Photosynthesis Research

, Volume 125, Issue 1–2, pp 105–114 | Cite as

Modified molecular interactions of the pheophytin and plastoquinone electron acceptors in photosystem II of chlorophyll d-containing Acaryochloris marina as revealed by FTIR spectroscopy

  • Yuko Sano
  • Kaichiro Endo
  • Tatsuya Tomo
  • Takumi Noguchi
Regular Paper

Abstract

Acaryochloris marina is a unique cyanobacterium that contains chlorophyll (Chl) d as a major pigment. Because Chl d has smaller excitation energy than Chl a used in ordinary photosynthetic organisms, the energetics of the photosystems of A. marina have been the subject of interest. It was previously shown that the redox potentials (Em’s) of the redox-active pheophytin a (Pheo) and the primary plastoquinone electron acceptor (QA) in photosystem II (PSII) of A. marina are higher than those in Chl a-containing PSII, to compensate for the smaller excitation energy of Chl d (Allakhverdiev et al., Proc Natl Acad Sci USA 107: 3924–3929, 2010; ibid. 108: 8054–8058, 2011). To clarify the mechanisms of these Em increases, in this study, we have investigated the molecular interactions of Pheo and QA in PSII core complexes from A. marina using Fourier transform infrared (FTIR) spectroscopy. Light-induced FTIR difference spectra upon single reduction of Pheo and QA showed that spectral features in the regions of the keto and ester C=O stretches and the chlorin ring vibrations of Pheo and in the CO/CC stretching region of the QA semiquinone anion in A. marina are significantly different from those of the corresponding spectra in Chl a-containing cyanobacteria. These observations indicate that the molecular interactions, including the hydrogen bond interactions at the C=O groups, of these cofactors are modified in their binding sites of PSII proteins. From these results, along with the sequence information of the D1 and D2 proteins, it is suggested that A. marina tunes the Em’s of Pheo and QA by altering nearby hydrogen bond networks to modify the structures of the binding pockets of these cofactors.

Keywords

Chlorophyll d Pheophytin Plastoquinone Fourier transform infrared spectroscopy Vibrational spectroscopy Redox potential 

Abbreviations

Chl

Chlorophyll

DFT

Density functional theory

Em

Redox potential

FTIR

Fourier transform infrared

Mes

2-(N-morpholino)ethanesulfonic acid

P

Special pair Chls

P680

Special pair Chls in Chl a-containing PSII

Pheo

Redox-active pheophytin in PSII

PQ

Plastoquinone

PSII

Photosystem II

QA

Primary plastoquinone electron acceptor in PSII

QB

Secondary plastoquinone electron acceptor in PSII

Notes

Acknowledgments

The authors thank Dr. Yuichiro Shimada for preparation of the PSII core complexes from Synechocystis sp. PCC6803. This study was supported by the Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (24000018, 24107003, and 25291033 to TN, and 24370025, 26220801 to TT).

Supplementary material

11120_2014_73_MOESM1_ESM.pdf (189 kb)
Supplementary material 1 (PDF 188 kb)

