Pontrelli Sammy, Bigovic Villi Kian, Sichert Andreas, Trouillon Julian, Rutz Adriano, Landry Zachary C, Rüdisser Simon H, Stocker Roman, Sauer Uwe
Institute of Molecular Systems Biology, ETH Zürich, Zürich, Switzerland.
Department of Biology, KU Leuven, Leuven, Belgium.
PLoS Biol. 2025 Jul 29;23(7):e3003287. doi: 10.1371/journal.pbio.3003287. eCollection 2025 Jul.
Metabolic cross-feeding networks are central to shaping microbial community dynamics in environments ranging from the rhizosphere, gut, and marine carbon cycling. Yet cross-feeding has predominantly been viewed by examining exchanged small metabolites. In contrast, the role of extracellular polymeric substance (EPS)-a complex mixture of proteins, polysaccharides, DNA, and humic-like compounds-in cross-feeding remains poorly understood, mainly due to technical challenges in measuring their secretion relative to small metabolites. Using chitin-degrading microbes as a model system, we used a bicarbonate-buffered bioreactor coupled with elemental analysis, which allowed us to quantify both EPS and small metabolite secretion. This revealed that ~25% of carbon exuded by a chitin degrader is in the form of EPS. EPS was produced at similar levels across marine chitin-degrading isolates and seawater communities, underscoring its importance relative to small metabolites. Notably, different sources of EPS were found to select for distinct and diverse microbial communities. Combining in vitro enzyme assays and untargeted metabolomics, we show that EPS undergoes sequential degradation-from large oligomers to smaller, broadly accessible monomers. This sequential breakdown creates a temporal succession of metabolic niches, potentially fueling a shift from specialist species degrading complex substrates to a more diverse community of generalists using simpler monomers. By identifying EPS as a major and dynamic contributor to cross-feeding networks, our findings reveal a hidden layer of complexity in how microbial communities assemble and function across ecosystems.
代谢交叉喂养网络对于塑造根际、肠道和海洋碳循环等环境中的微生物群落动态至关重要。然而,交叉喂养主要是通过研究交换的小分子代谢物来观察的。相比之下,胞外聚合物(EPS)——一种由蛋白质、多糖、DNA和类腐殖质化合物组成的复杂混合物——在交叉喂养中的作用仍知之甚少,主要是因为在测量其相对于小分子代谢物的分泌时存在技术挑战。我们以几丁质降解微生物为模型系统,使用了一个碳酸氢盐缓冲生物反应器并结合元素分析,这使我们能够量化EPS和小分子代谢物的分泌。结果表明,几丁质降解菌分泌的碳中约25%是以EPS的形式存在。在海洋几丁质降解分离株和海水群落中,EPS的产生水平相似,这突出了其相对于小分子代谢物的重要性。值得注意的是,发现不同来源的EPS会选择不同且多样的微生物群落。结合体外酶分析和非靶向代谢组学,我们表明EPS会经历从大的寡聚物到更小、更易获取的单体的顺序降解。这种顺序分解创造了代谢生态位的时间序列,可能推动从降解复杂底物的特化物种向使用更简单单体的更多样化的泛化物种群落的转变。通过将EPS确定为交叉喂养网络的主要动态贡献者,我们的研究结果揭示了微生物群落在生态系统中组装和发挥功能方式的一个隐藏的复杂层面。