Photosynthetica 2018, 56(1):210-216 | DOI: 10.1007/s11099-017-0758-4

Quantification of bound bicarbonate in photosystem II

K. Tikhonov1, D. Shevela2,*, V. V. Klimov1, J. Messinger2,3
1 Institute of Basic Biological Problems, Russian Academy of Science, Pushchino, Russia
2 Department of Chemistry, Chemical Biological Centre, Umeå University, Umeå, Sweden
3 Department of Chemistry, Molecular Biomimetics, Ångström Laboratory, Uppsala University, Uppsala, Sweden

In this study, we presented a new approach for quantification of bicarbonate (HCO3-) molecules bound to PSII. Our method, which is based on a combination of membrane-inlet mass spectrometry (MIMS) and 18O-labelling, excludes the possibility of "non-accounted" HCO3- by avoiding (1) the employment of formate for removal of HCO3- from PSII, and (2) the extremely low concentrations of HCO3-/CO2 during online MIMS measurements. By equilibration of PSII sample to ambient CO2 concentration of dissolved CO2/HCO3-, the method ensures that all physiological binding sites are saturated before analysis. With this approach, we determined that in spinach PSII membrane fragments 1.1 ± 0.1 HCO3- are bound per PSII reaction center, while none was bound to isolated PsbO protein. Our present results confirmed that PSII binds one HCO3- molecule as ligand to the non-heme iron of PSII, while unbound HCO3- optimizes the water-splitting reactions by acting as a mobile proton shuttle.

Additional key words: hydrogen carbonate; inorganic carbon; mass spectrometry; Mn-stabilizing protein; non-heme iron; oxygen-evolving complex

Received: June 2, 2017; Accepted: August 21, 2017; Published: March 1, 2018  Show citation

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Tikhonov, K., Shevela, D., Klimov, V.V., & Messinger, J. (2018). Quantification of bound bicarbonate in photosystem II. Photosynthetica, 56(SPECIAL ISSUE), 210-216. doi: 10.1007/s11099-017-0758-4
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    References