References

  1. Allakhverdiev SI, Tomo T, Shimada Y, Kindo H, Nagao R, Klimov VV, 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 107:3924–3929PubMedCentralPubMedCrossRefGoogle Scholar
  2. Allakhverdiev SI, Tsuchiya T, Watabe K, Kojima A, Los DA, Tomo T, Klimov VV, Mimuro M (2011) Redox potentials of primary electron acceptor quinone molecule (QA) and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. Proc Natl Acad Sci USA 108:8054–8058PubMedCentralPubMedCrossRefGoogle Scholar
  3. Ashizawa R, Noguchi T (2014) Effects of hydrogen bonding interactions on the redox potential and molecular vibrations of plastoquinone as studied by density functional theory calculations. Phys Chem Chem Phys 16:11864–11876PubMedCrossRefGoogle Scholar
  4. Berthomieu C, Hienerwadel R (2009) Fourier transform infrared (FTIR) spectroscopy. Photosynth Res 101:157–170PubMedCrossRefGoogle Scholar
  5. Berthomieu C, Nabedryk E, Mäntele W, Breton J (1990) Characterization by FTIR spectroscopy of the photoreduction of the primary quinone acceptor QA in photosystem II. FEBS Lett 269:363–367PubMedCrossRefGoogle Scholar
  6. Björn L, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynth Res 99:85–98PubMedCrossRefGoogle Scholar
  7. Breton J (2001) Fourier transform infrared spectroscopy of primary electron donors in type I photosynthetic reaction centers. Biochim Biophys Acta 1507:180–193PubMedCrossRefGoogle Scholar
  8. Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431PubMedCrossRefGoogle Scholar
  9. Chen M, Telfer A, Lin S, Pascal A, Larkum AWD, Barber J, Blankenship RE (2005) The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. Photochem Photobiol Sci 4:1060–1064PubMedCrossRefGoogle Scholar
  10. Chu H-A (2013) Fourier transform infrared difference spectroscopy for studying the molecular mechanism of photosynthetic water oxidation. Front Plant Sci 4:146PubMedCentralPubMedCrossRefGoogle Scholar
  11. Clarke AK, Soitamo A, Gustafsson P, Oquist G (1993) Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90:9973–9977PubMedCentralPubMedCrossRefGoogle Scholar
  12. Cser K, Deák Z, Telfer A, Barber J, Vass I (2008) Energetics of Photosystem II charge recombination in Acaryochloris marina studied by thermoluminescence and flash-induced chlorophyll fluorescence measurements. Photosynth Res 98:131–140PubMedCrossRefGoogle Scholar
  13. Cuni A, Xiong L, Sayre R, Rappaport F, Lavergne J (2004) Modification of the pheophytin midpoint potential in photosystem II: modulation of the quantum yield of charge separation and of charge recombination pathways. Phys Chem Chem Phys 6:4825–4831CrossRefGoogle Scholar
  14. Debus RJ (2008) Protein ligation of the photosynthetic oxygen-evolving center. Coord Chem Rev 252:244–258PubMedCentralPubMedCrossRefGoogle Scholar
  15. Debus RJ (2015) FTIR studies of metal ligands, networks of hydrogen bonds, and water molecules near the active site Mn4CaO5 cluster in photosystem II. Biochim Biophys Acta 1847:19–34PubMedCrossRefGoogle Scholar
  16. Faller P, Maly T, Rutherford AW, MacMillan F (2001) Chlorophyll and carotenoid radicals in photosystem II studied by pulsed ENDOR. Biochemistry 40:320–326PubMedCrossRefGoogle Scholar
  17. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  18. Fujiwara M, Tasumi M (1986) Metal-sensitive bands in the Raman and infrared-spectra of intact and metal-substituted chlorophyll a. J Phys Chem 90:5646–5650CrossRefGoogle Scholar
  19. Grabolle M, Dau H (2005) Energetics of primary and secondary electron transfer in Photosystem II membrane particles of spinach revisited on basis of recombination-fluorescence measurements. Biochim Biophys Acta 1708:209–218PubMedCrossRefGoogle Scholar
  20. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342PubMedCrossRefGoogle Scholar
  21. Hienerwadel R, Boussac A, Breton J, Berthomieu C (1996) Fourier transform infrared difference study of TyrosineD oxidation and plastoquinone QA reduction in photosystem II. Biochemistry 35:15447–15460PubMedCrossRefGoogle Scholar
  22. Hillier W, Messinger J (2005) Mechanism of photosynthetic oxygen production. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Springer, Dordrecht, pp 567–608CrossRefGoogle Scholar
  23. Hu Q, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M, Itoh S (1998) A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad Sci USA 95:13319–13323PubMedCentralPubMedCrossRefGoogle Scholar
  24. Ishikita H, Hasegawa K, Noguchi T (2011) How does the QB site influence propagate to the QA site in photosystem II? Biochemistry 50:5436–5442PubMedCrossRefGoogle Scholar
