Abstract
The structure and functional organization of the photosystem I (PSI) reaction center (RC) donor side has a significant similarity to the reaction centers of purple bacteria (bRCs), despite the fact that they belong to different types of RCs. Moreover, the redox potential values of their primary electron donors are identical (~0.5 V). In our earlier reports [Khorobrykh et al. (2008) Phylos. Trans. R. Soc. B., 363, 1245-1251; Terentyev et al. (2011) Biochemistry (Moscow., 76, 1360-1366; Khorobrykh et al. (2018) ChemBioChem, 14, 1725-1731], we have demonstrated redox interaction of low-potential Mn2+-bicarbonate complexes with bRCs, which might have been one of the first steps in the evolutionary origin of Mn-cluster of the photosystem II water-oxidizing complex that occurred in the Archean (over 3 billion years ago). In this study, we investigated redox interactions between Mn2+-bicarbonate complexes and PSI. Such interactions were almost absent in the original PSI preparations and emerged only in preoxidized PSI preparations containing ~50% oxidized RCs. The interaction between Mn2+-bicarbonate complexes and PSI required increased Mn2+ concentrations, while its dependence on the HCO3– concentration indicated involvement of electroneutral low-potential [Mn(HCO3)2] complex in the process. Analysis of the PSI crystal structure revealed steric hindrances on the RC donor side, which could block the redox interaction between Mn2+-bicarbonate complexes and oxidized primary electron donor. Comparison of structures of RCs from the PSI and ancient RCs from heliobacteria belonging to the same type of RCs suggested that such hindrances should be absent in the primitive PSI in the Archean and allowed to explain their evolutionary origin as a consequence of PSI RCs into the united electron transport chain (ETC) of the photosynthetic membrane that was accompanied by the evolutionary loss of PSI capacity for the redox interaction with Mn2+-bicarbonate complexes.
Similar content being viewed by others
Abbreviations
- bChl:
-
bacteriochlorophyll
- bRC:
-
bacterial reaction center
- Chl:
-
chlorophyll
- DCPIP:
-
reduced 2,6-dichlorophenolindophenol
- ETC:
-
electron transport chain
- hbRC:
-
heliobacterial reaction center
- Pc:
-
plastocyanin
- PSI:
-
photosystem I
- PSII:
-
photosystem II
- RC:
-
reaction center
REFERENCES
Nelson, N., and Yocum, C. F. (2006) Structure and function of photosystems I and II, Annu. Rev. Plant Biol., 57, 521-565, doi: 10.1146/annurev.arplant.57.032905.105350.
Nelson, N. (2013) Evolution of photosystem I and the control of global enthalpy in an oxidizing world, Photosynth. Res., 116, 145-151, doi: 10.1007/s11120-013-9902-6.
Caffarri, S., Tibiletti, T., Jennings, R., and Santabarbara, S. (2014) A comparison between plant photosystem I and photosystem II architecture and functioning, Curr. Protein Pept. Sci., 15, 296-331, doi: 10.2174/1389203715666140327102218.
Blankenship, R. E. (2010) Early evolution of photosynthesis, Plant Physiol., 154, 434-438, doi: 10.1104/pp.110.161687.
Allen, J. P., and Williams, J. C. (1998) Photosynthetic reaction centers, FEBS Lett., 438, 5-9, doi: 10.1016/S0014-5793(98)01245-9.
Hohmann-Marriott, M. F., and Blankenship, R. E. (2011) Evolution of photosynthesis, Annu. Rev. Plant Biol., 62, 515-548, doi: 10.1146/annurev-arplant-042110-103811.
Heathcote, P., Jones, M. R., and Fyfe, P. K. (2003) Type I photosynthetic reaction centres: structure and function, Philos. Trans. R. Soc. London. Ser. B Biol. Sci., 358, 231-243, doi: 10.1098/rstb.2002.1178.
Blankenship, R. E. (1992) Origin and early evolution of photosynthesis, Photosynth. Res., 33, 91-111, doi: 10.1007/BF00039173.
Lin, X., Murchison, H. A., Nagarajan, V., Parson, W. W., Allen, J. P., and Williams, J. C. (1994) Specific alteration of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides, Proc. Natl. Acad. Sci. USA, 91, 10265-10269, doi: 10.1073/pnas.91.22.10265.
Brettel, K., and Leibl, W. (2001) Electron transfer in photosystem I, Biochim. Biophys. Acta, 1507, 100-114, doi: 10.1016/S0005-2728(01)00202-X.
Semenov, A. Y., Kurashov, V. N., and Mamedov, M. D. (2011) Transmembrane charge transfer in photosynthetic reaction centers: some similarities and distinctions, J. Photochem. Photobiol. B Biol., 104, 326-332, doi: 10.1016/j.jphotobiol.2011.02.004.
Rappaport, F., Guergova-Kuras, M., Nixon, P. J., Diner, B. A., and Lavergne, J. (2002) Kinetics and pathways of charge recombination in photosystem II, Biochemistry, 41, 8518-8527, doi: 10.1021/bi025725p.
