IF 11.0 ) Pub Date : 2022-07-23 , DOI: 10.1038/s41396-022-01292-x
Jeffrey Letourneau 1 , Zachary C Holmes 1 , Eric P Dallow 1 , Heather K Durand 1 , Sharon Jiang 1 , Verónica M Carrion 2 , Savita K Gupta 1 , Adam C Mincey 3 , Michael J Muehlbauer 3 , James R Bain 3, 4 , Lawrence A David 1, 5
Affiliation  

Many ecosystems have been shown to retain a memory of past conditions, which in turn affects how they respond to future stimuli. In microbial ecosystems, community disturbance has been associated with lasting impacts on microbiome structure. However, whether microbial communities alter their response to repeated stimulus remains incompletely understood. Using the human gut microbiome as a model, we show that bacterial communities retain an “ecological memory” of past carbohydrate exposures. Memory of the prebiotic inulin was encoded within a day of supplementation among a cohort of human study participants. Using in vitro gut microbial models, we demonstrated that the strength of ecological memory scales with nutrient dose and persists for days. We found evidence that memory is seeded by transcriptional changes among primary degraders of inulin within hours of nutrient exposure, and that subsequent changes in the activity and abundance of these taxa are sufficient to enhance overall community nutrient metabolism. We also observed that ecological memory of one carbohydrate species impacts microbiome response to other carbohydrates, and that an individual’s habitual exposure to dietary fiber was associated with their gut microbiome’s efficiency at digesting inulin. Together, these findings suggest that the human gut microbiome’s metabolic potential reflects dietary exposures over preceding days and changes within hours of exposure to a novel nutrient. The dynamics of this ecological memory also highlight the potential for intra-individual microbiome variation to affect the design and interpretation of interventions involving the gut microbiome.



中文翻译:

人类肠道微生物组中先前营养暴露的生态记忆

许多生态系统已被证明可以保留对过去条件的记忆,这反过来会影响它们对未来刺激的反应。在微生物生态系统中,群落干扰与对微生物组结构的持久影响有关。然而,微生物群落是否会改变它们对重复刺激的反应仍然不完全清楚。使用人类肠道微生物组作为模型,我们表明细菌群落保留了过去碳水化合物暴露的“生态记忆”。在一组人类研究参与者中,益生元菊粉的记忆在一天内被编码。使用体外肠道微生物模型,我们证明了生态记忆的强度与营养剂量成比例并持续数天。我们发现有证据表明,在暴露于营养物质的数小时内,菊粉的主要降解者之间的转录变化会播种记忆,并且这些类群的活性和丰度的后续变化足以增强整个群落的营养代谢。我们还观察到,一种碳水化合物的生态记忆会影响微生物组对其他碳水化合物的反应,并且个人习惯性地接触膳食纤维与其肠道微生物组消化菊粉的效率有关。总之,这些研究结果表明,人类肠道微生物组的代谢潜力反映了前几天的饮食暴露以及暴露于新营养素数小时内的变化。

更新日期:2022-07-23
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