Skip to main content
Log in

Respiratory terminal oxidases alleviate photo-oxidative damage in photosystem I during repetitive short-pulse illumination in Synechocystis sp. PCC 6803

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Oxygenic phototrophs are vulnerable to damage by reactive oxygen species (ROS) that are produced in photosystem I (PSI) by excess photon energy over the demand of photosynthetic CO2 assimilation. In plant leaves, repetitive short-pulse (rSP) illumination produces ROS to inactivate PSI. The production of ROS is alleviated by oxidation of the reaction center chlorophyll in PSI, P700, during the illumination with the short-pulse light, which is supported by flavodiiron protein (FLV). In this study, we found that in the cyanobacterium Synechocystis sp. PCC 6803 P700 was oxidized and PSI was not inactivated during rSP illumination even in the absence of FLV. Conversely, the mutant deficient in respiratory terminal oxidases was impaired in P700 oxidation during the illumination with the short-pulse light to suffer from photo-oxidative damage in PSI. Interestingly, the other cyanobacterium Synechococcus sp. PCC 7002 could not oxidize P700 without FLV during rSP illumination. These data indicate that respiratory terminal oxidases are critical to protect PSI from ROS damage during rSP illumination in Synechocystis sp. PCC 6803 but not Synechococcus sp. PCC 7002.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro EM (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci USA 110:4111–4116

    Article  PubMed  Google Scholar 

  • Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Allen MM (1968) Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4:1–4

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, Schreiber U (1993) Effects of inorganic carbon accumulation on photosynthetic oxygen reduction and cyclic electron flow in the cyanobacterium Synechococcus PCC7942. Photosynth Res 37:177–191

    Article  PubMed  CAS  Google Scholar 

  • Bolychevtseva YV, Kuzminov FI, Elanskaya IV, Gorbunov MY, Karapetyan NV (2015) Photosystem activity and state transitions of the photosynthetic apparatus in cyanobacterium Synechocystis PCC 6803 mutants with different redox state of the plastoquinone pool. Biochemistry 80:50–60

    PubMed  CAS  Google Scholar 

  • Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cazzaniga S, Li Z, Niyogi KK, Bassi R, Dall’Osto L (2012) The Arabidopsis szl1 mutant reveals a critical role of β-carotene in photosystem I photoprotection. Plant Physiol 159:1745–1758

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chaux F, Burlacot A, Mekhalfi M, Auroy P, Blangy S, Richaud P, Peltier G (2017) Flavodiiron proteins promote fast and transient O2 photoreduction in Chlamydomonas. Plant Physiol. https://doi.org/10.1104/pp.17.00421

    Article  PubMed  PubMed Central  Google Scholar 

  • Cooley JW, Vermaas WFJ (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological function. J Bacteriol 183:4251–4258

    Article  PubMed  PubMed Central  CAS  Google 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 171:1307–1319

    PubMed  PubMed Central  CAS  Google Scholar 

  • Feilke K, Streb P, Cornic G, Perreau F, Kruk J, Krieger-Liszkay A (2016) Effect of Chlamydomonas plastid terminal oxidase 1 expressed in tobacco on photosynthetic electron transfer. Plant J 85:219–228

    Article  PubMed  CAS  Google Scholar 

  • Fujisawa T, Narikawa R, Maeda S, Watanabe S, Kanesaki Y, Kobayashi K, Nomata J, Hanaoka M, Watanabe M, Ehira S, Suzuki E, Awai K, Nakamura Y (2017) CyanoBase: a large-scale update on its 20th anniversary. Nucleic Acids Res 45:D551-D554

    Article  PubMed  CAS  Google Scholar 

  • Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114

    Article  PubMed  CAS  Google Scholar 

  • Grimme L, Boardman N (1972) Photochemical activities of a particle fraction P1 obtained from the green alga Chlorella fusca. Biochem Biophys Res Commun 49:1617–1623

    Article  PubMed  CAS  Google 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. https://doi.org/10.1111/ppl.12580

    Article  PubMed  Google 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 78:384–393

