Control of the cyanobacterial day-night metabolism by a biological clock system

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In natural environments, cyanobacteria are subjected to changing and often unpredictable environmental conditions. Some of the changes are, however, predictable, such as the day-night switch. For photosynthetic organisms, growth in such a light-dark cycle requires a complete reversal of their metabolism. Photosynthesis and CO2 fixation is performed during the day because these processes are light-dependent. At night, the glycogen reserves that were synthesized during the light period are degraded and the cells therefore transition from a photoautotrophic to a heterotrophic metabolism. Cyanobacteria are able to predict the daily changes in light availability using a biological clock which shares no homology to known clock systems from eukaryotic organisms. In our previous studies we revealed that homologs of the known bacterial-type clock proteins are important for the growth of the model cyanobacterium Synechocystis sp. PCC 6803 in light-dark cycles. Our studies of the effects of clock mutations on central metabolism in the light and the dark strongly contributed to the aim of the research unit “The Autotrophy Heterotrophy Switch in Cyanobacteria: Coherent decision-making on multiple regulatory layers” (abbreviated “SCyCode”). In close cooperation with SCyCode experts in metabolic and proteomic analyses, we revealed especially strong changes in the dark metabolism of Synechocystis sp. PCC 6803 clock mutants. Most importantly, a defective clock system in this organism led to a failure to switch off the activity of the carbon fixing enzyme RubisCO in the dark and a deficiency in the accumulation of the storage compound polyhydroxybutyrate, a biopolymer of biotechnological potential. Further, we studied an alternative clock system which we found to be relevant for heterotrophic growth. During the second funding period, we will focus on a mechanistic understanding of the role of the different clock proteins in the switch between autotrophy and heterotrophy in day-night cycles. The experiments which we have designed in cooperation with SCyCode members should identify the direct targets of the different clock systems, explain how Synechocystis clock proteins contribute to the regulation of carbon fixation and how clock-dependent protein phosphorylation and gene expression changes allow a balanced cyanobacterial metabolism in a day-night rhythm. These insights might be of crucial importance for potential biotechnological applications for sustainable exploitation of phototrophic microorganisms.