Abstract
In Synechocystis sp. PCC 6803 and some other cyanobacteria photosystem I reaction centres exist predominantly as trimers, with minor contribution of monomeric form, when cultivated at standard optimized conditions. In contrast, in plant chloroplasts photosystem I complex is exclusively monomeric. The functional significance of trimeric organization of cyanobacterial photosystem I remains not fully understood. In this study, we compared the photosynthetic characteristics of PSI in wild type and psaL knockout mutant. The results show that relative to photosystem I trimer in wild-type cells, photosystem I monomer in psaL− mutant has a smaller P700+ pool size under low and moderate light, slower P700 oxidation upon dark-to-light transition, and slower P700+ reduction upon light-to-dark transition. The mutant also shows strongly diminished photosystem I donor side limitations [quantum yield Y(ND)] at low, moderate and high light, but enhanced photosystem I acceptor side limitations [quantum yield Y(NA)], especially at low light (22 µmol photons m−2 s−1). In line with these functional characteristics are the determined differences in the relative expression genes encoding of selected electron transporters. The psaL− mutant showed significant (ca fivefold) upregulation of the photosystem I donor cytochrome c6, and downregulation of photosystem I acceptors (ferredoxin, flavodoxin) and proteins of alternative electron flows originating in photosystem I acceptor side. Taken together, our results suggest that photosystem I trimerization in wild-type Synechocystis cells plays a role in the protection of photosystem I from photoinhibition via maintaining enhanced donor side electron transport limitations and minimal acceptor side electron transport limitations at various light intensities.
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References
Allahverdiyeva Y, Isojärvi J, Zhang P, Aro E-M (2015) Cyanobacterial oxygenic photosynthesis is protected by flavodiiron proteins. Life 5:716–743
Allen MM (1968) Simple conditions for growth of unicellular blue-green algae on Plates 1, 2. J Phycol 4:1–4. https://doi.org/10.1111/j.1529-8817.1968.tb04667.x
Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84(1–3):173–180
Ashby MK, Mullineaux CW (1999) Cyanobacterial ycf27 gene products regulate energy transfer from phycobilisomes to photosystems I and II. FEMS Microbiol Lett 181(2):253–260. https://doi.org/10.1111/j.1574-6968.1999.tb08852.x
Bersanini L, Battchikova N, Jokel M et al (2014) Flavodiiron protein Flv2/Flv4-related photoprotective mechanism dissipates excitation pressure of PSII in cooperation with phycobilisomes in cyanobacteria. Plant Physiol 164:805–818. https://doi.org/10.1104/pp.113.231969
Boekema EJ, Dekker JP, Van Heel MG et al (1987) Evidence for a trimeric organization of the photosystem I complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 217:283–286
Chain RK, Malkin R (1979) On the interaction of 2,5-dibromo-3-methyl-6-isopropylbenzoquinone (DBMIB) with bound electron carriers in spinach chloroplasts. Arch Biochem Biophys 197:52–56. https://doi.org/10.1016/0003-9861(79)90217-0
Chaux F, Peltier G, Johnson X (2015) A security network in PSI photoprotection: regulation of photosynthetic control, NPQ and O2 photoreduction by cyclic electron flow. Front Plant Sci 6:875
Chitnis PR (2001) Photosystem I: function and physiology. Annu Rev Plant Biol 52:593–626
Chitnis VP, Chitnis PR (1993) PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336:330–334
Chitnis VP, Xu Q, Yu L et al (1993) Targeted inactivation of the gene psaL encoding a subunit of photosystem I of the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 268:11678–11684
Chukhutsina V, Bersanini L, Aro EM, Van Amerongen H (2015) Cyanobacterial light-harvesting phycobilisomes uncouple from photosystem I during dark-to-light transitions. Sci Rep 5:14193. https://doi.org/10.1038/srep14193
Dashdorj N, Xu W, Cohen RO et al (2005) Asymmetric electron transfer in cyanobacterial photosystem I: charge separation and secondary electron transfer dynamics of mutations near the primary electron acceptor A0. Biophys J 88:1238–1249
Domonkos I, Malec P, Sallai A et al (2004) Phosphatidylglycerol is essential for oligomerization of photosystem I reaction center. Plant Physiol 134:1471–1478
Farineau J, Bottin H, Garab G (1984) Effect of dibromothymoquinone (DBMIB) on reduction rates of photosystem I donors in intact chloroplasts. Biochem Biophys Res Commun 120:721–725. https://doi.org/10.1016/S0006-291X(84)80166-7
Fischer N, Sétif P, Rochaix JD (1999) Site-directed mutagenesis of the PsaC subunit of photosystem I. F(B) is the cluster interacting with soluble ferredoxin. J Biol Chem 274:23333–23340. https://doi.org/10.1074/jbc.274.33.23333
Frank J, Pompella A, Biesalski HK (2002) Immunohistochemical detection of protein oxidation. In: Armstrong D (ed) Oxidants and antioxidants. Methods in molecular biology™, vol 196. Humana Press, Totowa, pp 35–40. https://doi.org/10.1385/1-59259-274-0:35
Glazer AN, Stryer L (1984) Phycofluor probes. Trends Biochem Sci 9(10):423–427
He Z, Zheng F, Wu Y et al (2015) NDH-1L interacts with ferredoxin via the subunit NdhS in Thermosynechococcus elongatus. Photosynth Res 126:341–349. https://doi.org/10.1007/s11120-015-0090-4
Howitt CA, Udall PK, Vermaas WF (1999) Type 2 NADH dehydrogenases in the cyanobacterium Synechocystis sp. strain PCC 6803 are involved in regulation rather than respiration. J Bacteriol 181:3994–4003.
