Department of Microbiology/Organismic Interactions, Interfaculty Institute of Microbiology and Infection Medicine, Eberhard-Karls-Universität Tübingen, Germany.
Biological Faculty, Saint-Petersburg State University, Russia.
FEBS J. 2020 Feb;287(3):465-482. doi: 10.1111/febs.14989. Epub 2019 Jul 26.
During evolution, several algae and plants became heterotrophic and lost photosynthesis; however, in most cases, a nonphotosynthetic plastid was maintained. Among these organisms, the colourless alga Polytomella parva is a special case, as its plastid is devoid of any DNA, but is maintained for specific metabolic tasks carried out by nuclear encoded enzymes. This makes P. parva attractive to study molecular events underlying the transition from autotrophic to heterotrophic lifestyle. Here we characterize metabolic adaptation strategies of P. parva in comparison to the closely related photosynthetic alga Chlamydomonas reinhardtii with a focus on the role of plastid-localized PII signalling protein. Polytomella parva accumulates significantly higher amounts of most TCA cycle intermediates as well as glutamate, aspartate and arginine, the latter being specific for the colourless plastid. Correlating with the altered metabolite status, the carbon/nitrogen sensory PII signalling protein and its regulatory target N-acetyl-l-glutamate-kinase (NAGK; the controlling enzyme of arginine biosynthesis) show unique features: They have co-evolved into a stable hetero-oligomeric complex, irrespective of effector molecules. The PII signalling protein, so far known as a transiently interacting signalling protein, appears as a permanent subunit of the enzyme NAGK. NAGK requires PII to properly sense the feedback inhibitor arginine, and moreover, PII tunes arginine-inhibition in response to glutamine. No other PII effector molecules interfere, indicating that the PII-NAGK system in P. parva has lost the ability to estimate the cellular energy and carbon status but has specialized to provide an entirely glutamine-dependent arginine feedback control, highlighting the evolutionary plasticity of PII signalling system.
在进化过程中，一些藻类和植物变成了异养生物，失去了光合作用；然而，在大多数情况下，它们仍维持着一个非光合质体。在这些生物中，无色藻类 Polytomella parva 是一个特殊的例子，因为其质体中没有任何 DNA，但为核编码酶执行的特定代谢任务所保留。这使得 P. parva 成为研究从自养到异养生活方式转变的分子事件的理想对象。在这里，我们将 P. parva 的代谢适应策略与密切相关的光合藻类 Chlamydomonas reinhardtii 进行了比较，重点研究了质体定位的 PII 信号蛋白的作用。与光合作用相关的 Chlamydomonas reinhardtii 相比，Polytomella parva 积累了更多的三羧酸 (TCA) 循环中间产物以及谷氨酸、天冬氨酸和精氨酸，后者是无色质体所特有的。与改变的代谢状态相关，碳/氮感应 PII 信号蛋白及其调节靶标 N-乙酰-l-谷氨酸激酶 (NAGK；精氨酸生物合成的控制酶) 表现出独特的特征：它们已经共同进化为一个稳定的异源寡聚复合物，而不依赖于效应分子。到目前为止，PII 信号蛋白被认为是一种瞬时相互作用的信号蛋白，它作为酶 NAGK 的一个永久性亚基出现。NAGK 需要 PII 才能正确感知反馈抑制剂精氨酸，而且，PII 可以根据谷氨酰胺来调节精氨酸的抑制作用。没有其他 PII 效应分子干扰，这表明 P. parva 中的 PII-NAGK 系统已经失去了估计细胞能量和碳状态的能力，但已经专门用于提供完全依赖于谷氨酰胺的精氨酸反馈控制，突出了 PII 信号系统的进化灵活性。