    1. Ago H., Adachi H., Umena Y. et al.: Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga.-J. Biol. Chem. 291: 5676-5687, 2016. Go to original source...
    2. Ananyev G., Nguyen T., Putnam-Evans C., Dismukes G.C.: Mutagenesis of CP43-arginine-357 to serine reveals new evidence for (bi)carbonate functioning in the water oxidizing complex of photosystem II.-Photochem. Photobiol. Sci. 4: 991-998, 2005. Go to original source...
    3. Aoyama C., Suzuki H., Sugiura M., Noguchi T.: Flash-induced FTIR difference spectroscopy shows no evidence for the structural coupling of bicarbonate to the oxygen-evolving Mn cluster in photosystem II.-Biochemistry 47: 2760-2765, 2008. Go to original source...
    4. Baranov S.V., Tyryshkin A.M., Katz D. et al.: Bicarbonate is a native cofactor for assembly of the manganese cluster of the photosynthetic water oxidizing complex. Kinetics of reconstitution of O2 evolution by photoactivation.-Biochemistry 43: 2070-2079, 2004. Go to original source...
    5. Berthold D.A., Babcock G.T., Yocum C.F.: A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes.-FEBS Lett. 134: 231-234, 1981. Go to original source...
    6. Blubaugh D.J., Govindjee: The molecular mechanism of the bicarbonate effect at the plastoquinone reductase site of photosynthesis.-In: {ieGovindjee (ed.): Molecular Biology of Photosynthesis. Pp. 441-484. Springer, Dordrecht 1988. Go to original source...
    7. Brinkert K., De Causmaecker S., Krieger-Liszkay A. et al.: Bicarbonate-induced redox tuning in photosystem II for regulation and protection.-P. Natl. Acad. Sci. USA 113: 12144-12149, 2016. Go to original source...
    8. Dasgupta J., Tyryshkin A.M., Dismukes G.C.: ESEEM spectroscopy reveals carbonate and an N-donor protein-ligand binding to Mn2+ in the photoassembly reaction of the Mn4Ca cluster in photosystem II.-Angew. Chem. Int. Ed. 46: 8028-8031, 2007. Go to original source...
    9. Diamond W.D., Akinfiev N.N.: Solubility of CO2 in water from-1.5 to 100°C and from 0.1 to 100 MPa: evaluation of literature data and thermodynamic modelling.-Fluid Phase Equilibr. 208: 265-290, 2003. Go to original source...
    10. Enami I., Kamino K., Shen J.-R. et al.: Isolation and characterization of photosystem II complexes which lack lightharvesting chlorophyll a/b proteins but retain three extrinsic proteins related to oxygen evolution from spinach.-BBABioenergetics 977: 33-39, 1989. Go to original source...
    11. Ford R.C., Evans M.C.W.: Isolation of a photosystem 2 preparation from higher plants with highly enriched oxygen evolution activity.-FEBS Lett. 160: 159-164, 1983. Go to original source...
    12. Govindjee, Weger H.G., Turpin D.H. et al.: Formate releases carbon dioxide/bicarbonate from thylakoid membranes - measurements by mass spectroscopy and infrared gas analyzer.-Naturwissenschaften 78: 168-170, 1991. Go to original source...
    13. Govindjee, Xu C., van Rensen J.J.S.: On the requirement of bound bicarbonate for photosystem II activity.-Z. Naturforsch. 52: 24-32, 1997. Go to original source...
    14. Guskov A., Gabdulkhakov A., Broser M. et al.: Recent progress in the crystallographic studies of photosystem II.-ChemPhysChem 11: 1160-1171, 2010. Go to original source...
    15. Klimov V.V., Allakhverdiev S.I., Feyziev Y.M., Baranov S.V.: Bicarbonate requirement for the donor side of photosystem II.-FEBS Lett. 363: 251-255, 1995. Go to original source...
    16. Klimov V.V., Allakhverdiev S.I., Nishiyama Y. et al.: Stabilization of the oxygen-evolving complex of photosystem II by bicarbonate and glycinebetaine in thylakoid and subthylakoid preparations.-Funct. Plant Biol. 30: 797-803, 2003. Go to original source...
    17. Klimov V.V., Baranov S.V.: Bicarbonate requirement for the water-oxidizing complex of photosystem II.-BBABioenergetics 1503: 187-196, 2001. Go to original source...
    18. Klimov V.V., Baranov S.V., Allakhverdiev S.I.: Bicarbonate protects the donor side of photosystem II against photoinhibition and thermoinactivation.-FEBS Lett. 418: 243-246, 1997. Go to original source...
    19. Koroidov S., Shevela D., Shutova T. et al.: Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation.-P. Natl. Acad. Sci. USA 111: 6299-6304, 2014. Go to original source...
    20. Kozlov Y.N., Tikhonov K.G., Zastrizhnaya O.M., Klimov V.V.: pH dependence of the composition and stability of MnIIIbicarbonate complexes and its implication for redox interaction of MnII with photosystem II.-J. Photoch. Photobio. B 101: 362-366, 2010. Go to original source...
    21. McConnell I.L., Eaton-Rye J.J., van Rensen J.J.S.: Regulation of photosystem II electron transport by bicarbonate.-In: Eaton-Rye J.J., Tripathy B.C., Sharkey T.D. (ed.): Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation. Pp. 475-500. Springer, Dordrecht 2012. Go to original source...