Ilík P, Pavlovič A, Kouřil R et al (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytol 214:967–972. https://doi.org/10.1111/nph.14536
Ivanov AG, Krol M, Sveshnikov D et al (2006) Iron deficiency in cyanobacteria causes monomerization of photosystem I trimers and reduces the capacity for state transitions and the effective absorption cross section of photosystem I in vivo. Plant Physiol 141:1436–1445
Kamlowski A, Altenberg-Greulich B, Van Der Est A et al (1998) The quinone acceptor A1 in photosystem I: binding site, and comparison to QA in purple bacteria reaction centers. J Phys Chem B 102:8278–8287
Karapetyan NV, Holzwarth AR, Rögner M (1999) The photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and physiological significance. FEBS Lett. https://doi.org/10.1016/S0014-5793(99)01352-6
Kass H, Fromme P, Witt HT, Lubitz W (2001) Orientation and electronic structure of the primary donor radical cation P+ 700 in photosystem I: a single crystals EPR and ENDOR study. J Phys Chem 105:1225–1239
Kłodawska K, Kovács L, Várkonyi Z et al (2015) Elevated growth temperature can enhance photosystem I trimer formation and affects xanthophyll biosynthesis in cyanobacterium Synechocystis sp. PCC 6803 cells. Plant Cell Physiol 56:558–571. https://doi.org/10.1093/pcp/pcu199
Klughammer C, Schreiber U (1991) Analysis of light-induced absorbency changes in the near-infrared spectral region. 1. Characterization of various components in isolated-chloroplasts. Z Nat C 46:233–244. https://doi.org/10.1515/znc-1991-3-413
Klughammer C, Schreiber U (2008) Saturation Pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14
Kovacs T, Szalontai B, Kłodawska K, Vladkova R, Malec P, Gombos Z, Laczko-Dobos H (2019) Photosystem I oligomerization affects lipid composition in Synechocystis sp. PCC 6803. Biochim Biophys Acta 57:8–15. https://doi.org/10.1016/j.bbalip.2019.06.013
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218. https://doi.org/10.1023/B:PRES.0000015391.99477.0d
Kubota-Kawai H, Mutoh R, Shinmura K et al (2018) X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex. Nat Plants 4:218–224. https://doi.org/10.1038/s41477-018-0130-0
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lakshmi K, Jung Y, Golbeck J (1999) The iron–sulfur clusters FA and FB in photosystem I: an electron paramagnetic resonance. Biochemistry 38:13210–13215
Lea-Smith DJ, Bombelli P, Vasudevan R, Howe CJ (2016) Photosynthetic, respiratory and extracellular electron transport pathways in cyanobacteria. Biochim Biophys Acta 1857:247–255. https://doi.org/10.1016/j.bbabio.2015.10.007
Lima-Melo Y, Alencar VTCB, Lobo AKM, Sousa RHV, Tikkanen M, Aro E-M et al (2019) Photoinhibition of photosystem I provides oxidative protection during imbalanced photosynthetic electron transport in Arabidopsis thaliana. Front Plant Sci 10:1–13. https://doi.org/10.3389/fpls.2019.00916
Liu LN (2016) Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1857:256–265. https://doi.org/10.1016/j.bbabio.2015.11.010
Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342(6162):1104–1107. https://doi.org/10.1126/science.1242321
Malakhov MP, Malakhova OA, Murata N (1999) Balanced regulation of expression of the gene for cytochrome cM and that of genes for plastocyanin and cytochrome c 6 in Synechocystis. FEBS Lett 444:281–284
Malavath T, Caspy I, Netzer-El SY et al (2018) Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis. Biochim Biophys Acta 1859:645–654. https://doi.org/10.1016/j.bbabio.2018.02.002
Mullineaux CW (2014a) Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1837:503–511. https://doi.org/10.1016/j.bbabio.2013.11.017
Mullineaux CW (2014b) Electron transport and light-harvesting switches in cyanobacteria. Front Plant Sci 5:1–6. https://doi.org/10.3389/fpls.2014.00007
Munekage Y, Hojo M, Meurer J et al (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371. https://doi.org/10.1016/S0092-8674(02)00867-X
Naithani S, Hou JM, Chitnis PR (2000) Targeted inactivation of the psaK1, psaK2 and psaM genes encoding subunits of Photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 63:225–236. https://doi.org/10.1023/A:1006463932538
Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565
Netzer-El SY, Caspy I, Nelson N (2019) Crystal structure of photosystem I monomer from Synechocystis PCC 6803. Front Plant Sci 9:1–7. https://doi.org/10.3389/fpls.2018.01865
Noridomi M, Nakamura S, Tsuyama M et al (2017) Opposite domination of cyclic and pseudocyclic electron flows in short-illuminated dark-adapted leaves of angiosperms and gymnosperms. Photosynth Res 134:149–164. https://doi.org/10.1007/s11120-017-0419-2
