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Distinguishing the Roles of Thylakoid Respiratory Terminal Oxidases in the Cyanobacterium Synechocystis sp. PCC 6803.

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Ermakova, Maria 
Huokko, Tuomas 
Richaud, Pierre 
Bersanini, Luca 
Howe, Christopher J 


Various oxygen-utilizing electron sinks, including the soluble flavodiiron proteins (Flv1/3), and the membrane-localized respiratory terminal oxidases (RTOs), cytochrome c oxidase (Cox) and cytochrome bd quinol oxidase (Cyd), are present in the photosynthetic electron transfer chain of Synechocystis sp. PCC 6803. However, the role of individual RTOs and their relative importance compared with other electron sinks are poorly understood, particularly under light. Via membrane inlet mass spectrometry gas exchange, chlorophyll a fluorescence, P700 analysis, and inhibitor treatment of the wild type and various mutants deficient in RTOs, Flv1/3, and photosystem I, we investigated the contribution of these complexes to the alleviation of excess electrons in the photosynthetic chain. To our knowledge, for the first time, we demonstrated the activity of Cyd in oxygen uptake under light, although it was detected only upon inhibition of electron transfer at the cytochrome b6f site and in ∆flv1/3 under fluctuating light conditions, where linear electron transfer was drastically inhibited due to impaired photosystem I activity. Cox is mostly responsible for dark respiration and competes with P700 for electrons under high light. Only the ∆cox/cyd double mutant, but not single mutants, demonstrated a highly reduced plastoquinone pool in darkness and impaired gross oxygen evolution under light, indicating that thylakoid-based RTOs are able to compensate partially for each other. Thus, both electron sinks contribute to the alleviation of excess electrons under illumination: RTOs continue to function under light, operating on slower time ranges and on a limited scale, whereas Flv1/3 responds rapidly as a light-induced component and has greater capacity.



Electron Transport, Fluorescence, Light, Mutation, Oxidation-Reduction, Oxidoreductases, Oxygen, Photosynthesis, Photosystem I Protein Complex, Photosystem II Protein Complex, Plastoquinone, Synechocystis, Thylakoids

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Plant Physiol

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Oxford University Press (OUP)
This work was financially supported by the Academy of Finland Finnish Centre of Excellence in Molecular Biology of Primary Producers (2014-2 019) project #271832 and by the Kone Foundation (to Y.A.). L.B. was supported by the Alfred Kordelin Foundation, D.J.L-S by the Environmental Services Association Education Trust. Support was also provided by the HélioBiotec platform, funded by the European Union (European Regional Development Fund), the Région Provence Alpes Côte d’Azur, the French Ministry of Research, and the CEA.