The PII signaling protein from red algae represents an evolutionary link between cyanobacterial and Chloroplastida PII proteins

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

doi:10.1038/s41598-017-19046-7

Tatyana Lapina, Khaled A Selim + Show 2 more

Open Access

https://doi.org/10.1038/s41598-017-19046-7

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Abstract

PII superfamily consists of widespread signal transduction proteins found in all domains of life. Whereas they are well-studied in Archaea, Bacteria and Chloroplastida, no PII homolog has been analyzed in Rhodophyta (red algae), where PII is encoded by a chloroplast localized glnB gene. Here, we characterized relevant sensory properties of PII from the red alga Porphyra purpurea (PpPII) in comparison to PII proteins from different phyla of oxygenic phototrophs (cyanobacteria, Chlamydomonas and Physcomitrella) to assess evolutionary conservation versus adaptive properties. Like its cyanobacterial counterparts, PpPII binds ATP/ADP and 2-oxoglutarate in synergy with ATP. However, green algae and land plant PII proteins lost the ability to bind ADP. In contrast to PII proteins from green algae and land plants, PpPII enhances the activity of N-acetyl-L-glutamate kinase (NAGK) and relieves it from feedback inhibition by arginine in a glutamine-independent manner. Like PII from Chloroplastida, PpPII is not able to interact with the cyanobacterial transcriptional co-activator PipX. These data emphasize the conserved role of NAGK as a major PII-interactor throughout the evolution of oxygenic phototrophs, and confirms the specific role of PipX for cyanobacteria. Our results highlight the PII signaling system in red algae as an evolutionary intermediate between Cyanobacteria and Chlorophyta.

Highlights

The PII superfamily were originally described as widely distributed members of a family of cell signaling proteins occurring in all domains of life[1,2,3] with representatives in almost all bacteria and in nitrogen-fixing archaea[4,5] as well as in oxygenic eukaryotic phototrophs[6]
The highest degree of identity occurs with the cyanobacterial homologues S. elongatus PCC 7942 (63.96%) and Synechocystis sp
During the evolution of Rhodophyta, the PII proteins that are ubiquitously present in Bacteria, Archaea and in the chloroplasts of green algae and land plants[1,5,23] have been lost in most red algae

Summary

Introduction

The PII superfamily were originally described as widely distributed members of a family of cell signaling proteins occurring in all domains of life[1,2,3] with representatives in almost all bacteria and in nitrogen-fixing archaea[4,5] as well as in oxygenic eukaryotic phototrophs[6]. In green algae and land plants, NAGK activity-regulation responds - via a specific feature of the respective PII proteins - to the cellular glutamine levels in addition to the primary effects ATP and 2-OG24,25. A short additional C-terminal segment, absent in bacterial PII proteins, was shown to act as low-affinity glutamine binding site This segment seems to have evolved when the glnB gene from the endosymbiont was translocated to the nucleus, since it is absent in Rhodophyta, where this translocation has not taken place. This suggests that the PII signaling protein from red algae resembles the PII signaling system of the early endosymbiont. Functional analysis of red algal PII proteins is necessary to close the gap in our understanding of PII evolution in oxygenic phototrophs

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