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State 1 and State 2 in Photosynthetic Apparatus of Red Microalgae and Cyanobacteria

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Abstract

Imbalanced light absorption by photosystem I (PSI) and photosystem II (PSII) in oxygenic phototrophs leads to changes in interaction of photosystems altering the linear electron flow. In plants and green algae, this imbalance is mitigated by a partial migration of the chlorophyll a/b containing light-harvesting antenna between the two photosystem core complexes. This migration is registered as fluorescence changes of the pigment apparatus and is termed the reverse transitions between States 1 and 2. By contrast, the molecular mechanism of State 1/2 transitions in phycobilisome (PBS)-containing photosynthetics, cyanobacteria and red algae, is still insufficiently understood. The suggested hypotheses – PBS movement along the surface of thylakoid membrane between PSI and PSII complexes, reversible PBS detachment from the dimeric PSII complex, and spillover – have some limitations as they do not fully explain the accumulated data. Here, we have recorded changes in the stationary fluorescence emission spectra of red algae and cyanobacteria in States 1/2 at room temperature, which allowed us to offer an explanation of the existing contradictions. The change of room temperature fluorescence of chlorophyll belonged to PSII was revealed, while the fluorescence of PBS associated with the PSII complexes remained during States 1/2 transitions at the stable level. Only the reversible dissociation of PBS from the monomeric PSI was revealed earlier which implied different degree of surface contact of PBS with the two photosystems. The detachment of PBS from the PSI corresponds to ferredoxin oxidation as electron carrier and the increase of cyclic electron transport in the pigment apparatus in State I.

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Abbreviations

PAM:

Pulse-Amplitude Modulated Fluorescence

PBS:

phycobilisome

PSI:

photosystem I

PSII:

photosystem II

References

  1. Mullineaux, C. W., and Emlyn-Jones, D. (2005) State transitions: an example of acclimation to low-light stress, J. Exp. Bot., 56, 389-393.

    Article  CAS  PubMed  Google Scholar 

  2. Calzadilla, P. I., and Kirilovsky, D. (2020) Revisiting cyanobacterial state transitions, Photochem. Photobiol. Sci., 19, 585-603.

    Article  CAS  PubMed  Google Scholar 

  3. Murata, N. (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluoresence in Porphyridium cruentum, Biochim. Biophys. Acta, 172, 242-251.

    Article  CAS  PubMed  Google Scholar 

  4. Bonaventura, C., and Myers, J. (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa, Biochim. Biophys. Acta, 189, 366-383.

    Article  CAS  PubMed  Google Scholar 

  5. Minagawa, J. (2011) State transitions – the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast, Biochim. Biophys. Acta, 1807, 897-905.

    Article  CAS  PubMed  Google Scholar 

  6. Lemeille, S., and Rochaix, J.-D. (2010) State transitions at the crossroad of thylakoid signalling pathways, Photosynth. Res., 106, 33-46.

    Article  CAS  PubMed  Google Scholar 

  7. Pesaresi, P., Pribil, M., Wunder, T., and Leister, D. (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38, Biochim. Biophys. Acta, 1078, 887-896.

    Article  CAS  Google Scholar 

  8. Kanervo, E., Suorsa, M., and Aro, E.-A. (2005) Functional flexibility and acclimation of the thylakoid membrane, Photochem. Photobiol. Sci., 4, 1072-1080.

    Article  CAS  PubMed  Google Scholar 

  9. Dumas, L., Zito, F., Blangy, S., Auroy, P., Johnson, X., et al. (2017) A stromal region of cytochrome b6f subunit IV is involved in the activation of the Stt7 kinase in Chlamydomonas, Proc. Natl. Acad. Sci. USA, 114, 12063-12068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ruban, A. V., and Johnson, M. P. (2009) Dynamics of the photosystems cross-section associated with the state transitions in higher plants, Photosyth. Res., 99, 173-183.

    Article  CAS  Google Scholar 

  11. Golbeck, J. H. (1994) In The Molecular Biology of Cyanobacteria (Bryant, D. A., ed.) Kluwer Academic Publishers, Dordrecht, pp. 320-354.