Allakhverdiev, S. I., Tomo, T., Shimada, Y., Kindo, H., Nagao, R., Klimov, V. V., and Mimuro, M. (2010) Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls, Proc. Natl. Acad. Sci. USA, 107, 3924-3929, doi: 10.1073/pnas.0913460107.
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, doi: 10.1038/nature09913.
Dismukes, G. C., Klimov, V. V., Baranov, S. V., Kozlov, Y. N., DasGupta, J., and Tyryshkin, A. (2001) The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis, Proc. Natl. Acad. Sci. USA, 98, 2170-2175, doi: 10.1073/pnas.061514798.
Khorobrykh, A. A., Terentyev, V. V., Zharmukhamedov, S. K., and Klimov, V. V. (2008) Redox interaction of Mn-bicarbonate complexes with reaction centres of purple bacteria, Philos. Trans. R. Soc. B Biol. Sci., 363, 1245-1251, doi: 10.1098/rstb.2007.2221.
Terentyev, V. V., Shkuropatov, A. Y., Shkuropatova, V. A., Shuvalov, V. A., and Klimov, V. V. (2011) Investigation of the redox interaction between Mn-bicarbonate complexes and reaction centers from Rhodobacter sphaeroides R-26, Chromatium minutissimum, and Chloroflexus aurantiacus, Biochemistry (Moscow), 76, 1360-1366, doi: 10.1134/S0006297911120091.
Khorobrykh, A., Dasgupta, J., Kolling, D. R. J., Terentyev, V., Klimov, V. V., and Dismukes, G. C. (2013) Evolutionary origins of the photosynthetic water oxidation cluster: bicarbonate permits Mn2+ photo-oxidation by anoxygenic bacterial reaction centers, Chembiochem, 14, 1725-1731, doi: 10.1002/cbic.201300355.
Terentyev, V. V., Khorobrykh, A. A., and Klimov, V. V. (2015) Photooxidation of Mn-bicarbonate complexes by reaction centers of purple bacteria as a possible stage in the evolutionary origin of the water-oxidizing complex of photosystem II, in: Photosynthesis: New Approaches to the Molecular, Cellular, and Organismal Levels (Allakhverdiev, S. I., ed.) Scrivener Publishing LLC, pp. 85-132, doi: https://doi.org/10.1002/9781119084150.ch2.
Kozlov, Y. N., and Kazakova, A. A. (1997) Changes in the redox potential and catalase activity of Mn2+ ions during formation of Mn-bicarbonate complexes, Membr. Cell Biol., 11, 115-120.
Kozlov, Y. N., Zharmukhamedov, S. K., Tikhonov, K. G., Dasgupta, J., Kazakova, A. A., Dismukes, G. C., and Klimov, V. V. (2004) Oxidation potentials and electron donation to photosystem II of manganese complexes containing bicarbonate and carboxylate ligands, Phys. Chem. Chem. Phys., 6, 4905-4911, doi: 10.1039/b406569g.
Dasgupta, J., Tyryshkin, A. M., Kozlov, Y. N., Klimov, V. V., and Dismukes, G. C. (2006) Carbonate complexation of Mn2+ in the aqueous phase: redox behavior and ligand binding modes by electrochemistry and EPR spectroscopy, J. Phys. Chem. B, 110, 5099-5111, doi: 10.1021/jp055213v.
Tikhonov, K. G., Zastrizhnaya, O. M., Kozlov, Y. N., and Klimov, V. V. (2006) Composition and catalase-like activity of Mn(II)-bicarbonate complexes, Biochemistry (Moscow), 71, 1270-1277, doi: 10.1134/S0006297906110137.
Ford, R. C., and Evans, M. C. W. (1983) Isolation of a photosystem II preparation from higher plants with highly enriched oxygen evolution activity, FEBS Lett., 160, 159-164, doi: 10.1016/0014-5793(83)80957-0.
Porra, R. J., Thompson, W. A., and Kriedemann, P. E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy, Biochim. Biophys. Acta, 975, 384-394, doi: 10.1016/S0005-2728(89)80347-0.
Terentyev, V. V., Shukshina, A. K., and Shitov, A. V. (2019) Carbonic anhydrase CAH3 supports the activity of photosystem II under increased pH, Biochim. Biophys. Acta, 1860, 582-590, doi: 10.1016/j.bbabio.2019.06.003.
Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics, J. Mol. Graph., 14, 33-38, doi: 10.1016/0263-7855(96)00018-5.
Amunts, A., Toporik, H., Borovikova, A., and Nelson, N. (2010) Structure determination and improved model of plant photosystem I, J. Biol. Chem., 285, 3478-3486, doi: 10.1074/jbc.M109.072645.
Melis, A. (1989) Spectroscopic methods in photosynthesis: photosystem stoichiometry and chlorophyll antenna size, Philos. Trans. R. Soc. B Biol. Sci., 323, 397-409, doi: 10.1098/rstb.1989.0019.
