Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC, USA.
Duke Office of Clinical Research, Duke University School of Medicine, Durham, NC, USA.
ISME J. 2022 Nov;16(11):2479-2490. doi: 10.1038/s41396-022-01292-x. Epub 2022 Jul 23.
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.
许多生态系统被证明能够保留对过去条件的记忆，而这些记忆反过来又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不完全清楚。我们以人类肠道微生物组为模型，表明细菌群落保留了对过去碳水化合物暴露的“生态记忆”。在一群人类研究参与者中，补充菊粉后的一天内就记录到了对这种益生元的记忆。使用体外肠道微生物模型，我们证明生态记忆的强度与营养剂量成正比，并持续数天。我们发现证据表明，记忆是由营养物质暴露后数小时内菊粉主要降解者之间的转录变化引发的，而这些分类群的后续活性和丰度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，并且个体对膳食纤维的习惯性暴露与其肠道微生物组消化菊粉的效率有关。总之，这些发现表明，人类肠道微生物组的代谢潜力反映了前几天的饮食暴露情况，并在暴露于新营养素后的数小时内发生变化。这种生态记忆的动态也突出了个体内微生物组变异可能影响涉及肠道微生物组的干预措施的设计和解释的潜力。
