TY - JOUR

T1 - The PII signaling protein from red algae represents an evolutionary link between cyanobacterial and Chloroplastida PII proteins

AU - Lapina, Tatyana

AU - Selim, Khaled A.

AU - Forchhammer, Karl

AU - Ermilova, Elena

PY - 2018/12/1

Y1 - 2018/12/1

N2 - 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.

AB - 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.

KW - Algal Proteins/genetics

KW - Amino Acid Sequence

KW - Bacterial Proteins/genetics

KW - Calorimetry

KW - Chlamydomonas/metabolism

KW - Chloroplasts/metabolism

KW - Cyanobacteria/metabolism

KW - Evolution, Molecular

KW - Ketoglutaric Acids/metabolism

KW - Kinetics

KW - PII Nitrogen Regulatory Proteins/genetics

KW - Phosphotransferases (Carboxyl Group Acceptor)/metabolism

KW - Protein Binding

KW - Rhodophyta/metabolism

KW - Sequence Alignment

KW - Signal Transduction

KW - Surface Plasmon Resonance

UR - http://www.scopus.com/inward/record.url?scp=85040768165&partnerID=8YFLogxK

UR - http://www.mendeley.com/research/pii-signaling-protein-red-algae-represents-evolutionary-link-between-cyanobacterial-chloroplastida-p

U2 - 10.1038/s41598-017-19046-7

DO - 10.1038/s41598-017-19046-7

M3 - Article

C2 - 29335634

AN - SCOPUS:85040768165

VL - 8

SP - 790

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 790

ER -