Hu, Q., Miyashita, H., Iwasaki, I., Kurano, N., Miyachi, S., Iwaki, M., and Itoh, S. (1998) A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis, Proc. Natl. Acad. Sci. USA, 95, 13319-13323, doi: 10.1073/pnas.95.22.13319.
Shuvalov, V. A. (1976) The study of the primary photoprocesses in photosystem I of chloroplasts recombination luminescence, chlorophyll triplet state and triplet–triplet annihilation, Biochim. Biophys. Acta, 430, 113-121, doi: 10.1016/0005-2728(76)90227-9.
Kozlov, Y. N., Tikhonov, K. G., Zastrizhnaya, O. M., and Klimov, V. V. (2010) pH-Dependence of the composition and stability of MnIII-bicarbonate complexes and its implication for redox interaction of MnII with photosystemII, J. Photochem. Photobiol. B Biol., 101, 362-366, doi: 10.1016/j.jphotobiol.2010.08.009.
Yang, X., Zhang, Y. H., Yang, Z. L., Chen, L. J., He, J. L., and Wang, R. F. (2009) pH dependence of photosynthetic behavior of plant photosystem I particles, Russ. J. Plant Physiol., 56, 599-606, doi: 10.1134/S1021443709050033.
Petrova, A., Mamedov, M., Ivanov, B., Semenov, A., and Kozuleva, M. (2018) Effect of artificial redox mediators on the photoinduced oxygen reduction by photosystem I complexes, Photosynth. Res., 137, 421-429, doi: 10.1007/s11120-018-0514-z.
Semenov, A., Cherepanov, D., and Mamedov, M. (2008) Electrogenic reactions and dielectric properties of photosystem II, Photosynth. Res., 98, 121-130, doi: 10.1007/s11120-008-9377-z.
Sommer, F., Drepper, F., Haehnel, W., and Hippler, M. (2004) The hydrophobic recognition site formed by residues PsaA-Trp 651 and PsaB-Trp 627 of photosystem I in chlamydomonas reinhardtii confers distinct selectivity for binding of blastocyanin and cytochrome c6, J. Biol. Chem., 279, 20009-20017, doi: 10.1074/jbc. M313986200.
Busch, A., and Hippler, M. (2011) The structure and function of eukaryotic photosystem I, Biochim. Biophys. Acta, 1807, 864-877, doi: 10.1016/j.bbabio.2010.09.009.
Hippler, M., Drepper, F., Farah, J., and Rochaix, J.-D. (1997) Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF, Biochemistry, 36, 6343-6349, doi: 10.1021/bi970082c.
Gisriel, C., Sarrou, I., Ferlez, B., Golbeck, J. H., Redding, K. E., and Fromme, R. (2017) Structure of a symmetric photosynthetic reaction center–photosystem, Science, 357, 1021-1025, doi: 10.1126/science.aan5611.
Nunn, J. F. (1998) Evolution of the atmosphere, Proc. Geol. Assoc., 109, 1-13, doi: 10.1016/S0016-7878(98)80001-1.
Royer, D. L. (2006) CO2-forced climate thresholds during the Phanerozoic, Geochim. Cosmochim. Acta, 70, 5665-5675, doi: 10.1016/j.gca.2005.11.031.
Johnson, J. E., Webb, S. M., Thomas, K., Ono, S., Kirschvink, J. L., and Fischer, W. W. (2013) Manganese-oxidizing photosynthesis before the rise of cyanobacteria, Proc. Natl. Acad. Sci. USA, 110, 11238-11243, doi: 10.1073/pnas.1305530110.
Okita, P. M., Maynard, J. B., Spiker, E. C., and Force, E. R. (1988) Isotopic evidence for organic matter oxidation by manganese reduction in the formation of stratiform manganese carbonate ore, Geochim. Cosmochim. Acta, 52, 2679-2685, doi: 10.1016/0016-7037(88)90036-1.
Kozuleva, M. A., and Ivanov, B. N. (2016) The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain, Plant Cell Physiol., 57, 1397-1404, doi: 10.1093/pcp/pcw035.
Orf, G. S., Gisriel, C., and Redding, K. E. (2018) Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center, Photosynth. Res., 138, 11-37, doi: 10.1007/s11120-018-0503-2.
Funding
The work was performed within the framework of the State task AAAA-A17-117030110136-8.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This study contains no experiments with humans or animals performed by any of the authors. The authors declare no conflict of interests.
Additional information
In memory of Yuri Nikolaevich Kozlov
Rights and permissions
About this article
Cite this article
Terentyev, V., Zharmukhamedov, S. Evolutionary Loss of the Ability of the Photosystem I Primary Electron Donor for the Redox Interaction with Mn-Bicarbonate Complexes. Biochemistry Moscow 85, 697–708 (2020). https://doi.org/10.1134/S0006297920060073
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297920060073