Identification of the direct regulon of NtcA during early acclimation to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803

Giner‐Lamia, Joaquín; Robles‐Rengel, Rocío; Hernández‐Prieto, Miguel A.; Muro‐Pastor, M. Isabel; Florencio, Francisco J.; Futschik, Matthias E.

doi:10.1093/nar/gkx860

Cited by 85 publications

(95 citation statements)

References 78 publications

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“…Sequestering of PipX by PII at low ATP/ADP ratios would interfere with energetically expensive biological processes, decreasing transcriptional activity in the dark (Hosokawa et al ., ; Takano et al ., ). In addition to down regulation of NtcA target genes co‐regulated by PipX (Espinosa et al ., ; Valladares et al ., ; Espinosa et al ., ; Giner‐Lamia et al ., ), it would also affect the predicted signalling pathway responsible for the toxic functions of PipX in the absence of PII (Fig. ; Espinosa et al ., ; Chang et al ., ).…”

Section: Resultsmentioning

confidence: 99%

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

Espinosa

Labella

Cantos

et al. 2018

Environmental Microbiology

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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.

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Section: Resultsmentioning

confidence: 99%

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

Espinosa

Labella

Cantos

et al. 2018

Environmental Microbiology

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“…A major receptor for 2-OG is the P II signal transduction protein, which coordinates cellular C/N metabolism by tuning key enzymes and regulatory proteins (reviewed by Forchhammer, 2004;2010;Forchhammer and Lüddecke, 2016). This enables NtcA to activate genes for the acquisition of alternate nitrogen sources and for increased GS activity (Luque and Forchhammer, 2008;Giner-Lamia et al, 2017). In complex with 2-OG, NtcA not only attains increased DNAbinding affinity (Luque et al, 2004) but, additionally, interacts with the transcriptional co-activator PipX (Llacer et al, 2010;Zhao et al, 2010;Forcada-Nadal et al, 2014).…”

Section: Metabolic Responses To Nitrogen Starvationmentioning

confidence: 99%

“…In complex with 2-OG, NtcA not only attains increased DNAbinding affinity (Luque et al, 2004) but, additionally, interacts with the transcriptional co-activator PipX (Llacer et al, 2010;Zhao et al, 2010;Forcada-Nadal et al, 2014). This enables NtcA to activate genes for the acquisition of alternate nitrogen sources and for increased GS activity (Luque and Forchhammer, 2008;Giner-Lamia et al, 2017). Binding of PipX by NtcA is antagonized by the P II signal transduction protein, which preferentially binds PipX at elevated ADP levels (Zeth et al, 2014;Lüddecke and Forchhammer, 2015;Espinosa et al, 2018).…”

Section: Metabolic Responses To Nitrogen Starvationmentioning

confidence: 99%

Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation

Forchhammer

Schwarz

2018

Environmental Microbiology

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Summary Cyanobacteria evolved sophisticated mechanisms allowing them to cope with environmental depletion of combined nitrogen. Here, we describe progress in understanding the processes involved in acclimation of nondiazotrophic cyanobacteria to nitrogen shortage, known as nitrogen chlorosis. The process includes immediate metabolic changes and degradation of light harvesting complexes as well as long‐term acclimation responses. Consequently, quiescent cells substantially differing from vegetative cells are obtained. Thus, the process leading to these considerable metabolic and morphological changes is referred to as a developmental program. Current understanding of the relevant regulatory processes depicts an intricate mechanism involving modulation of transcription activators by proteinaceous interacting components, as well as by small metabolites reporting the energy status and carbon–nitrogen balance of the cell. In addition, we describe in detail the quiescent state characterizing cells under prolonged starvation and the process of recovery from this dormant chlorotic state. Accumulated data provide an in depth understanding of the mechanisms accompanying the cycling of cyanobacterial cells between vegetative growth, the quiescent‐state and the recovery program, allowing them to regain proliferative growth upon nutrient replenishment.

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“…The nirA gene encoding nitrite reductase belongs to the core regulon controlled by global nitrogen regulator NtcA (44). The NtcA box within P nirA is overlapping the HLR1 by 5 nt ( Figure 6B (I) ).…”

Section: Resultsmentioning

confidence: 99%

Global analysis of the RpaB regulon based on the positional distribution of HLR1 sequences and comparative differential RNA-Seq data

Riediger

Kadowaki

Nagayama

et al. 2018

Preprint

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21 expression, regulatory networks, sRNAs 22 23 The transcription factor RpaB regulates the expression of genes encoding 24 photosynthesis-associated proteins during light acclimation. The binding site of RpaB 25 is the HLR1 motif, a pair of imperfect octameric direct repeats, separated by two 26 random nucleotides. Here, we used high-resolution mapping data of transcriptional 27 start sites (TSSs) in the model Synechocystis sp. PCC 6803 in conjunction with the 28 positional distribution of HLR1 sites for the global prediction of the RpaB regulon. The 29 results demonstrate that RpaB regulates the expression of more than 150 promoters, 30 driving the transcription of protein-coding and non-coding genes and antisense 31 transcripts under low light and upon the shift to high light when DNA binding activity is 32lost. Transcriptional activation by RpaB is achieved when the HLR1 motif is located 66 33 to 45 nt upstream, repression occurs when it is close to or overlapping the TSS. 34 Selected examples were validated by multiple experimental approaches, including 35 chromatin affinity purification, reporter gene, northern hybridization and electrophoretic 36 mobility shift assays. We found that RpaB controls ssr2016/pgr5, which is involved in 37 cyclic electron flow and state transitions; six out of nine ferredoxins; three of four FtsH 38 proteases; gcvP/slr0293, encoding a crucial photorespiratory protein; and nirA and isiA 39 for which we suggest cross-regulation with the transcription factors NtcA or FurA, 40 respectively. In addition to photosynthetic gene functions, RpaB contributes to the 41 control of genes affiliated with nitrogen assimilation, cofactor biosyntheses, the 42 CRISPR system and the circadian clock, making it one of the most versatile regulators 43 in cyanobacteria.44 Significance Statement: RpaB is a transcription factor in cyanobacteria and in the 45 chloroplasts of several lineages of eukaryotic algae. Like other important transcription 46 factors, the gene encoding RpaB cannot be deleted, making the study of deletion 47 54 RpaB ("regulator of phycobilisome association B") is an OmpR-type transcription factor 55 of crucial importance for the transcriptional control of multiple photosynthesis-56 associated genes under varying light conditions. RpaB was discovered in 57 Synechocystis sp. PCC 6803 (from here: Synechocystis 6803) based on its ability to 58 affect the energy distribution from phycobilisomes (PBS) to photosystem I (PSI) 59 relative to photosystem II (PSII) (1). Orthologs of rpaB belong to the cyanobacterial 60 core genome and were discovered in the chloroplast genomes of all non-green algae 61 except Odontella (2) and in the charophyte alga Chlorokybus atmophyticus (see (3) for 62 a recent review), suggesting important and evolutionarily widely conserved functions.63The rpaB gene cannot be deleted by conventional methods, indicating its essentiality 64 (1, 4-7). Despite its wide distribution, most insight into the genes controlled by RpaB 65 have been obtained from analyses ...

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Identification of the direct regulon of NtcA during early acclimation to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803

Cited by 85 publications

References 78 publications

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

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

Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation

Global analysis of the RpaB regulon based on the positional distribution of HLR1 sequences and comparative differential RNA-Seq data

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