  25. Itoh S, Mino H, Itoh K, Shigenaga T, Uzumaki T, Iwaki M (2007) Function of chlorophyll d in reaction centers of photosystems I and II of the oxygenic photosynthesis of Acaryochloris marina. Biochemistry 46:12473–12481PubMedCrossRefGoogle Scholar
  26. Iwai M, Katoh H, Katayama M, Ikeuchi M (2004) Improved genetic transformation of the thermophilic cyanobacterium, Thermosynechococcus elongatus BP-1. Plant Cell Physiol 45:171–175PubMedCrossRefGoogle Scholar
  27. Iwai M, Suzuki T, Kamiyama A, Sakurai I, Dohmae N, Inoue Y, Ikeuchi M (2010) The PsbK subunit is required for the stable assembly and stability of other small subunits in the PSII complex in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Plant Cell Physiol 51:554–560PubMedCrossRefGoogle Scholar
  28. Kato Y, Sugiura M, Oda A, Watanabe T (2009) Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in photosystem II. Proc Natl Acad Sci USA 106:17365–17370PubMedCentralPubMedCrossRefGoogle Scholar
  29. Kiss E, Kós PB, Chen M, Vass I (2012) A unique regulation of the expression of the psbA, psbD, and psbE genes, encoding the D1, D2 and cytochrome b559 subunits of the photosystem II complex in the chlorophyll d containing cyanobacterium Acaryochloris marina. Biochim Biophys Acta 1817:1083–1094PubMedCrossRefGoogle Scholar
  30. Klimov VV, Allakhverdiev SI, Demeter S, Krasnovskii AA (1979) Photoreduction of pheophytin in the photosystem 2 of chloroplasts with respect to the redox potential of the medium. Dokl Akad Nauk SSSR 249:227–230Google Scholar
  31. Kós PB, Deák Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777:74–83PubMedCrossRefGoogle Scholar
  32. Krieger-Liszkay A, Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II. Relevance to photodamage and phytotoxicity. Biochemistry 37:17339–17344PubMedCrossRefGoogle Scholar
  33. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564PubMedCrossRefGoogle Scholar
  34. Loughlin P, Lin Y, Chen M (2013) Chlorophyll d and Acaryochloris marina: current status. Photosynth Res 116:277–293PubMedCrossRefGoogle Scholar
  35. Mäntele W (1993) Reaction-induced infrared difference spectroscopy for the study of protein function and reaction-mechanisms. Trends Biochem Sci 18:197–202PubMedCrossRefGoogle Scholar
  36. McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483PubMedCrossRefGoogle Scholar
  37. Merry SAP, Nixon PJ, Barter LMC, Schilstra M, Porter G, Barber J, Durrant JR, Klug DR (1998) Modulation of quantum yield of primary radical pair formation in photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry 37:17439–17447PubMedCrossRefGoogle Scholar
  38. Mielke SP, Kiang NY, Blankenship RE, Mauzerall D (2013) Photosystem trap energies and spectrally-dependent energy-storage efficiencies in the Chl d-utilizing cyanobacterium, Acaryochloris marina. Biochim Biophys Acta 1827:255–265PubMedCrossRefGoogle Scholar
  39. Mimuro M, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T (2007) Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta 1767:327–334PubMedCrossRefGoogle Scholar
  40. Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402CrossRefGoogle Scholar
  41. Nabedryk E, Andrianambinintsoa S, Berger G, Leonhard M, Mäntele W, Breton J (1990) Characterization of bonding interactions of the intermediary electron-acceptor in the reaction center of photosystem II by FTIR spectroscopy. Biochim Biophys Acta 1016:49–54CrossRefGoogle Scholar
  42. Noguchi T (2007) Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution. Photosynth Res 91:59–69PubMedCrossRefGoogle Scholar
  43. Noguchi T (2008) Fourier transform infrared analysis of the photosynthetic oxygen-evolving center. Coord Chem Rev 252:336–346CrossRefGoogle Scholar
  44. Noguchi T (2013) Monitoring the reactions of photosynthetic water oxidation using infrared spectroscopy. Biomed Spectrosc Imaging 2:115–128Google Scholar
  45. Noguchi T (2015) Fourier transform infrared difference and time-resolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation. Biochim Biophys Acta 1847:35–45PubMedCrossRefGoogle Scholar
  46. Noguchi T, Berthomieu C (2005) Molecular analysis by vibrational spectroscopy. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Springer, Dordrecht, pp 367–387CrossRefGoogle Scholar
  47. Noguchi T, Inoue Y (1995) Molecular interactions of the redox-active accessory chlorophyll on the electron-donor side of photosystem II as studied by Fourier transform infrared spectroscopy. FEBS Lett 370:241–244PubMedCrossRefGoogle Scholar
