Microbe-cellulose hydrogels as a model system for particulate carbon degradation in soil aggregates

IF 5.1 Q1 ECOLOGY ISME communications Pub Date : 2024-05-04 DOI:10.1093/ismeco/ycae068
Pieter Candry, Bruce J Godfrey, M. K. Winkler
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Abstract

Particulate carbon (C) degradation in soils is a critical process in the global C cycle governing greenhouse gas fluxes and C storage. Millimeter-scale soil aggregates impose strong controls on particulate C degradation by inducing chemical gradients of e.g., oxygen, as well as limiting microbial mobility in pore structures. To date, experimental models of soil aggregates have incorporated porosity and chemical gradients but not particulate C. Here, we demonstrate a proof-of-concept encapsulating microbial cells and particulate C substrates in hydrogel matrices as a novel experimental model for soil aggregates. Ruminiclostridium cellulolyticum was co-encapsulated with cellulose in millimeter-scale polyethyleneglycol-dimethacrylate (PEGDMA) hydrogel beads. Microbial activity was delayed in hydrogel-encapsulated conditions, with cellulose degradation and fermentation activity being observed after 13 days of incubation. Unexpectedly, hydrogel encapsulation shifted product formation of R. cellulolyticum from an ethanol-lactate-acetate mixture to an acetate-dominated product profile. Fluorescence microscopy enabled simultaneous visualization of the PEGDMA matrix, cellulose particles, and individual cells in the matrix, demonstrating growth on cellulose particles during incubation. Together, these microbe-cellulose-PEGDMA hydrogels present a novel, reproducible experimental soil surrogate to connect single cells to process outcomes at the scale of soil aggregates and ecosystems.
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将微生物-纤维素水凝胶作为土壤团聚体中颗粒碳降解的模型系统
土壤中的微粒碳(C)降解是全球碳循环中的一个关键过程,影响着温室气体通量和碳储存。毫米尺度的土壤团聚体通过诱导氧等化学梯度以及限制孔隙结构中微生物的流动性,对微粒碳降解施加了强有力的控制。迄今为止,土壤团聚体的实验模型都包含孔隙度和化学梯度,但不包括微粒碳。在这里,我们展示了一种概念验证方法,即在水凝胶基质中封装微生物细胞和微粒碳基质,作为土壤团聚体的新型实验模型。纤维素溶解瘤反刍梭菌与纤维素共同被包裹在毫米级聚乙二醇二甲基丙烯酸酯(PEGDMA)水凝胶珠中。在水凝胶包囊条件下,微生物的活性被延迟,培养 13 天后才能观察到纤维素降解和发酵活性。意想不到的是,水凝胶封装使 R. cellulolyticum 的产物形成从乙醇-乳酸-乙酸酯混合物转变为以乙酸酯为主的产物。荧光显微镜可同时观察到 PEGDMA 基质、纤维素颗粒和基质中的单个细胞,显示了培养过程中纤维素颗粒上的生长情况。总之,这些微生物-纤维素-PEGDMA 水凝胶提供了一种新颖、可重复的实验土壤替代物,可将单细胞与土壤聚集体和生态系统规模的过程结果联系起来。
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