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Metabolome Phenotyping of Inorganic Carbon Limitation in Cells of the Wild Type and Photorespiratory Mutants of the Cyanobacterium Synechocystis sp. Strain PCC 6803

Author:
Eisenhut, Marion, Huege, Jan, Schwarz, Doreen, Bauwe, Hermann, Kopka, Joachim, Hagemann, Martin
Source:
Plant physiology 2008 v.148 no.4 pp. 2109-2120
ISSN:
0032-0889
Subject:
Calvin cycle, Cyanobacterium, Synechocystis, air, autotrophs, biogeochemical cycles, carbon, dephosphorylation, environmental factors, glutamine, malates, metabolites, metabolome, mutants, nitrogen, nitrogen metabolism, phosphorylation, regulatory proteins, sucrose
Abstract:
The amount of inorganic carbon represents one of the main environmental factors determining productivity of photoautotrophic organisms. Using the model cyanobacterium Synechocystis sp. PCC 6803, we performed a first metabolome study with cyanobacterial cells shifted from high CO₂ (5% in air) into conditions of low CO₂ (LC; ambient air with 0.035% CO₂). Using gas chromatography-mass spectrometry, 74 metabolites were reproducibly identified under different growth conditions. Shifting wild-type cells into LC conditions resulted in a global metabolic reprogramming and involved increases of, for example, 2-oxoglutarate (2OG) and phosphoenolpyruvate, and reductions of, for example, sucrose and fructose-1,6-bisphosphate. A decrease in Calvin-Benson cycle activity and increased usage of associated carbon cycling routes, including photorespiratory metabolism, was indicated by synergistic accumulation of the fumarate, malate, and 2-phosphoglycolate pools and a transient increase of 3-phosphoglycerate. The unexpected accumulation of 2OG with a concomitant decrease of glutamine pointed toward reduced nitrogen availability when cells are confronted with LC. Despite the increase in 2OG and low amino acid pools, we found a complete dephosphorylation of the PII regulatory protein at LC characteristic for nitrogen-replete conditions. Moreover, mutants with defined blocks in the photorespiratory metabolism leading to the accumulation of glycolate and glycine, respectively, exhibited features of LC-treated wild-type cells such as the changed 2OG to glutamine ratio and PII phosphorylation state already under high CO₂ conditions. Thus, metabolome profiling demonstrated that acclimation to LC involves coordinated changes of carbon and interacting nitrogen metabolism. We hypothesize that Synechocystis has a temporal lag of acclimating carbon versus nitrogen metabolism with carbon leading.
Agid:
564000