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Extra O2 evolution reveals an O2-independent alternative electron sink in photosynthesis of marine diatoms

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Abstract

Following the principle of oxygenic photosynthesis, electron transport in the thylakoid membranes (i.e., light reaction) generates ATP and NADPH from light energy, which is subsequently utilized for CO2 fixation in the Calvin-Benson-Bassham cycle (i.e., dark reaction). However, light and dark reactions could discord when an alternative electron flow occurs with a rate comparable to the linear electron flow. Here, we quantitatively monitored O2 and total dissolved inorganic carbon (DIC) during photosynthesis in the pennate diatom Phaeodactylum tricornutum, and found that evolved O2 was larger than the consumption of DIC, which was consistent with 14CO2 measurements in literature. In our measurements, the stoichiometry of O2 evolution to DIC consumption was always around 1.5 during photosynthesis at different DIC concentrations. The same stoichiometry was observed in the cells grown under different CO2 concentrations and nitrogen sources except for the nitrogen-starved cells showing O2 evolution 2.5 times larger than DIC consumption. An inhibitor to nitrogen assimilation did not affect the extra O2 evolution. Further, the same physiological phenomenon was observed in the centric diatom Thalassiosira pseudonana. Based on the present dataset, we propose that the marine diatoms possess the metabolic pathway(s) functioning as the O2-independent electron sink under steady state photosynthesis that reaches nearly half of electron flux of the Calvin-Benson-Bassham cycle.

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Data availability

The data of physiological analyses in this manuscript are available from the corresponding author upon request.

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Acknowledgements

We would like to thank Dr. Matthew B. Brown (Kwansei Gakuin University) for many helpful advices and for kindly proofreading our English writing.

Funding

This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI (19H01153 to G.S. and Y.M.) and by JST CREST “Cell dynamics” (JPMJCR20E1 to Y.M.).

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  1. Department of Bioscience, School of Biological and Environmental Sciences, Kwansei Gakuin University, 1 Gakuen Uegahara, Sanda, Hyogo, 669-1330, Japan

    Ginga Shimakawa & Yusuke Matsuda

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  1. Ginga Shimakawa
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  2. Yusuke Matsuda
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GS designed the research plans, performed the experiments, analyzed the data, and wrote the manuscript with the assistance from YM.

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Correspondence to Ginga Shimakawa.

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Shimakawa, G., Matsuda, Y. Extra O2 evolution reveals an O2-independent alternative electron sink in photosynthesis of marine diatoms. Photosynth Res 159, 61–68 (2024). https://doi.org/10.1007/s11120-023-01073-3

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