    Article  PubMed  CAS  Google Scholar 

  • Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235

    Article  PubMed  CAS  Google Scholar 

  • Helman Y, Barkan E, Eisenstadt D, Luz B, Kaplan A (2005) Fractionation of the three stable oxygen isotopes by oxygen-producing and oxygen-consuming reactions in photosynthetic organisms. Plant Physiol 138:2292–2298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hirano M, Satoh K, Katoh S (1980) Plastoquinone as a common link between photosynthesis and respiration in a blue-green alga. Photosynth Res 1:149–162

    Article  PubMed  CAS  Google Scholar 

  • Joët T, Genty B, Josse E-M, Kuntz M, Cournac L, Peltier G (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J Biol Chem 277:31623–31630

    Article  PubMed  CAS  Google Scholar 

  • Johnson GN, Stepien P (2016) Plastid terminal oxidase as a route to improving plant stress tolerance: known knowns and known unknowns. Plant Cell Physiol 57:1387–1396

    PubMed  CAS  Google Scholar 

  • Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase. Nature 291:513–515

    Article  CAS  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268

    Article  CAS  Google Scholar 

  • Kramer DM, Avenson TJ, Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357

    Article  PubMed  CAS  Google Scholar 

  • Lea-Smith DJ, Ross N, Zori M, Bendall DS, Dennis JS, Scott SA, Smith AG, Howe CJ (2013) Thylakoid terminal oxidases are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol 162:484–495

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li H, Jubelirer S, Garcia Costas AM, Frigaard N-U, Bryant DA (2009) Multiple antioxidant proteins protect Chlorobaculum tepidum against oxygen and reactive oxygen species. Arch Microbiol 191:853

    Article  PubMed  CAS  Google Scholar 

  • McConnell MD, Koop R, Vasil’ev S, Bruce D (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol 130:1201–1212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miyake C, Miyata M, Shinzaki Y, Tomizawa K (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves-relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol 46:629–637

    Article  PubMed  CAS  Google Scholar 

  • Nomura CT, Persson S, Shen G, Inoue-Sakamoto K, Bryant DA (2006) Characterization of two cytochrome oxidase operons in the marine cyanobacterium Synechococcus sp. PCC 7002: inactivation of ctaDI affects the PS I:PS II ratio. Photosynth Res 87:215

    Article  PubMed  CAS  Google Scholar 

  • Paumann M, Regelsberger G, Obinger C, Peschek GA (2005) The bioenergetic role of dioxygen and the terminal oxidase(s) in cyanobacteria. Biochim Biophys Acta Bioenerg 1707:231–253

    Article  CAS  Google Scholar 

  • Pils D, Schmetterer G (2001) Characterization of three bioenergetically active respiratory terminal oxidases in the cyanobacterium Synechocystis sp. strain PCC 6803. FEMS Microbiol Lett 203:217–222

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  PubMed  CAS  Google Scholar 

  • Schuurmans RM, van Alphen P, Schuurmans JM, Matthijs HCP, Hellingwerf KJ (2015) Comparison of the photosynthetic yield of cyanobacteria and green algae: different methods give different answers. PLoS ONE 10:e0139061

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sedoud A, López-Igual R, ur Rehman A, Wilson A, Perreau F, Boulay C, Vass I, Krieger-Liszkay A, Kirilovsky D (2014) The cyanobacterial photoactive orange carotenoid protein is an excellent singlet oxygen quencher. Plant Cell 26:1781–1791

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sejima T, Takagi D, Fukayama H, Makino A, Miyake C (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol 55:1184–1193

    Article  PubMed  CAS  Google 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 57:1443–1453

    PubMed  CAS  Google Scholar 

  • Shimakawa G, Iwamoto T, Mabuchi T, Saito R, Yamamoto H, Amako K, Sugimoto T, Makino A, Miyake C (2013) Acrolein, an α,β-unsaturated carbonyl, inhibits both growth and PSII activity in the cyanobacterium Synechocystis sp. PCC 6803. Biosci Biotechnol Biochem 77:1655–1660

