The nitrogen interaction network in Synechococcus WH5701, a cyanobacterium with two PipX and two PII-like proteins

Laichoubi, Karim Boumediene; Beez, Sabine; Espinosa, José; Forchhammer, Karl; Contreras, Asunción

doi:10.1099/mic.0.047266-0

Cited by 20 publications

(15 citation statements)

References 35 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…A few cyanobacteria possess multiple PII paralogues, and in these cases, the organisms also contain multiple PipX paralogues. In the case of the marine cyanobacterium Synechococcus WH5701, it could be shown that only one of the two PII paralogues activates NAGK and binds to PipX protein; the function of the other PII paralogue is unknown (Laichoubi et al 2011). A further target of PII was identified as PamA in the cyanobacterium Synechocystis PCC 6803.…”

Section: Further Functions Of Pii Signaling In Oxygenic Phototrophsmentioning

confidence: 99%

“…While most cyanobacteria harbor one PII protein, some strains encode a second or even a third paralogue (Laichoubi et al 2011). In contrast to many bacteria, where PII proteins (mainly of the GlnB subfamily) are involved in regulation of glutamine synthetase at various levels (Ninfa and Atkinson 2000;Leigh and Dodsworth 2007), cyanobacterial PII proteins have evolved to regulate the ornithine pathway, which leads to arginine and polyamine synthesis, and to the modulation of nitrogen-dependent transcription.…”

mentioning

confidence: 99%

See 1 more Smart Citation

From cyanobacteria to plants: conservation of PII functions during plastid evolution

Chellamuthu

Alva

Forchhammer

2012

Planta

Self Cite

View full text Add to dashboard Cite

This article reviews the current state-of-the-art concerning the functions of the signal processing protein PII in cyanobacteria and plants, with a special focus on evolutionary aspects. We start out with a general introduction to PII proteins, their distribution, and their evolution. We also discuss PII-like proteins and domains, in particular, the similarity between ATP-phosphoribosyltransferase (ATP-PRT) and its PII-like domain and the complex between N-acetyl-L-glutamate kinase (NAGK) and its PII activator protein from oxygenic phototrophs. The structural basis of the function of PII as an ATP/ADP/ 2-oxoglutarate signal processor is described for Synechococcus elongatus PII. In both cyanobacteria and plants, a major target of PII regulation is NAGK, which catalyzes the committed step of arginine biosynthesis. The common principles of NAGK regulation by PII are outlined. Based on the observation that PII proteins from cyanobacteria and plants can functionally replace each other, the hypothesis that PII-dependent NAGK control was under selective pressure during the evolution of plastids of Chloroplastida and Rhodophyta is tested by bioinformatics approaches. It is noteworthy that two lineages of heterokont algae, diatoms and brown algae, also possess NAGK, albeit lacking PII; their NAGK however appears to have descended from an alphaproteobacterium and not from a cyanobacterium as in plants. We end this article by coming to the conclusion that during the evolution of plastids, PII lost its function in coordinating gene expression through the PipX-NtcA network but preserved its role in nitrogen (arginine) storage metabolism, and subsequently took over the fine-tuned regulation of carbon (fatty acid) storage metabolism, which is important in certain developmental stages of plants.

show abstract

Section: Further Functions Of Pii Signaling In Oxygenic Phototrophsmentioning

confidence: 99%

mentioning

confidence: 99%

From cyanobacteria to plants: conservation of PII functions during plastid evolution

Chellamuthu

Alva

Forchhammer

2012

Planta

Self Cite

View full text Add to dashboard Cite

show abstract

“…Knowledge of this nitrogen regulatory interaction network of cyanobacteria, has largely benefited from the “guilty by association” principle implicit in yeast two- and three-hybrid approaches (Burillo et al, 2004; Espinosa et al, 2006; Llacer et al, 2007, 2010; Laichoubi et al, 2011, 2012; Labella et al, 2016). The same principle can be applied to proteins encoded within the same operon, particularly in the cyanobacterium Synechococcus elongatus PCC7942 (hereafter S. elongatus ), where most of the mRNA transcripts identified (approximately 62%) are monocistronic and thus the co-transcription of 2 given genes provides a very strong suggestion of functional association (Vijayan et al, 2011; Memon et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

