Abstract
Cyanobacteria are photoautotrophic prokaryotes with a plant-like photosynthetic machinery. Because of their short generation times, the ease of their genetic manipulation, and the limited size of their genome and proteome, cyanobacteria are popular model organisms for photosynthetic research. Although the principal mechanisms of photosynthesis are well-known, much less is known about the biogenesis of the thylakoid membrane, hosting the components of the photosynthetic, and respiratory electron transport chain in cyanobacteria. Here we present a detailed proteome analysis of the important model and host organism Synechocystis sp. PCC 6803 under light-activated heterotrophic growth conditions. Because of the mechanistic importance and severe changes in thylakoid membrane morphology under light-activated heterotrophic growth conditions, a focus was put on the analysis of the membrane proteome, which was supported by a targeted lipidome analysis. In total, 1528 proteins (24.5% membrane integral) were identified in our analysis. For 641 of these proteins quantitative information was obtained by spectral counting. Prominent changes were observed for proteins associated with oxidative stress response and protein folding. Because of the heterotrophic growth conditions, also proteins involved in carbon metabolism and C/N-balance were severely affected. Although intracellular thylakoid membranes were significantly reduced, only minor changes were observed in their protein composition. The increased proportion of the membrane-stabilizing sulfoqinovosyl diacyl lipids found in the lipidome analysis, as well as the increased content of lipids with more saturated acyl chains, are clear indications for a coordinated synthesis of proteins and lipids, resulting in stabilization of intracellular thylakoid membranes under stress conditions.
Highlights
From the ‡Plant Biochemistry, Faculty of Biology & Biotechnology, Ruhr-University Bochum, 44780 Bochum, Germany; §Department of Pharmacy and Biochemistry, Johannes Gutenberg-University Mainz, 55128 Mainz, Germany; ¶Department of Molecular Cell Biology, Bielefeld University, 33615 Bielefeld, Germany
Experimental Strategy—Growth under lightactivated heterotrophic growth (LAHG) conditions has a serious impact on the structure of Synechocystis cells
The chlorophyll content per cell dramatically decreases [15], and severe reduction of pigment-binding protein complexes is one of the most prominent phenotype associated with LAHG conditions
Summary
LAHG conditions on the abundance of soluble Synechocystis proteins have been analyzed previously, only 23 proteins with a significantly altered expression level (LAHG versus autotrophic growth) have been described. It is essentially still completely enigmatic how the formation of internal TM is controlled, some proteins have been suggested to be involved These proteins include the vesicle inducing protein in plastids 1 (Vipp1), DnaK proteins, a prohibitin-like protein, as well as the YidC protein, a membrane protein integrase (16 –19). Some proteins have been suggested to be more directly involved in TM formation, the stability of the TM is globally affected indirectly by pathways, which control the biogenesis of lipids and/or cofactors, and mutants defective in synthesis of chlorophyll or of the membrane lipid phosphatidylglycerol (PG) have severely reduced TM systems [20, 21]. The effect on Synechocystis lipids was analyzed in a targeted mass spectrometric approach, revealing significant adjustment of fatty acid saturation in response to the LAHG conditions
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