  12. Rakhimberdieva, M. G., Boichenko, V. A., Karapetyan, N. V., and Stadnichuk, I. N. (2001) Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis, Biochemistry, 40, 15780-15788.

    Article  CAS  PubMed  Google Scholar 

  13. Umena, Y., Kawakami, K., Shen, J. R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å, Nature, 473, 55-60.

    Article  CAS  PubMed  Google Scholar 

  14. Bald, D., Kruip, J., and Rögner, M. (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems?, Photosynth. Res., 49, 103-118.

    Article  CAS  PubMed  Google Scholar 

  15. Mullineaux, C. W., and Allen, J. F. (1990) State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystems I and II, Photosynth. Res., 23, 297-311.

    Article  CAS  PubMed  Google Scholar 

  16. Ogawa, T., Harada, T., Ozaki, H., and Sonoike, K. (2013) Disruption of the ndhF1 gene affects chlorophyll fluorescence through state transition in the cyanobacterium Synechocystis sp. PCC 6803, resulting in apparent high efficiency of photosynthesis, Plant Cell Physiol., 54, 1164-1171.

    Article  CAS  PubMed  Google Scholar 

  17. Federman, S., Malkin, S., and Scherz, A. (2000) Excitation energy transfer in aggregates of photosystem I and photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: can assembly of the pigment–protein complexes control the extent of spillover?, Photosynth. Res., 64, 199-207.

    Article  CAS  PubMed  Google Scholar 

  18. Mullineaux, C. W. (2008) Phycobilisome-reaction centre interaction in cyanobacteria, Photosynth. Res., 95, 175-182.

    Article  CAS  PubMed  Google Scholar 

  19. Li, H., Li, D., Yang, S., Xie, J., and Zhao, J. (2006) The state transition mechanism – simply depending on light-on and -off in Spirulina platensis, Biochim. Biophys. Acta, 1757, 1512-1519.

    Article  CAS  PubMed  Google Scholar 

  20. Dong, C., Tang, A., Zhao, J., Mullineaux, C. W., Shen, G., and Bryant, D. A. (2009) ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002, Biochim. Biophys. Acta, 1787, 1122-1128.

    Article  CAS  PubMed  Google Scholar 

  21. Zlenko, D. V., Elanskaya, I. V., Lukashev, E. P., Bolychevtseva, Y. V., Suzina, N. E., et al. (2019) Role of the PB-loop in ApcE and phycobilisome core function in cyanobacterium Synechocystis sp. PCC 6803, Biochim. Biophys. Acta, 1860, 155-166.

    Article  CAS  Google Scholar 

  22. McConnell, M. D., Koop, R., Vasil’ev, S., and 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  CAS  PubMed  PubMed Central  Google Scholar 

  23. Strašková, A., Steinbach, G., Konert, G., Kotabová, E., Komenda, J., et al. (2019) Pigment–protein complexes are organized into stable microdomains in cyanobacterial thylakoids, Biochim. Biophys. Acta, 1860, 1-15.

    Article  CAS  Google Scholar 

  24. Wollman, F. A. (1979) Ultrastructural comparison of Cyanidium caldarium wild type and III-C mutant lacking phycobilisomes, Plant Physiol., 63, 375-381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mörschel, E., and Schatz, G. H. (1987) Correlation of photosystem-II complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus, Planta, 1723, 145-154.

    Article  Google Scholar 

  26. Calzadilla, P. I., Zhan, J., Sétif, P., Lemaire, C., Solymosi, D., et al. (2019) The cytochrome b6f complex is not involved in cyanobacterial state transitions, Plant Cell, 31, 911-931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Liu, H., Zhang, H., Niedzwiedzki, D. M., Prado, M., He, G., et al. (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria, Science, 342, 1104-1107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mullineaux, C. W. (1992) Excitation energy transfer from phycobilisomes to Photosystem I in a cyanobacterium, Biochim. Biophys. Acta, 1100, 285-292.