PipY, a Member of the Conserved COG0325 Family of PLP-Binding Proteins, Expands the Cyanobacterial Nitrogen Regulatory Network

et al. 2017

Self Cite

View full text Add to dashboard Cite

Synechococcus elongatus PCC 7942 is a paradigmatic model organism for nitrogen regulation in cyanobacteria. Expression of genes involved in nitrogen assimilation is positively regulated by the 2-oxoglutarate receptor and global transcriptional regulator NtcA. Maximal activation requires the subsequent binding of the co-activator PipX. PII, a protein found in all three domains of life as an integrator of signals of the nitrogen and carbon balance, binds to PipX to counteract NtcA activity at low 2-oxoglutarate levels. PII-PipX complexes can also bind to the transcriptional regulator PlmA, whose regulon remains unknown. Here we expand the nitrogen regulatory network to PipY, encoded by the bicistronic operon pipXY in S. elongatus. Work with PipY, the cyanobacterial member of the widespread family of COG0325 proteins, confirms the conserved roles in vitamin B6 and amino/keto acid homeostasis and reveals new PLP-related phenotypes, including sensitivity to antibiotics targeting essential PLP-holoenzymes or synthetic lethality with cysK. In addition, the related phenotypes of pipY and pipX mutants are consistent with genetic interactions in the contexts of survival to PLP-targeting antibiotics and transcriptional regulation. We also showed that PipY overexpression increased the length of S. elongatus cells. Taken together, our results support a universal regulatory role for COG0325 proteins, paving the way to a better understanding of these proteins and of their connections with other biological processes.

show abstract

“…In particular, genetic analyses are consistent with a greater complexity of the protein‐protein interaction network involving PII and PipX regulators and thus suggest that they may be integrating multiple signalling pathways. Particularly interesting is the phenomenon described as the toxicity of PipX in the absence of PII, which implicate both proteins in the regulation of essential processes in S. elongatus (Espinosa et al ., 2009, 2010; Laichoubi et al ., ; Chang et al ., ), an implication also supported by in silico (Laichoubi et al ., ) and transcriptomic analyses (Espinosa et al ., ). However, the molecular bases of the relevant signalling pathway(s) inferred from these studies remain to be elucidated.…”

Section: Introductionmentioning

confidence: 99%

Energy drives the dynamic localization of cyanobacterial nitrogen regulators during diurnal cycles

Espinosa

Labella

Cantos

et al. 2018

Environmental Microbiology

Self Cite

View full text Add to dashboard Cite

Cyanobacteria, phototrophic organisms performing oxygenic photosynthesis, must adapt their metabolic processes to the challenges imposed by the succession of days and nights. Two conserved cyanobacterial proteins, PII and PipX, function as hubs of the nitrogen interaction network, forming complexes with a variety of diverse targets. While PII proteins are found in all three domains of life as integrators of signals of the nitrogen and carbon balance, PipX proteins are unique to cyanobacteria, where they provide a mechanistic link between PII signalling and the control of gene expression by the global nitrogen regulator NtcA. Here we demonstrate that PII and PipX display distinct localization patterns during diurnal cycles, co-localizing into the same foci at the periphery and poles of the cells during dark periods, a circadian-independent process requiring a low ATP/ADP ratio. Genetic, cellular biology and biochemical approaches used here provide new insights into the nitrogen regulatory network, calling attention to the roles of PII as energy sensors and its interactions with PipX in the context of essential signalling pathways. This study expands the contribution of the nitrogen regulators PII and PipX to integrate and transduce key environmental signals that allow cyanobacteria to thrive in our planet.

show abstract

The nitrogen interaction network in Synechococcus WH5701, a cyanobacterium with two PipX and two PII-like proteins

Cited by 20 publications

References 35 publications

From cyanobacteria to plants: conservation of PII functions during plastid evolution

From cyanobacteria to plants: conservation of PII functions during plastid evolution

PipY, a Member of the Conserved COG0325 Family of PLP-Binding Proteins, Expands the Cyanobacterial Nitrogen Regulatory Network

Energy drives the dynamic localization of cyanobacterial nitrogen regulators during diurnal cycles

Contact Info

Product

Resources

About