Pinto F, Pacheco CC, Ferreira D et al (2012) Selection of suitable reference genes for RT-qPCR analyses in cyanobacteria. PLoS ONE 7:1–9. https://doi.org/10.1371/journal.pone.0034983
Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701
Salomon E, Keren N (2011) Manganese limitation induces changes in the activity and in the organization of photosynthetic complexes in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol 155:571–579
Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261. https://doi.org/10.1016/j.bbabio.2004.11.006
Schreiber U, Klughammer C (2008) Non-photochemical fluorescence quenching and quantum yields in PS I and PS II: analysis of heat-induced limitations using Maxi-Imaging- PAM and Dual-PAM-100. PAM Appl Notes 1:15–18
Scott M, McCollum C, Vasil’ev S, Crozier C, Espie GS, Krol M et al (2006) Mechanism of the down regulation of photosynthesis by blue light in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 45(29):8952–8958
Sejima T, Takagi D, Fukayama H et al (2014) Repetitive short-pulse light mainly inactivates photosystem i in sunflower leaves. Plant Cell Physiol 55:1184–1193. https://doi.org/10.1093/pcp/pcu061
Shimakawa G, Miyake C (2018) Oxidation of P700 ensures robust photosynthesis. Front Plant Sci 9:1617
Shimakawa G, Shaku K, Miyake C (2016) Oxidation of P700 in photosystem I is essential for the growth of cyanobacteria. Plant Physiol 172(3):1443–1450. https://doi.org/10.1104/pp.16.01227
Shirao M, Kuroki S, Kaneko K et al (2013) Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol 54:1152–1163
Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142(1):56–64. https://doi.org/10.1111/j.1399-3054.2010.01437.x
Sonoike K, Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194(2):287–293. https://doi.org/10.1007/BF00196400
Suorsa M, Järvi S, Grieco M et al (2012) Proton gradient regulation 5 is essential for proper acclimation of arabidopsis photosystem i to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948. https://doi.org/10.1105/tpc.112.097162
Takagi D, Ishizaki K, Hanawa H et al (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 161:56–74
Tsiotis G, Haase W, Engel A, Michel H (1995) Isolation and structural characterization of trimeric cyanobacterial photosystem I Complex with the help of recombinant antibody fragments. Eur J Biochem 231:823–830. https://doi.org/10.1111/j.1432-1033.1995.0823d.x
Vassiliev IR, Yu J, Jung YS et al (1999) The cysteine-proximal aspartates in the F(x)-binding niche of photosystem. I: effect of alanine and lysine replacements on photoautotrophic growth, electron transfer rates, single-turnover flash efficiency, and EPR spectral properties. J Biol Chem 274:9993–10001. https://doi.org/10.1074/jbc.274.15.9993
Vinyard DJ, Ananyev GM, Charles Dismukes G (2013) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 82:577–606
Wang Q, Jantaro S, Lu B et al (2008) The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol 147:1239–1250
Webber AN, Lubitz W (2001) P700: the primary electron donor of photosystem I. Biochim Biophys Acta 1507:61–79. https://doi.org/10.1016/S0005-2728(01)00198-0
Xu Q, Hoppe D, Chitnis VP et al (1995) Mutational analysis of photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803: targeted inactivation of psaI reveals the function of PsaI in the structural organization of PsaL. J Biol Chem 270:16243–16250
Yan J, Kurisu G, Cramer WA (2006) Intraprotein transfer of the quinone analogue inhibitor 2, 5-dibromo-3-methyl-6-isopropyl-p-benzoquinone in the cytochrome b6f complex. Proc Natl Acad Sci 103:69–74
Yeremenko N, Jeanjean R, Prommeenate P et al (2005) Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 46:1433–1436. https://doi.org/10.1093/pcp/pci147
Zhang P, Allahverdiyeva Y, Eisenhut M, Aro E-M (2009) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS ONE 4:e5331. https://doi.org/10.1371/journal.pone.0005331
Acknowledgements
This work was partially supported by a grant to KK from the Polish National Science Centre (2017/01/X/NZ3/00411) and by the Leading National Research Center Program (KNOW) implemented by the Ministry of Science and Higher Education of the Republic of Poland (35p/8/2017).
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Kłodawska, K., Kovács, L., Vladkova, R. et al. Trimeric organization of photosystem I is required to maintain the balanced photosynthetic electron flow in cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 143, 251–262 (2020). https://doi.org/10.1007/s11120-019-00696-9
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DOI: https://doi.org/10.1007/s11120-019-00696-9