Comparative analysis of strategies to prepare electron sinks in aquatic photoautotrophs
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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.
KeywordsReactive oxygen species P700 oxidation Photosystem I Seaweeds
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.
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.
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).
Compliance with ethical standards
Conflict of interest
The authors have no conflict of interest to declare.
- Bailleul B, Berne N, Murik O, Petroutsos D, Prihoda J, Tanaka A, Villanova V, Bligny R, Flori S, Falconet D, Krieger-Liszkay A, Santabarbara S, Rappaport F, Joliot P, Tirichine L, Falkowski PG, Cardol P, Bowler C, Finazzi G (2015) Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524:366–369CrossRefGoogle Scholar
- Curien G, Flori S, Villanova V, Magneschi L, Giustini C, Forti G, Matringe M, Petroutsos D, Kuntz M, Finazzi G (2016) The water to water cycles in microalgae. Plant Cell Physiol 57:1354–1363Google Scholar
- Ermakova M, Huokko T, Richaud P, Bersanini L, Howe CJ, Lea-Smith DJ, Peltier G, Allahverdiyeva Y (2016) Distinguishing the roles of thylakoid respiratory terminal oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 171:1307–1319Google Scholar
- Flori S, Jouneau P-H, Bailleul B, Gallet B, Estrozi LF, Moriscot C, Bastien O, Eicke S, Schober A, Bártulos CR, Maréchal E, Kroth PG, Petroutsos D, Zeeman S, Breyton C, Schoehn G, Falconet D, Finazzi G (2017) Plastid thylakoid architecture optimizes photosynthesis in diatoms. Nat Commun 8:15885CrossRefGoogle Scholar
- Hanawa H, Ishizaki K, Nohira K, Takagi D, Shimakawa G, Sejima T, Shaku K, Makino A, Miyake C (2017) Land plants drive photorespiration as higher electron-sink: comparative study of post-illumination transient O2-uptake rates from liverworts to angiosperms through ferns and gymnosperms. Physiol Plant 161:138–149CrossRefGoogle Scholar
- Hayashi R, Shimakawa G, Shaku K, Shimizu S, Akimoto S, Yamamoto H, Amako K, Sugimoto T, Tamoi M, Makino A, Miyake C (2014) O2-dependent large electron flow functioned as an electron sink, replacing the steady-state electron flux in photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803, but not in the cyanobacterium Synechococcus sp. PCC 7942. Biosci Biotechnol Biochem 78:384–393CrossRefGoogle Scholar
- Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33:541–553Google Scholar
- Mosebach L, Heilmann C, Mutoh R, Gäbelein P, Steinbeck J, Happe T, Ikegami T, Hanke G, Kurisu G, Hippler M (2017) Association of Ferredoxin: NADP+ oxidoreductase with the photosynthetic apparatus modulates electron transfer in Chlamydomonas reinhardtii. Photosynth Res 134:291–306CrossRefGoogle Scholar
- Rippka R, Waterbury JB, Stanier RY (1981) Isolation and purification of cyanobacteria: Some general principles. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes: a handbook on habitats, isolation, and identification of bacteria. Springer Berlin Heidelberg, Berlin, pp 212–220CrossRefGoogle Scholar
- Schmitt F, Kreslavski VD, Zharmukhamedov SK, Friedrich T, Renger G, Los DA, Kuznetsov VV, Allakhverdiev SI (2015) The multiple roles of various reactive oxygen species (ROS) in photosynthetic organisms. In Photosynthesis, Allakhverdiev SI (ed). https://doi.org/10.1002/9781119084150.ch1
- Schreiber U, Klughammer C (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Appl Notes 1:11–14Google Scholar
- Shaku K, Shimakawa G, Hashiguchi M, Miyake C (2016) Reduction-induced suppression of electron flow (RISE) in the photosynthetic electron transport system of Synechococcus elongatus PCC 7942. Plant Cell Physiol 57:1443–1453Google Scholar
- Shimakawa G, Akimoto S, Ueno Y, Wada A, Shaku K, Takahashi Y, Miyake C (2016b) Diversity in photosynthetic electron transport under [CO2]-limitation: the cyanobacterium Synechococcus sp. PCC 7002 and green alga Chlamydomonas reinhardtii drive an O2-dependent alternative electron flow and non-photochemical quenching of chlorophyll fluorescence during CO2-limited photosynthesis. Photosynth Res 130:293–305CrossRefGoogle Scholar
- Takagi D, Ishizaki K, Hanawa H, Mabuchi T, Shimakawa G, Yamamoto H, Miyake C (2017) Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I. Physiol Plant 161:56–74CrossRefGoogle Scholar