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

Khaled A. Selim, Tatyana Lapina, Karl Forchhammer, Elena Ermilova

Research output

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.

Original languageEnglish
Number of pages18
JournalFEBS Journal
Early online date26 Jul 2019
DOIs
Publication statusPublished - 26 Jul 2019

Fingerprint

acetylglutamate kinase
Plastids
Algae
Transducers
Arginine
glutamate 5-kinase
Enzymes
Glutamine
arginine glutamate
Proteins
Carbon
Chlamydomonas reinhardtii
Aptitude
Photosynthesis
Molecules
Biosynthesis
Life Style
Metabolites
Nitrogen
Feedback control

Cite this

@article{2177c8031fbe4931b735506825541ee2,
title = "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",
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.",
keywords = "2-OXOGLUTARATE, ACETYLGLUTAMATE-KINASE, COMPLEX-FORMATION, GENOME, GS-GOGAT cycles, MECHANISM, N-acetyl-l-glutamate kinase, NITROGEN, Nonphotosynthetic plastids, P-II, PATHWAY, PII-signalling, PLANTS, PROTEIN, TCA, algal metabolomics, arginine biosynthesis",
author = "Selim, {Khaled A.} and Tatyana Lapina and Karl Forchhammer and Elena Ermilova",
note = "Selim, K. A., Lapina, T., Forchhammer, K., & Ermilova, E. (2019). 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 . The FEBS Journal. https://doi.org/10.1111/febs.14989",
year = "2019",
month = "7",
day = "26",
doi = "10.1111/febs.14989",
language = "English",
journal = "FEBS Journal",
issn = "1742-464X",
publisher = "Wiley-Blackwell",

}

TY - JOUR

T1 - 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

AU - Selim, Khaled A.

AU - Lapina, Tatyana

AU - Forchhammer, Karl

AU - Ermilova, Elena

N1 - Selim, K. A., Lapina, T., Forchhammer, K., & Ermilova, E. (2019). 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 . The FEBS Journal. https://doi.org/10.1111/febs.14989

PY - 2019/7/26

Y1 - 2019/7/26

N2 - 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.

AB - 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.

KW - 2-OXOGLUTARATE

KW - ACETYLGLUTAMATE-KINASE

KW - COMPLEX-FORMATION

KW - GENOME

KW - GS-GOGAT cycles

KW - MECHANISM

KW - N-acetyl-l-glutamate kinase

KW - NITROGEN

KW - Nonphotosynthetic plastids

KW - P-II

KW - PATHWAY

KW - PII-signalling

KW - PLANTS

KW - PROTEIN

KW - TCA

KW - algal metabolomics

KW - arginine biosynthesis

UR - http://www.mendeley.com/research/interaction-nacetyl-l-glutamate-kinase-pii-signal-transducer-nonphotosynthetic-alga-polytomella-parv

UR - https://www.ncbi.nlm.nih.gov/pubmed/31287617

UR - https://febs.onlinelibrary.wiley.com/doi/full/10.1111/febs.14989

U2 - 10.1111/febs.14989

DO - 10.1111/febs.14989

M3 - Article

JO - FEBS Journal

JF - FEBS Journal

SN - 1742-464X

ER -