CAS Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS), Beijing, 100085, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.
Microbiome. 2024 Sep 7;12(1):166. doi: 10.1186/s40168-024-01890-1.
Microbial anaerobic metabolism is a key driver of biogeochemical cycles, influencing ecosystem function and health of both natural and engineered environments. However, the temporal dynamics of the intricate interactions between microorganisms and the organic metabolites are still poorly understood. Leveraging metagenomic and metabolomic approaches, we unveiled the principles governing microbial metabolism during a 96-day anaerobic bioreactor experiment.
During the turnover and assembly of metabolites, homogeneous selection was predominant, peaking at 84.05% on day 12. Consistent dynamic coordination between microbes and metabolites was observed regarding their composition and assembly processes. Our findings suggested that microbes drove deterministic metabolite turnover, leading to consistent molecular conversions across parallel reactors. Moreover, due to the more favorable thermodynamics of N-containing organic biotransformations, microbes preferentially carried out sequential degradations from N-containing to S-containing compounds. Similarly, the metabolic strategy of C18 lipid-like molecules could switch from synthesis to degradation due to nutrient exhaustion and thermodynamical disadvantage. This indicated that community biotransformation thermodynamics emerged as a key regulator of both catabolic and synthetic metabolisms, shaping metabolic strategy shifts at the community level. Furthermore, the co-occurrence network of microbes-metabolites was structured around microbial metabolic functions centered on methanogenesis, with CH as a network hub, connecting with 62.15% of total nodes as 1st and 2nd neighbors. Microbes aggregate molecules with different molecular traits and are modularized depending on their metabolic abilities. They established increasingly positive relationships with high-molecular-weight molecules, facilitating resource acquisition and energy utilization. This metabolic complementarity and substance exchange further underscored the cooperative nature of microbial interactions.
All results revealed three key rules governing microbial anaerobic degradation. These rules indicate that microbes adapt to environmental conditions according to their community-level metabolic trade-offs and synergistic metabolic functions, further driving the deterministic dynamics of molecular composition. This research offers valuable insights for enhancing the prediction and regulation of microbial activities and carbon flow in anaerobic environments. Video Abstract.
微生物的厌氧代谢是生物地球化学循环的关键驱动力，影响着自然和工程环境的生态系统功能和健康。然而，微生物与有机代谢物之间复杂相互作用的时间动态仍然知之甚少。利用宏基因组学和代谢组学方法，我们在一个为期 96 天的厌氧生物反应器实验中揭示了微生物代谢的控制原理。
在代谢物的周转和组装过程中，同质选择占主导地位，在第 12 天达到 84.05%的峰值。微生物和代谢物在组成和组装过程中表现出一致的动态协调。我们的研究结果表明，微生物驱动确定性代谢物周转，导致平行反应器中一致的分子转化。此外，由于含 N 有机生物转化的热力学更有利，微生物优先进行从含 N 到含 S 化合物的连续降解。同样，由于营养物质耗尽和热力学劣势，C18 类脂样分子的代谢策略可以从合成转变为降解。这表明群落生物转化热力学成为分解代谢和合成代谢的关键调节因素，在群落水平上塑造代谢策略的转变。此外，微生物-代谢物的共现网络围绕以产甲烷为中心的微生物代谢功能构建，CH 作为网络枢纽，与总节点的 62.15%作为第一和第二邻居相连。微生物聚集具有不同分子特征的分子，并根据其代谢能力模块化。它们与高分子量分子建立越来越积极的关系，促进资源获取和能量利用。这种代谢互补性和物质交换进一步强调了微生物相互作用的合作性质。
所有结果揭示了三条控制微生物厌氧降解的关键规则。这些规则表明，微生物根据其群落水平的代谢权衡和协同代谢功能适应环境条件，进一步驱动分子组成的确定性动态。这项研究为增强对厌氧环境中微生物活性和碳流的预测和调控提供了有价值的见解。视频摘要。
