Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland.
Department of Environmental Microbiology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland.
Elife. 2024 Oct 21;13:RP93855. doi: 10.7554/eLife.93855.
Most of Earth's biomass is composed of polysaccharides. During biomass decomposition, polysaccharides are degraded by heterotrophic bacteria as a nutrient and energy source and are thereby partly remineralized into CO. As polysaccharides are heterogeneously distributed in nature, following the colonization and degradation of a polysaccharide hotspot the cells need to reach new polysaccharide hotspots. Even though many studies indicate that these degradation-dispersal cycles contribute to the carbon flow in marine systems, we know little about how cells alternate between polysaccharide degradation and motility, and which environmental factors trigger this behavioral switch. Here, we studied the growth of the marine bacterium ZF270 on the abundant marine polysaccharide alginate, both in its soluble polymeric form as well as on its breakdown products. We used microfluidics coupled to time-lapse microscopy to analyze motility and growth of individual cells, and RNA sequencing to study associated changes in gene expression. We found that single cells grow at reduced rate on alginate until they form large groups that cooperatively break down the polymer. Exposing cell groups to digested alginate accelerates cell growth and changes the expression of genes involved in alginate degradation and catabolism, central metabolism, ribosomal biosynthesis, and transport. However, exposure to digested alginate also triggers cells to become motile and disperse from cell groups, proportionally increasing with the group size before the nutrient switch, and this is accompanied by high expression of genes involved in flagellar assembly, chemotaxis, and quorum sensing. The motile cells chemotax toward polymeric but not digested alginate, likely enabling them to find new polysaccharide hotspots. Overall, our findings reveal cellular mechanisms that might also underlie bacterial degradation-dispersal cycles, which influence the remineralization of biomass in marine environments.
地球上的大部分生物量由多糖组成。在生物质分解过程中，多糖作为营养和能量源被异养细菌降解，部分被再矿化为 CO。由于多糖在自然界中呈异质分布，在多糖热点被定植和降解后，细胞需要到达新的多糖热点。尽管许多研究表明这些降解-扩散循环有助于海洋系统中的碳流动，但我们对细胞如何在多糖降解和运动之间交替，以及哪些环境因素引发这种行为转变知之甚少。在这里，我们研究了海洋细菌 ZF270 在丰富的海洋多糖海藻酸盐上的生长情况，包括其可溶性聚合物形式和其分解产物。我们使用微流控技术结合延时显微镜分析了单个细胞的运动和生长，并进行 RNA 测序以研究相关基因表达的变化。我们发现，单个细胞在海藻酸盐上的生长速度较慢，直到它们形成大的群体，共同降解聚合物。将细胞群体暴露于消化的海藻酸盐会加速细胞生长，并改变与海藻酸盐降解和分解代谢、中心代谢、核糖体生物合成和运输相关的基因表达。然而，暴露于消化的海藻酸盐也会触发细胞变得运动，并从细胞群体中扩散，在营养物质转换之前，这种扩散与群体大小成比例增加，并且伴随着与鞭毛组装、趋化性和群体感应相关的基因的高表达。游动细胞向聚合但不是消化的海藻酸盐趋化，这可能使它们能够找到新的多糖热点。总的来说，我们的研究结果揭示了细胞机制，这些机制可能也构成了细菌降解-扩散循环的基础，从而影响海洋环境中生物质的再矿化。
