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BIOENERGETICS AND PHOTOSYNTHESIS

Metabolome Phenotyping of Inorganic Carbon Limitation in Cells of the Wild Type and Photorespiratory Mutants of the Cyanobacterium Synechocystis sp. Strain PCC 6803^1,[W]

Universität Rostock, Institut für Biowissenschaften, Pflanzenphysiologie, 18051 Rostock, Germany (M.E., D.S., H.B., M.H.); and Max-Planck-Institut für Molekulare Pflanzenphysiologie, 14476 Golm, Germany (J.H., J.K.)

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.

² These authors contributed equally to the article.

The author responsible for the distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Martin Hagemann (martin.hagemann{at}uni-rostock.de).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.129403

^* Corresponding author; e-mail martin.hagemann{at}uni-rostock.de.

Received September 5, 2008; accepted October 16, 2008; published October 22, 2008.