    22. Messinger J., Badger M.R., Wydrzynski T.: Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II.-P. Natl. Acad. Sci. USA 92: 3209-3213, 1995. Go to original source...
    23. Müh F., Glöckner C., Hellmich J., Zouni A.: Light-induced quinone reduction in photosystem II.-Biochim. Biophys. Acta 1817: 44-65, 2012. Go to original source...
    24. Pobeguts O.V., Smolova T.N., Timoshevsky D.S., Klimov V.V.: Interaction of bicarbonate with the manganese-stabilizing protein of photosystem II.-J. Photoch. Photobio. B 100: 30-37, 2010. Go to original source...
    25. Pobeguts O.V., Smolova T.N., Zastrizhnaya O.M., Klimov V.V.: Protective effect of bicarbonate against extraction of the extrinsic proteins of the water-oxidizing complex from photosystem II membrane fragments.-Biochim. Biophys. Acta 1767: 624-632, 2007. Go to original source...
    26. Rappaport F., Diner B.A.: Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in Photosystem II.-Coord. Chem. Rev. 252: 259-272, 2008. Go to original source...
    27. Shen J.-R., Katoh S.: Inactivation and calcium-dependent reactivation of oxygen evolution in photosystem II preparations treated at pH 3.0 or with high concentrations of NaCl.-Plant Cell Physiol. 32: 439-446, 1991. Go to original source...
    28. Shen J.-R.: The structure of photosystem II and the mechanism of water oxidation in photosynthesis.-Annu. Rev. Plant Biol. 66: 23-48, 2015. Go to original source...
    29. Shevela D., Eaton-Rye J.J., Shen J.-R., Govindjee.: Photosystem II and the unique role of bicarbonate: A historical perspective.-Biochim. Biophys. Acta 1817: 1134-1151, 2012. Go to original source...
    30. Shevela D., Messinger J.: Studying the oxidation of water to molecular oxygen in photosynthetic and artificial systems by time-resolved membrane-inlet mass spectrometry.-Front. Plant Sci. 4: 473, 2013. Go to original source...
    31. Shevela D., Nöring B., Koroidov S. et al.: Efficiency of photosynthetic water oxidation at ambient and depleted levels of inorganic carbon.-Photosynth. Res. 117: 401-412, 2013. Go to original source...
    32. Shevela D., Su J.H., Klimov V., Messinger J.: Hydrogencarbonate is not a tightly bound constituent of the wateroxidizing complex in photosystem II.-Biochim. Biophys. Acta 1777: 532-539, 2008. Go to original source...
    33. Shutova T., Kenneweg H., Buchta J. et al.: The photosystem IIassociated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal.-EMBO J. 27: 782-791, 2008. Go to original source...
    34. Stemler A., Babcock G.T., Govindjee.: Effect of bicarbonate on photosynthetic oxygen evolution in flashing light in chloroplast fragments.-P. Natl. Acad. Sci. USA 71: 4679-4683, 1974. Go to original source...
    35. Stemler A., Govindjee.: Bicarbonate ion as a critical factor in photosynthetic oxygen evolution.-Plant Physiol. 52: 119-123, 1973. Go to original source...
    36. Stemler A.J.: The bicarbonate effect, oxygen evolution, and the shadow of Otto Warburg.-Photosynth. Res. 73: 177-183, 2002. Go to original source...
    37. Ulas G., Olack G., Brudvig G.W.: Evidence against bicarbonate bound in the O2-evolving complex of photosystem II.-Biochemistry 47: 3073-3075, 2008. Go to original source...
    38. Umena Y., Kawakami K., Shen J.-R., Kamiya N.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.-Nature 473: 55-60, 2011. Go to original source...
    39. van Rensen J.J.S.: Role of bicarbonate at the acceptor side of photosystem II.-Photosynth. Res. 73: 185-192, 2002. Go to original source...
    40. van Rensen J.J.S., Klimov V.V.: Bicarbonate interactions.-In: Wydrzynski T., Satoh K. (ed.): Photosystem II. The Light-Driven Water:Plastoquinone Oxidoreductase. Pp. 329-346. Springer, Dordrecht 2005.
    41. van Rensen J.J.S., Xu C., Govindjee.: Role of bicarbonate in photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis.-Physiol. Plantarum 105: 585-592, 1999. Go to original source...
    42. Villarejo A., Shutova T., Moskvin O. et al: A photosystem IIassociated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution.-EMBO J. 21: 1930-1938, 2002. Go to original source...
    43. Vinyard D.J., Ananyev G.M., Dismukes G.C.: Photosystem II: The reaction center of oxygenic photosynthesis.-Annu. Rev. Biochem. 82: 577-606, 2013. Go to original source...
    44. Wei X., Su X., Cao P. et al.: Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution.-Nature 534: 69-74, 2016. Go to original source...
    45. Wydrzynski T., Govindjee.: New site of bicarbonate effect in photosystem II of photosynthesis-Evidence from chlorophyll fluorescence transients in spinach-chloroplasts.-Biochim. Biophys. Acta 387: 403-408, 1975. Go to original source...

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