Interaction of N‐acetyl‐l‐glutamate kinase with the PII signal transducer in the non‐photosynthetic alga Polytomella parva: Co‐evolution towards a hetero‐oligomeric enzyme. (26th July 2019)

• Record Type: Journal Article
• Authors: Selim, Khaled A.; Lapina, Tatyana; Forchhammer, Karl; Ermilova, Elena
• Is Part Of: FEBS journal. Volume 287:Number 3(2020)
• Page Start: 465
• Page End: 482
• Publication Date: 2019-07-26
• Subjects: algal metabolomics -- arginine biosynthesis -- N‐acetyl‐l‐glutamate kinase -- Nonphotosynthetic plastids -- PII‐signalling -- TCA/GS‐GOGAT cycles; Biochemistry -- Periodicals; Molecular biology -- Periodicals; Pathology, Molecular -- Periodicals; 572
• DOI: 10.1111/febs.14989
• Languages: English
• ISSNs: 1742-464X

Abstract

Abstract : 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. Abstract : The major target of the PII signalling protein in Archaeplastida is N‐acetyl glutamate kinase (NAGK). PII is known as a transiently interacting signalling protein. In this work, we demonstrate that NAGK co‐evolved with PII signalling protein towards a stable hetero‐oligomeric complex that tunes arginine feedback inhibition (+ve/−ve) in response to glutamine status in nonphotosynthetic alga Polytomella parva . This is likely to be a metabolic adaptation strategy in line with the evolutionary loss of photosynthesis in this species.