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Comparative analysis of strategies to prepare electron sinks in aquatic photoautotrophs

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Abstract

While subject to illumination, photosystem I (PSI) has the potential to produce reactive oxygen species (ROS) that can cause photo-oxidative damage in oxygenic photoautotrophs. The reaction center chlorophyll in PSI (P700) is kept oxidized in excess light conditions to limit over-excitation of PSI and alleviate the production of ROS. Oxidation of P700 requires a sufficient electron sink for PSI, which is responsible for flavodiiron proteins (FLV) safely dissipating electrons to O2 in cyanobacteria, green algae, and land plants except for angiosperms during short-pulse light (SP) illumination under which photosynthesis and photorespiration do not occur. This fact implies that O2 usage is essential for P700 oxidation but also raises the question why angiosperms lost FLV. Here, we first found that aquatic photoautotrophs in red plastid lineage, in which no gene for FLV has been found, could keep P700 oxidized during SP illumination alleviating the photo-oxidative damage in PSI even without O2 usage. We comprehensively assessed P700 oxidation during SP illumination in the presence and absence of O2 in cyanobacteria (Cyanophyta), green algae (Chlorophyta), angiosperms (Streptophyta), red algae (Rhodophyta), and secondary algae (Cryptophyta, Haptophyta, and Heterokontophyta). A variety of dependencies of P700 oxidation on O2 among these photoautotrophs clearly suggest that O2 usage and FLV are not universally required to oxidize P700 for protecting PSI against ROS damage. Our results expand the understanding of the diverse strategies taken by oxygenic photoautotrophs to oxidize P700 and mitigate the risks of ROS.

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Acknowledgements

The authors thank Prof. Yuichiro Takahashi (Okayama University) for supplying the culture of Chlamydomonas reinhardtii and Editage (http://www.editage.jp) for providing English corrections.

Funding

This work was supported by the Japan Society for the Promotion of Science (JSPS; Grant No. 26450079 to C.M.) and the Core Research for Evolutional Science and Technology (CREST) division of the Japan Science and Technology Agency (Grant No. AL65D21010 to C.M.). G.S. was supported as a JSPS research fellow (Grant No. 16J03443).

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Authors and Affiliations

  1. Department of Biological and Environmental Science, Faculty of Agriculture, Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai, Nada, Kobe, Hyogo, 657-8501, Japan

    Ginga Shimakawa, Ayumi Wada & Chikahiro Miyake

  2. Kobe University Research Center for Inland Seas, 2746 Iwaya, Awaji, Hyogo, 656-2401, Japan

    Akio Murakami

  3. Fisheries Technology Institute, Hyogo Prefectural Technology Center for Agriculture, Forestry and Fisheries, Akashi, Hyogo, 674-0093, Japan

    Kyosuke Niwa

  4. Department of Marine Biosciences, Faculty of Marine Life Science, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato, Tokyo, 108-8477, Japan

    Kyosuke Niwa

  5. Research Center for the Development of Intelligent Self-Organized Biomaterials, Research Center for Environmental Bioscience, Department of Bioscience, Kwansei-Gakuin University, 2-1 Gakuen, Sanda, Hyogo, 669-1337, Japan

    Yusuke Matsuda

  6. Core Research for Environmental Science and Technology, Japan Science and Technology Agency, 7 Goban, Chiyoda, Tokyo, 102-0076, Japan

    Chikahiro Miyake

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  1. Ginga Shimakawa
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  2. Akio Murakami
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  3. Kyosuke Niwa
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  4. Yusuke Matsuda
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  5. Ayumi Wada
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Contributions

CM conceived the original screening and research plans; CM supervised the experiments; GS performed most of the experiments; AM, KN, YM, and AW provided technical assistance to GS; CM and GS designed the experiments and analyzed the data; CM and GS conceived the project and wrote the manuscript.

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Correspondence to Chikahiro Miyake.

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Supplemental Fig. S1

. Residual total oxidizable P700 after rSP illumination (20,000 μmol photons m−2 s−1, 1 s, every 10 s, for 30 min) in N2 gas presence in the cyanobacterium (Synechococcus elongatus PCC 7942), in the green algae (Chlamydomonas reinhardtii, Ulva pertusa and Codium fragile), in the angiosperms (Ipomoea nil, Nymphaea tetragona, Magnolia kobus and Zostera marina), in the red algae (Pyropia yezoensis, Porphyridium aerugineum, Porphyridium purpureum, Chondrus ocellatus, Chondrus giganteus, Callophyllis japonica and Grateloupia lanceolata), in the unicellular secondary algae (Chroomonas placoidea, Isochrysis galbana, Nannochloropsis oceanica, Vischeria punctata and Phaeodactylum tricornutum) and in the brown algae (Ecklonia cava, Dictyota dichotoma, Sargassum horneri and Undaria pinnatifida). Bars represent mean ± SD (n = 3). (PDF 224 KB)

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Shimakawa, G., Murakami, A., Niwa, K. et al. Comparative analysis of strategies to prepare electron sinks in aquatic photoautotrophs. Photosynth Res 139, 401–411 (2019). https://doi.org/10.1007/s11120-018-0522-z

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