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Growth rate-dependent coordination of catabolism and anabolism in the archaeon Methanococcus maripaludis under phosphate limitation
The ISME Journal ( IF 11.0 ) Pub Date : 2022-07-02 , DOI: 10.1038/s41396-022-01278-9
Wenyu Gu 1 , Albert L Müller 1 , Jörg S Deutzmann 1 , James R Williamson 2 , Alfred M Spormann 1, 3
Affiliation  

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−1 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.



中文翻译:

磷酸盐限制下古菌马里帕鲁迪斯甲烷球菌分解代谢和合成代谢的生长速率依赖性协调

微生物的分解代谢和合成代谢过程经过精细协调,可在不同的环境条件下提供最佳的适应性。了解这种协调和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,我们在磷酸盐(即合成代谢)限制下的恒化器实验中,以0.09至0.003 h -1的不同稀释率,描述了马里帕鲁迪斯甲烷球菌(一种专门的产甲烷古菌)的系统级生理学特征。磷酸盐作为限制养分提供,而甲酸作为分解代谢底物和碳源过量提供。我们观察到分解代谢和合成代谢的脱钩导致在相同稀释率下相对于分解代谢受限的细胞而言生物量产量较低。此外,几个粗粒蛋白质组部分的质量丰度(即根据其功能分组的蛋白质的组合丰度)表现出与生长速率的线性关系,主要是核糖体及其生物发生。因此,细胞RNA含量也与生长速率相关。尽管产甲烷蛋白质组部分是不变的,但产甲烷的代谢能力(在转移到分批培养后立即以甲烷生产率测量)与生长速率相关,表明翻译独立的调节使得细胞仅在生长允许的条件下增加分解代谢活性。这些观察结果与甲酸盐(即分解代谢)限制下的M. maripaludis生理学形成鲜明对比,其中细胞在各种生长速率下保持不变的蛋白质组,包括核糖体含量和高产甲烷能力。我们的研究结果表明,M. maripaludis在合成代谢磷酸盐和分解代谢甲酸限制期间采用根本不同的策略来协调整体生理学。

更新日期:2022-07-03
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