    Article  PubMed  CAS  Google Scholar 

  • Shimakawa G, Hasunuma T, Kondo A, Matsuda M, Makino A, Miyake C (2014) Respiration accumulates Calvin cycle intermediates for the rapid start of photosynthesis in Synechocystis sp. PCC 6803. Biosci Biotechnol Biochem 78:1997–2007

    Article  PubMed  CAS  Google Scholar 

  • Shimakawa G, Shaku K, Nishi A, Hayashi R, Yamamoto H, Sakamoto K, Makino A, Miyake C (2015) FLAVODIIRON2 and FLAVODIIRON4 proteins mediate an oxygen-dependent alternative electron flow in Synechocystis sp. PCC 6803 under CO2-limited conditions. Plant Physiol 167:472–480

    Article  PubMed  CAS  Google Scholar 

  • Shimakawa G, Shaku K, Miyake C (2016a) Oxidation of P700 in photosystem I is essential for the growth of cyanobacteria. Plant Physiol 172:1443–1450

    Article  PubMed  PubMed Central  CAS  Google 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 130:293–305

    Article  PubMed  CAS  Google Scholar 

  • Shimakawa G, Ishizaki K, Tsukamoto S, Tanaka M, Sejima T, Miyake C (2017) The liverwort, Marchantia, drives alternative electron flow using a flavodiiron protein to protect PSI. Plant Physiol 173:1636–1647

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    Article  PubMed  CAS  Google Scholar 

  • Stevens SE, Porter RD (1980) Transformation in Agmenellum quadruplicatum. Proc Natl Acad Sci USA 77:6052–6056

    Article  PubMed  CAS  Google Scholar 

  • Takagi D, Takumi S, Hashiguchi M, Sejima T, Miyake C (2016a) Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol 171:1626–1634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takagi D, Hashiguchi M, Sejima T, Makino A, Miyake C (2016b) Photorespiration provides the chance of cyclic electron flow to operate for the redox-regulation of P700 in photosynthetic electron transport system of sunflower leaves. Photosynth Res 129:279–290

    Article  PubMed  CAS  Google 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. https://doi.org/10.1111/ppl.12562

    Article  PubMed  Google Scholar 

  • Tikhonov AN, Khomutov GB, Ruuge EK, Blumenfeld LA (1981) Electron transport control in chloroplasts. Effects of photosynthetic control monitored by the intrathylakoid pH. Biochim Biophys Acta Bioenerg 637:321–333

    Article  CAS  Google Scholar 

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  PubMed  Google Scholar 

  • Vicente JB, Gomes CM, Wasserfallen A, Teixeira M (2002) Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem Biophys Res Commun 294:82–87

    Article  PubMed  CAS  Google Scholar 

  • Wiese C, Shi L, Heber U (1998) Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation. Physiol Plant 102:437–446

    Article  CAS  Google Scholar 

  • Williams JGK (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167:766–778

    Article  CAS  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zivcak M, Brestic M, Kunderlikova K, Sytar O, Allakhverdiev SI (2015) Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynth Res 126:449–463

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. Akihiko Kondo, Prof. Tomohisa Hasunuma, and Dr. Shimpei Aikawa (Kobe University) for supplying the Synechococcus sp. PCC 7002 wild type. This work was supported by the Japan Society for the Promotion of Science (JSPS; Grant No. 26450079 to C.M.) and by 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. is supported by a JSPS research fellowship (Grant No. 16J03443). We would like to thank Editage (http://www.editage.jp) for English language editing.

Author information

Authors and Affiliations

Authors

Contributions

CM conceived the original screening and research plans; CM supervised the experiments; GS performed all of the experiments; CM and GS designed the experiments and analyzed the data; CM and GS conceived the project and wrote the article.

Corresponding author

Correspondence to Chikahiro Miyake.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 465 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shimakawa, G., Miyake, C. Respiratory terminal oxidases alleviate photo-oxidative damage in photosystem I during repetitive short-pulse illumination in Synechocystis sp. PCC 6803. Photosynth Res 137, 241–250 (2018). https://doi.org/10.1007/s11120-018-0495-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-018-0495-y

Keywords

Navigation