Thioredoxin A regulates protein synthesis to maintain carbon and nitrogen partitioning in cyanobacteria

Abstract Thioredoxins play an essential role in regulating enzyme activity in response to environmental changes, especially in photosynthetic organisms. They are crucial for metabolic regulation in cyanobacteria, but the key redox-regulated central processes remain to be determined. Physiological, m...

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Published in:Plant physiology (Bethesda) 2024-07, Vol.195 (4), p.2921-2936
Main Authors: Mallén-Ponce, Manuel J, Florencio, Francisco Javier, Huertas, María José
Format: Article
Language:English
Subjects:
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Carbon - metabolism
Cyanobacteria - genetics
Cyanobacteria - metabolism
Gene Expression Regulation, Bacterial
Nitrogen - metabolism
Photosynthesis - genetics
Protein Biosynthesis
Synechocystis - genetics
Synechocystis - metabolism
Thioredoxins - genetics
Thioredoxins - metabolism
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Summary:Abstract Thioredoxins play an essential role in regulating enzyme activity in response to environmental changes, especially in photosynthetic organisms. They are crucial for metabolic regulation in cyanobacteria, but the key redox-regulated central processes remain to be determined. Physiological, metabolic, and transcriptomic characterization of a conditional mutant of the essential Synechocystis sp. PCC 6803 thioredoxin trxA gene (STXA2) revealed that decreased TrxA levels alter cell morphology and induce a dormant-like state. Furthermore, 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-Tu. Transcriptomic analysis of TrxA depletion in STXA2 revealed a robust transcriptional response. Downregulated genes formed a large cluster directly related to photosynthesis, ATP synthesis, and CO2 fixation. In contrast, upregulated genes were grouped into different clusters related to respiratory electron transport, carotenoid biosynthesis, amino acid metabolism, and protein degradation, among others. These findings highlight the complex regulatory mechanisms that govern cyanobacterial metabolism, where TrxA acts as a critical regulator that orchestrates the transition from anabolic to maintenance metabolism and regulates carbon and nitrogen balance. Thioredoxin A depletion in cyanobacteria leads to protein synthesis inhibition, reserve polymer accumulation, and induction of a robust transcriptomic response that triggers a dormant-like state.
ISSN:0032-0889
1532-2548
1532-2548
DOI:10.1093/plphys/kiae101