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TrxA-mediated regulation of protein synthesis contributes to the maintenance of carbon and nitrogen balance in cyanobacteria.

ABSTRACT: Thioredoxins play an essential role in regulating enzyme activity upon response to environmental changes, especially in photosynthetic organisms. These are crucial for the regulation of metabolism in cyanobacteria, but the key central processes redox-regulated remain to be determined. Physiological, metabolic and transcriptomic characterization of a conditional mutant of the essential trxA gene in Synechocystis (STXA2) revealed that reduced TrxA levels alter cell morphology and enter in a dormant-like state. TrxA depletion in the STXA2 strain inhibited protein synthesis and led to changes in amino acid pools and nitrogen/carbon reserve polymers, accompanied by oxidation of the Elongation Factor EF-Tu. Transcriptomic analysis of TrxA depletion in STXA2 showed a robust transcriptional response. Genes that responded negatively were grouped in a large cluster and were directly related to photosynthesis, ATP synthesis and CO2 fixation, while genes that responded positively were grouped in different clusters and related to respiratory electron transport, carotenoids synthesis, amino acid metabolism and protein degradation, among others. Regulation of cyanobacterial metabolism is complex and fine-tuned, our results link TrxA to the switch from anabolic to maintenance metabolism in cyanobacteria, regulating carbon and nitrogen balance.

ORGANISM(S): Synechocystis sp. PCC 6803

PROVIDER: GSE243518 | GEO | 2023/09/24

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.

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TrxA-mediated regulation of protein synthesis contributes to the maintenance of carbon and nitrogen balance in cyanobacteria.

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