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SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION

A Systems-Level Analysis of the Effects of Light Quality on the Metabolism of a Cyanobacterium^1,[W],[OA]

Department of Biology, Washington University, St. Louis, Missouri 63130 (A.K.S., M.B.-P., H.B.P.); Department of Electrical and Systems Engineering, Washington University, St. Louis, Missouri 63130 (T.E.); Department of Mathematics and Statistics, Texas Tech University, Lubbock, Texas 79409 (B.G.); and Department of Molecular Microbiology and Immunology, Saint Louis University, St. Louis, Missouri 63104 (R.A.)

Photosynthetic organisms experience changes in light quantity and light quality in their natural habitat. In response to changes in light quality, these organisms redistribute excitation energy and adjust photosystem stoichiometry to maximize the utilization of available light energy. However, the response of other cellular processes to changes in light quality is mostly unknown. Here, we report a systematic investigation into the adaptation of cellular processes in Synechocystis species PCC 6803 to light that preferentially excites either photosystem II or photosystem I. We find that preferential excitation of photosystem II and photosystem I induces massive reprogramming of the Synechocystis transcriptome. The rewiring of cellular processes begins as soon as Synechocystis senses the imbalance in the excitation of reaction centers. We find that Synechocystis utilizes the cyclic photosynthetic electron transport chain for ATP generation and a major part of the respiratory pathway to generate reducing equivalents and carbon skeletons during preferential excitation of photosystem I. In contrast, cytochrome c oxidase and photosystem I act as terminal components of the photosynthetic electron transport chain to produce sufficient ATP and limited amounts of NADPH and reduced ferredoxin during preferential excitation of photosystem II. To overcome the shortage of NADPH and reduced ferredoxin, Synechocystis preferentially activates transporters and acquisition pathways to assimilate ammonia, urea, and arginine over nitrate as a nitrogen source. This study provides a systematic analysis of cellular processes in cyanobacteria in response to preferential excitation and shows that the cyanobacterial cell undergoes significant adjustment of cellular processes, many of which were previously unknown.

The author responsible for 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: Himadri B. Pakrasi (pakrasi{at}wustl.edu).

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www.plantphysiol.org/cgi/doi/10.1104/pp.109.144824

^* Corresponding author; e-mail pakrasi{at}wustl.edu.

Received July 15, 2009; accepted September 14, 2009; published September 16, 2009.