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Elucidating the direct target regulon of NtcA during the early acclimation to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803 [RNA-Seq]

ABSTRACT: Cyanobacteria are oxygenic photoautotrophs responsible for a substantial proportion of nitrogen fixation and primary production in the hydrosphere. Non-nitrogen fixing cyanobacteria, such as Synechocystis sp. PCC 6803, depend of the availability of nitrogenized species to survive. Therefore, an intricate regulatory network around the transcriptional factor NtcA maintains the homeostasis of nitrogen in these organisms. The mechanisms controlling NtcA activity are well understood but a comprehensive study of its regulon is missing in Synechocystis. To define NtcA regulon during the early stage of nitrogen starvation, we have performed chromatin immunoprecipitation followed by sequencing (ChiP-seq), in parallel with genome level transcriptome analysis (RNA-seq). By combining both methods we assigned 51 activated and 28 repressed genes directly by NtcA. Most of direct targets included genes involved in nitrogen and carbon metabolism and photosynthesis. NtcA regulon also included 8 ncRNAs, of which ncr0710, Syr6 and NsiR7 were experimentally validated. Intriguingly, we identified several NtcA intragenic binding sites suggesting that NtcA can modulate transcriptional expression by binding along the whole transcript and not only in the promoter region as previously though. Finally, the transcriptional implication of PipX was analyzed in some NtcA-targets genes, revealing that PipX assists NtcA in the global nitrogen regulation in Synechocystis.

ORGANISM(S): Synechocystis sp. PCC 6803

PROVIDER: GSE97289 | GEO | 2017/10/01

SECONDARY ACCESSION(S): PRJNA381210

REPOSITORIES: GEO

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Project description:Unlike all other bacteria, the physiology of cyanobacteria is based on the assimilation of organic matter from inorganic carbon driven by oxygenic photosynthesis. This setting poses special regulatory challenges, particularly in integrating carbon and nitrogen metabolism. Several regulatory factors control the primary nitrogen metabolism, such as the PII protein and proteins interacting with it (PirA, PirC or PipX), or the inactivating factors IF7 and IF17 impacting glutamine synthetase activity. However, regulatory proteins of other enzymes in the nitrogen assimilation pathway have not been described thus far. Here, we show that the 81 amino acids regulatory protein NirP1 in the cyanobacterium Synechocystis sp. PCC 6803 functions as an inhibitor of nitrite reductase, a central enzyme in the assimilation of ammonia from nitrate/nitrite. Ectopic overexpression of the nirP1 gene under standard growth conditions led to a pigmentation phenotype and delayed growth, which was correlated by the excretion of nitrite and dramatic changes in metabolite pools. We show that nitrite excretion occurs in Synechocystis wild type cells upon the shift from high CO2 (HC) to low CO2 (LC) conditions when NirP1 expression becomes activated. The expression of nirP1 is controlled by two transcription factors, NtcA, which binds to a recognition site in a repressive position above the transcription start site (TSS), and an activator, which probably binds to an element 60 to 43 nt upstream of the TSS. Therefore, the joint activity of NtcA and this activator leads to the observed induction of NirP1 under LC conditions, whereas it is repressed by shifts to nitrogen starvation. The data demonstrate that NirP1 plays a crucial role in the coordination of C and N primary metabolism in cyanobacteria by targeting the activity of one of the central enzymes. In natural environments, the excreted nitrite will be utilized by other microorganisms; therefore, NirP1 will ultimately impact the activities and composition of the surrounding microbiome.

Dataset Information

Elucidating the direct target regulon of NtcA during the early acclimation to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803 [RNA-Seq]

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