Department of Civil and Environmental Engineering, Stanford University, Stanford, CA, USA.
Department of Integrative Structural and Computational Biology, Department of Chemistry, The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA, USA.
ISME J. 2022 Oct;16(10):2313-2319. doi: 10.1038/s41396-022-01278-9. Epub 2022 Jul 2.
Catabolic and anabolic processes are finely coordinated in microorganisms to provide optimized fitness under varying environmental conditions. Understanding this coordination and the resulting physiological traits reveals fundamental strategies of microbial acclimation. Here, we characterized the system-level physiology of Methanococcus maripaludis, a niche-specialized methanogenic archaeon, at different dilution rates ranging from 0.09 to 0.003 h in chemostat experiments under phosphate (i.e., anabolic) limitation. Phosphate was supplied as the limiting nutrient, while formate was supplied in excess as the catabolic substrate and carbon source. We observed a decoupling of catabolism and anabolism resulting in lower biomass yield relative to catabolically limited cells at the same dilution rates. In addition, the mass abundance of several coarse-grained proteome sectors (i.e., combined abundance of proteins grouped based on their function) exhibited a linear relationship with growth rate, mostly ribosomes and their biogenesis. Accordingly, cellular RNA content also correlated with growth rate. Although the methanogenesis proteome sector was invariant, the metabolic capacity for methanogenesis, measured as methane production rates immediately after transfer to batch culture, correlated with growth rate suggesting translationally independent regulation that allows cells to only increase catabolic activity under growth-permissible conditions. These observations are in stark contrast to the physiology of M. maripaludis under formate (i.e., catabolic) limitation, where cells keep an invariant proteome including ribosomal content and a high methanogenesis capacity across a wide range of growth rates. Our findings reveal that M. maripaludis employs fundamentally different strategies to coordinate global physiology during anabolic phosphate and catabolic formate limitation.
在微生物中，分解代谢和合成代谢过程被精细地协调，以在不断变化的环境条件下提供最佳的适应性。了解这种协调以及由此产生的生理特征揭示了微生物适应的基本策略。在这里，我们在恒化器实验中研究了甲烷八叠球菌（Methanococcus maripaludis）的系统水平生理学，该菌是一种专门适应于特定生境的产甲烷古菌，在不同的稀释率下（范围从 0.09 到 0.003 h），磷（即合成代谢）限制条件下。磷被作为限制营养物供应，而甲酸盐作为分解代谢底物和碳源过量供应。我们观察到分解代谢和合成代谢的解耦，导致在相同的稀释率下，相对于分解代谢受限的细胞，生物量产量降低。此外，几个粗粒度蛋白质组部分（即根据功能分组的蛋白质的组合丰度）的质量丰度与生长速率呈线性关系，主要是核糖体及其生物发生。相应地，细胞 RNA 含量也与生长速率相关。尽管甲烷生成蛋白质组部分是不变的，但甲烷生成的代谢能力，即立即转移到批量培养后的甲烷产生速率，与生长速率相关，这表明存在翻译独立的调节，使细胞仅在生长允许的条件下增加分解代谢活性。这些观察结果与 M. maripaludis 在甲酸盐（即分解代谢）限制下的生理学形成鲜明对比，在这种情况下，细胞保持不变的蛋白质组，包括核糖体含量和在广泛的生长速率范围内的高甲烷生成能力。我们的发现表明，M. maripaludis 在磷（即合成代谢）限制和甲酸盐（即分解代谢）限制下协调全局生理学时采用了根本不同的策略。
