A Systems-Level Analysis of the Effects of Light Quality on the Metabolism of a Cyanobacterium

Abhay K Singh,Bijoy Ghosh,Rajeev Aurora,Thanura Elvitigala,Maitrayee Bhattacharyya-Pakrasi,Himadri B Pakrasi

doi:10.1104/pp.109.144824

Abstract

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.

Highlights

Light is one of the most important environmental factors for photosynthetic organisms
Cells under photosystem II (PSII) light grew at a rate that was comparable to growth of cells under white light
We have systematically investigated the adaptation of cellular processes in Synechocystis in response to changes in light quality

Summary

Introduction

Light is one of the most important environmental factors for photosynthetic organisms. The primary reactions of oxygenic photosynthesis are catalyzed by two large pigment-protein complexes, photosystem II (PSII) and photosystem I (PSI) (reviewed in Pakrasi, 1995). These two complexes act in series to drive several light-dependent electrochemical reactions. The electrons from reduced PQ are transferred to PSI via a membrane-bound cytochrome b6f complex and a diffusible pool of plastocyanin or cytochrome c553 leading to reduction of ferredoxin and NADP+ The ability of both PSII and PSI to catalyze electrochemical reactions is dependent on the presence of unique light harvesting antennae structures that are used for the efficient absorption of light. Two major phycobiliproteins commonly present in the PBS of cyanobacteria are the red-light absorbing allophycocyanin (AP) with λmax ≈ 650 nm and phycocyanin (PC) with λmax ≈ 620 nm

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Conclusion