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Published on October 22, 2008; 10.1104/pp.108.129403

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Received September 5, 2008
Accepted October 16, 2008

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

Marion Eisenhut , Jan Huege , Doreen Schwarz , Hermann Bauwe , Joachim Kopka , and Martin Hagemann *

Universitat Rostock, Institut fur Biowissenschaften, Pflanzenphysiologie, Albert-Einstein-Str. 3, 18051 Rostock, Germany; Max-Planck-Institut fur Molekulare Pflanzenphysiologie, Am Muhlenberg 1, 14476 Golm, Germany

* Corresponding author; email: martin.hagemann{at}uni-rostock.de.

The amount of inorganic carbon represents one of the main environmental factors determining productivity of photoautotrophic organisms. Using the model cyanobacterium Synechocystis PCC 6803, we performed a first metabolome study with cyanobacterial cells shifted from high CO2 (5% in air, HC) into conditions of low CO2 (ambient air with 0.035% CO2, LC). Using GC-MS, 74 metabolites were reproducibly identified under different growth conditions. Shifting wild type (WT) cells into LC conditions resulted in a global metabolic reprogramming and involved increases of e.g. 2-oxoglutarate (2OG) and phosphoenolpyruvate as well as reductions of e.g. 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 concomitant decrease of glutamine pointed towards 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 N-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 WT cells such as the changed 2OG to glutamine ratio and PII phosphorylation state already under HC conditions. Thus metabolome profiling demonstrated that acclimation to LC involves coordinated changes of C- and interacting N-metabolism. We hypothesize that Synechocystis has a temporal lag of acclimating C- versus N-metabolism with carbon leading.






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