Redox Potential of Pheophytin a in Photosystem II of Two Cyanobacteria Having the Different Special Pair Chlorophylls

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2010 Feb 10

PMID 20142495

Citations 28

Authors

Suleyman I Allakhverdiev

Tatsuya Tomo

Yuichiro Shimada

Hayato Kindo

Ryo Nagao

Vyacheslav V Klimov

Mamoru Mimuro

Affiliations

Soon will be listed here.

Abstract

Water oxidation by photosystem (PS) II in oxygenic photosynthetic organisms is a major source of energy on the earth, leading to the production of a stable reductant. Mechanisms generating a high oxidation potential for water oxidation have been a major focus of photosynthesis research. This potential has not been estimated directly but has been measured by the redox potential of the primary electron acceptor, pheophytin (Phe) a. However, the reported values for Phe a are still controversial. Here, we measured the redox potential of Phe a under physiological conditions (pH 7.0; 25 degrees C) in two cyanobacteria with different special pair chlorophylls (Chls): Synechocystis sp. PCC 6803, whose special pair for PS II consists of Chl a, and Acaryochloris marina MBIC 11017, whose special pair for PS II consists of Chl d. We obtained redox potentials of -536 +/- 8 mV for Synechocystis sp. PCC 6803 and -478 +/- 24 mV for A. marina on PS II complexes in the presence of 1.0 M betaine. The difference in the redox potential of Phe a between the two species closely corresponded with the difference in the light energy absorbed by Chl a versus Chl d. We estimated the potentials of the special pair of PS II to be 1.20 V and 1.18 V for Synechocystis sp. PCC 6803 (P680) and A. marina (P713), respectively. This clearly indicates conservation in the properties of water-oxidation systems in oxygenic photosynthetic organisms, irrespective of the special-pair chlorophylls.

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References

Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y . Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 1996; 3(3):109-36. DOI: 10.1093/dnares/3.3.109. View

Kamiya N, Shen J . Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc Natl Acad Sci U S A. 2003; 100(1):98-103. PMC: 140893. DOI: 10.1073/pnas.0135651100. View

Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W . Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol. 2009; 16(3):334-42. DOI: 10.1038/nsmb.1559. View

Tomo T, Okubo T, Akimoto S, Yokono M, Miyashita H, Tsuchiya T . Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc Natl Acad Sci U S A. 2007; 104(17):7283-8. PMC: 1851883. DOI: 10.1073/pnas.0701847104. View

Shevela D, Noring B, Eckert H, Messinger J, Renger G . Characterization of the water oxidizing complex of photosystem II of the Chl d-containing cyanobacterium Acaryochloris marina via its reactivity towards endogenous electron donors and acceptors. Phys Chem Chem Phys. 2006; 8(29):3460-6. DOI: 10.1039/b604389e. View

Chen M, Telfer A, Lin S, Pascal A, Larkum A, Barber J . The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. Photochem Photobiol Sci. 2005; 4(12):1060-4. DOI: 10.1039/b507057k. View

Nanba O, Satoh K . Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci U S A. 1987; 84(1):109-12. PMC: 304151. DOI: 10.1073/pnas.84.1.109. View

Reddy A, Chaitanya K, Vivekanandan M . Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol. 2004; 161(11):1189-202. DOI: 10.1016/j.jplph.2004.01.013. View

Merry S, Nixon P, Barter L, Schilstra M, Porter G, Barber J . Modulation of quantum yield of primary radical pair formation in photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry. 1998; 37(50):17439-47. DOI: 10.1021/bi980502d. View

10.

Mimuro M, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T . Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta. 2007; 1767(4):327-34. DOI: 10.1016/j.bbabio.2007.02.012. View

11.

Shimada Y, Suzuki H, Tsuchiya T, Tomo T, Noguchi T, Mimuro M . Effect of a single-amino acid substitution of the 43 kDa chlorophyll protein on the oxygen-evolving reaction of the cyanobacterium Synechocystis sp. PCC 6803: analysis of the Glu354Gln mutation. Biochemistry. 2009; 48(26):6095-103. DOI: 10.1021/bi900317a. View

12.

Vasilev S, Bergmann A, Redlin H, Eichler H, Renger G . Erratum to 'on the role of exchangeable hydrogen bonds for the kinetics of P680 Q formation and P680 Pheo recombination in photosystem II' [Biochim. Biophys. Acta 1276 (1996) 35-44]. Biochim Biophys Acta. 2019; 1277(1-2):161. View

13.

Klimov V, Klevanik A, Shuvalov V, Kransnovsky A . Reduction of pheophytin in the primary light reaction of photosystem II. FEBS Lett. 1977; 82(2):183-6. DOI: 10.1016/0014-5793(77)80580-2. View

14.

Renger G, Renger T . Photosystem II: The machinery of photosynthetic water splitting. Photosynth Res. 2008; 98(1-3):53-80. DOI: 10.1007/s11120-008-9345-7. View

15.

Park E, Jeknic Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N . Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J. 2004; 40(4):474-87. DOI: 10.1111/j.1365-313X.2004.02237.x. View

16.

Ferreira K, Iverson T, Maghlaoui K, Barber J, Iwata S . Architecture of the photosynthetic oxygen-evolving center. Science. 2004; 303(5665):1831-8. DOI: 10.1126/science.1093087. View

17.

Shibamoto T, Kato Y, Sugiura M, Watanabe T . Redox potential of the primary plastoquinone electron acceptor Q(A) in photosystem II from Thermosynechococcus elongatus determined by spectroelectrochemistry. Biochemistry. 2009; 48(45):10682-4. DOI: 10.1021/bi901691j. View

18.

Groot M, Pawlowicz N, van Wilderen L, Breton J, van Stokkum I, van Grondelle R . Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc Natl Acad Sci U S A. 2005; 102(37):13087-92. PMC: 1196200. DOI: 10.1073/pnas.0503483102. View

19.

Allakhverdiev S, Hayashi H, Nishiyama Y, Ivanov A, Aliev J, Klimov V . Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol. 2003; 160(1):41-9. DOI: 10.1078/0176-1617-00845. View

20.

Swingley W, Chen M, Cheung P, Conrad A, Dejesa L, Hao J . Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proc Natl Acad Sci U S A. 2008; 105(6):2005-10. PMC: 2538872. DOI: 10.1073/pnas.0709772105. View