  48. Noguchi T, Inoue Y, Tang X-S (1999a) Hydrogen bonding interaction between the primary quinone acceptor QA and a histidine side chain in photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry 38:399–403PubMedCrossRefGoogle Scholar
  49. Noguchi T, Kurreck J, Inoue Y, Renger G (1999b) Comparative FTIR analysis of the microenvironment of QA in cyanide and high-pH treated and iron-depleted PS II membrane fragments. Biochemistry 38:4846–4852PubMedCrossRefGoogle Scholar
  50. Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41:8518–8527PubMedCrossRefGoogle Scholar
  51. Razeghifard MR, Kim S, Patzlaff JS, Hutchison RS, Krick T, Ayala I, Steenhuis JJ, Boesch SE, Wheeler RA, Barry BA (1999) In vivo, in vitro, and calculated vibrational spectra of plastoquinone and the plastosemiquinone anion radical. J Phys Chem B 103:9790–9800CrossRefGoogle Scholar
  52. Razeghifard MR, Chen M, Hughes JL, Freeman J, Krausz E, Wydrzynski T (2005) Spectroscopic studies of photosystem II in chlorophyll d-containing Acaryochloris marina. Biochemistry 44:11178–11187PubMedCrossRefGoogle Scholar
  53. Renger G (2007) Oxidative photosynthetic water splitting: energetics, kinetics and mechanism. Photosynth Res 92:407–425PubMedCrossRefGoogle Scholar
  54. Renger T, Schlodder E (2008) The primary electron donor of photosystem II of the cyanobacterium Acaryochloris marina is a chlorophyll d and the water oxidation is driven by a chlorophyll a/chlorophyll d heterodimer. J Phys Chem B 112:7351–7354PubMedCrossRefGoogle Scholar
  55. Saito K, Shen JR, Ishikita H (2012) Cationic state distribution over the chlorophyll d-containing PD1/PD2 Pair in photosystem II. Biochim Biophys Acta 1817:1191–1195PubMedCrossRefGoogle Scholar
  56. Salih GF, Jansson C (1997) Activation of the silent psbA1 gene in the cyanobacterium Synechocystis sp. strain 6803 produces a novel and functional D1 protein. Plant Cell 9:869–878PubMedCentralPubMedCrossRefGoogle Scholar
  57. Schlodder E, Çetin M, Eckert HJ, Schmitt FJ, Barber J, Telfer A (2007) Both chlorophylls a and d are essential for the photochemistry in photosystem II of the cyanobacteria, Acaryochloris marina. Biochim Biophys Acta 1767:589–595PubMedCrossRefGoogle Scholar
  58. Shevela D, Nöring B, Eckert HJ, Messinger J, Renger G (2006) 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 8:3460–3466PubMedCrossRefGoogle Scholar
  59. Shibuya Y, Takahashi R, Okubo T, Suzuki H, Sugiura M, Noguchi T (2010) Hydrogen bond interactions of the pheophytin electron acceptor and its radical anion in photosystem II as revealed by Fourier transform infrared difference spectroscopy. Biochemistry 49:493–501PubMedCrossRefGoogle Scholar
  60. Sivakumar V, Wang RL, Hastings G (2003) Photo-oxidation of P740, the primary electron donor in photosystem I from Acaryochloris marina. Biophys J 85:3162–3172PubMedCentralPubMedCrossRefGoogle Scholar
  61. Sugiura M, Azami C, Koyama K, Rutherford AW, Rappaport F, Boussac A (2014) Modification of the pheophytin redox potential in Thermosynechococcus elongatus Photosystem II with PsbA3 as D1. Biochim Biophys Acta 1837:139–148PubMedCrossRefGoogle Scholar
  62. Takahashi R, Hasegawa K, Takano A, Noguchi T (2010) The structures and binding sites of phenolic herbicides in the QB pocket of photosystem II. Biochemistry 49:5445–5454PubMedCrossRefGoogle Scholar
  63. Takano A, Takahashi R, Suzuki H, Noguchi T (2008) Herbicide effect on the hydrogen-bonding interaction of the primary quinone electron acceptor QA in photosystem II as studied by Fourier transform infrared spectroscopy. Photosynth Res 98:159–167PubMedCrossRefGoogle Scholar
  64. Tomo T, Okubo T, Akimoto S, Yokono M, Miyashita H, Tsuchiya T, Noguchi T, Mimuro M (2007) Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc Natl Acad Sci USA 104:7283–7288PubMedCentralPubMedCrossRefGoogle Scholar
  65. Tomo T, Allakhverdiev SI, Mimuro M (2011) Constitution and energetics of photosystem I and photosystem II in the chlorophyll d-dominated cyanobacterium Acaryochloris marina. J Photochem Photobiol B 104:333–340PubMedCrossRefGoogle Scholar
  66. Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60PubMedCrossRefGoogle Scholar
  67. Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14:200–205PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Yuko Sano
    • 1
  • Kaichiro Endo
    • 2
  • Tatsuya Tomo
    • 2
    • 3
  • Takumi Noguchi
    • 1
  1. 1.Division of Material Science, Graduate School of ScienceNagoya UniversityNagoyaJapan
  2. 2.Faculty of ScienceTokyo University of ScienceTokyoJapan
  3. 3.PRESTOJapan Science and Technology Agency (JST)SaitamaJapan

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