    Article  CAS  Google Scholar 

  29. Stadnichuk, I. N., Bulychev, A. A., Lukashev, E. P., Sinetova, M. P., Khristin, M. S., et al. (2011) Far-red light-regulated efficient energy transfer from phycobilisomes to photosystem I in the red microalga Galdieria sulphuraria and photosystems-related heterogeneity of phycobilisome population, Biochim. Biophys. Acta, 1807, 227-235.

    Article  CAS  PubMed  Google Scholar 

  30. Chukhutsina, V., Bersanini, L., Aro, E. M., and Van Amerongen, H. (2015) Cyanobacterial light-harvesting phycobilisomes uncouple from photosystem I during dark-to-light transitions, Sci. Rep., 5, 1-10.

    Article  CAS  Google Scholar 

  31. Schreiber, U., Klughammer, C., and Neubauer, C. (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system, Z. Naturforsch., 43, 686-698.

    Article  CAS  Google Scholar 

  32. Rögner, M., Mühlenhoff, U., Boekema, E. J., and Witt, H. (1990) Mono-, di- and trimeric PSI reaction center complexes isolated from the thermophilic cyanobacterium Synechococcus sp.: size, shape and activity, Biochim. Biophys. Acta, 1015, 415-424.

    Article  Google Scholar 

  33. Stadnichuk, I. N., Rakhimberdieva, M. G., Boichenko, V. A., Bolychevtseva, Yu. V., Karapetyan, N. V., and Selyakh, I. O. (2000) Glucose-induced inhibition of the photosynthetic pigment apparatus in heterotrophically grown alga Galdieria, Russ. J. Plant Physiol. Engl. Transl., 47, 585-592.

    CAS  Google Scholar 

  34. Acuña, A. M., Snellenburg, J. J., Gwizdala, M., Kirilovsky, D., van Grondelle, R., and van Stokkum, I. H. M. (2016) Resolving the contribution of the uncoupled phycobilisomes to cyanobacterial pulse-amplitude modulated (PAM) fluorometry signals, Photosynth. Res., 127, 91-102.

    Article  PubMed  CAS  Google Scholar 

  35. Campbell, D., Hurry, V., Clarke, A. K., Gustafsson, P., and Öquist, G. (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation, Microbiol. Mol. Biol. Rev., 62, 667-683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Remelli, W., and Santabarbara, S. (2018) Excitation and emission wavelength dependence of fluorescence spectra in whole cells of the cyanobacterium Synechocystis sp. PPC6803: influence on the estimation of Photosystem II maximal quantum efficiency, Biochim. Biophys. Acta, 1859, 1207-1222.

    Article  CAS  Google Scholar 

  37. Shubin, V. V., Murthy, S. D. S., Karapetyan, N. V., and Mohanty, P. (1991) Origin of the 77 K variable fluorescence at 758 nm in the cyanobacterium Spirulina platensis, Biochim. Biophys. Acta, 1060, 28-36.

    Article  CAS  Google Scholar 

  38. Matthijs, H. C. P., Jeanjean, R., Yeremenko, N., Huisman, J., Joset, F., and Hellingwerf, K. J. (2002) Hypothesis: versatile function of ferredoxin-NADP+ reductase in cyanobacteria provides regulation for transient photosystem I-driven cyclic electron flow, Funct. Plant Biol., 29, 201-210.

    Article  CAS  PubMed  Google Scholar 

  39. Alcántara-Sánchez, F., Leyva-Castillo, L. E., Chagolla-López, A., de la Vara, L. G., and Gómez-Lojero, C. (2017) Distribution of isoforms of ferredoxin-NADP+ reductase (FNR) in cyanobacteria in two growth conditions, Intern. J. Biochem. Cell Biol., 85, 123-134.

    Article  CAS  Google Scholar 

  40. Tian, L., Liu, Z., Wang, F., Shen, L., Chen, J., et al. (2017) Isolation and characterization of PSI-LHCI super-complex and their sub-complexes from a red alga Cyanidioschyzon merolae, Photosynth. Res., 133, 201-214.

    Article  CAS  PubMed  Google Scholar 

  41. Glazer, A. N. (1989) The light guide. Directional energy transfer in a photosynthetic antenna, J. Biol. Chem., 264, 1-4.

    Article  CAS  PubMed  Google Scholar 

  42. El Bissati, K., Delphin, E., Murata, N., Etienn, A.-L., and Kirilovsky, D. (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms, Biochim. Biophys. Acta, 1457, 229-242.

    Article  CAS  PubMed  Google Scholar 

  43. Stadnichuk, I. N., Lukashev, E. P., and Elanskaya, I. V. (2009) Fluorescence changes accompanying short-term light adaptations in photosystem I and photosystem II of the cyanobacterium Synechocystis sp. PCC 6803 and phycobiliprotein-impaired mutants: state 1/state2 transitions and carotenoid-induced quenching of phycobilisomes, Photosynth. Res., 99, 227-241.

    Article  CAS  PubMed  Google Scholar 

  44. Zlenko, D. V., Krasilnikov, P. M., and Stadnichuk, I. N. (2016) Structural modeling of the phycobilisome core and its association with the photosystems, Photosynth. Res., 130, 347-356.

    Article  CAS  PubMed  Google Scholar 

  45. Krasilnikov, P. M., Zlenko, D. V., and Stadnichuk, I. N. (2020) Rates and pathways of energy migration from the phycobilisome to the photosystem II and to the orange carotenoid protein in cyanobacteria, FEBS Lett., 594, 1145-1154.

    Article  CAS  PubMed  Google Scholar 

  46. Zlenko, D. V., Galochkina, T. V., Krasilnikov, P. M., and Stadnichuk, I. N. (2017) Coupled rows of PBS cores and PSII dimers in cyanobacteria: symmetry and structure, Photosynth. Res., 133, 245-260.

    Article  CAS  PubMed  Google Scholar 

  47. Voloshina, O. V., Bolychevtseva, Y. V., Kuzminov, F. I., Gorbunov, M. Y., Elanskaya, I. V., and Fadeev, V. V. (2016) Photosystem II activity of wild type Synechocystis PCC 6803 and its mutants with different plastoquinone pool redox state, Biochemistry (Moscow), 81, 858-870.

    Article  CAS  Google Scholar 

  48. Karge, O., Bondar, A. N., and Dau, H. (2014) Cationic screening of charged surface groups (carboxylates) affects electron transfer steps in photosystem-II water oxidation and quinone reduction, Biochim. Biophys. Acta, 1837, 1625-1634.

    Article  CAS  PubMed  Google Scholar 

  49. Piven, I., Ajlani, G., and Sokolenko, A. (2005) Phycobilisome linker proteins are phosphorylated in Synechocystis sp. PCC 6803, J. Biol. Chem., 280, 21667-21672.

    Article  CAS  PubMed  Google Scholar 

  50. Nelson, N., and Junge, W. (2015) Structure and energy transfer in photosystems of oxygenic photosynthesis, Annu. Rev. Biochem., 84, 659-683.

    Article  CAS  PubMed  Google Scholar 

  51. Morsy, F. M., Nakajima, M., Yoshida, T., Fujiwara, T., Sakamoto, T., and Wada, K. (2008) Subcellular localization of ferredoxin-NADP+ oxidoreductase in phycobilisome retaining oxygenic photosysnthetic organisms, Photosynth. Res., 95, 73-85.

    Article  CAS  PubMed  Google Scholar 

  52. Vershubskii, A. V., Mishanin, V. I., and Tikhonov, A. N. (2014) Modeling of the Photosynthetic electron transport regulation in cyanobacteria, Biochemistry (Moscow) Suppl. Ser. A Membr. Cell Biol., 8, 262-278.

    Article  Google Scholar 

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Correspondence to Yulia V. Bolychevtseva or Igor N. Stadnichuk.

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Bolychevtseva, Y.V., Tropin, I.V. & Stadnichuk, I.N. State 1 and State 2 in Photosynthetic Apparatus of Red Microalgae and Cyanobacteria. Biochemistry Moscow 86, 1181–1191 (2021). https://doi.org/10.1134/S0006297921100023

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