Skip to main content
SpringerLink
Log in

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

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

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 (E m’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 E m 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 Q −A 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 E m’s of Pheo and QA by altering nearby hydrogen bond networks to modify the structures of the binding pockets of these cofactors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

DFT:

Density functional theory

E m :

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

References

  • 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 107:3924–3929

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 108:8054–8058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 16:11864–11876

    Article  CAS  PubMed  Google Scholar 

  • Berthomieu C, Hienerwadel R (2009) Fourier transform infrared (FTIR) spectroscopy. Photosynth Res 101:157–170

    Article  CAS  PubMed  Google Scholar 

  • 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 269:363–367

    Article  CAS  PubMed  Google Scholar 

  • Björn L, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynth Res 99:85–98

    Article  PubMed  Google Scholar 

  • Breton J (2001) Fourier transform infrared spectroscopy of primary electron donors in type I photosynthetic reaction centers. Biochim Biophys Acta 1507:180–193

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431

    Article  CAS  PubMed  Google Scholar 

  • 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 4:1060–1064

    Article  CAS  PubMed  Google Scholar 

  • Chu H-A (2013) Fourier transform infrared difference spectroscopy for studying the molecular mechanism of photosynthetic water oxidation. Front Plant Sci 4:146

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 90:9973–9977

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 98:131–140

    Article  CAS  PubMed  Google Scholar 

  • 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 6:4825–4831

    Article  CAS  Google Scholar 

  • Debus RJ (2008) Protein ligation of the photosynthetic oxygen-evolving center. Coord Chem Rev 252:244–258

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 1847:19–34

    Article  CAS  PubMed  Google Scholar 

  • Faller P, Maly T, Rutherford AW, MacMillan F (2001) Chlorophyll and carotenoid radicals in photosystem II studied by pulsed ENDOR. Biochemistry 40:320–326

    Article  CAS  PubMed  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara M, Tasumi M (1986) Metal-sensitive bands in the Raman and infrared-spectra of intact and metal-substituted chlorophyll a. J Phys Chem 90:5646–5650

    Article  CAS  Google Scholar 

  • 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 1708:209–218

    Article  CAS  PubMed  Google Scholar 

  • 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 16:334–342

    Article  CAS  PubMed  Google Scholar 

  • 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 35:15447–15460

    Article  CAS  PubMed  Google Scholar 

  • 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 567–608

    Chapter  Google Scholar 

  • 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 95:13319–13323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ishikita H, Hasegawa K, Noguchi T (2011) How does the QB site influence propagate to the QA site in photosystem II? Biochemistry 50:5436–5442

    Article  CAS  PubMed  Google Scholar 

  • 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 46:12473–12481

    Article  CAS  PubMed  Google Scholar 

  • Iwai M, Katoh H, Katayama M, Ikeuchi M (2004) Improved genetic transformation of the thermophilic cyanobacterium, Thermosynechococcus elongatus BP-1. Plant Cell Physiol 45:171–175

    Article  CAS  PubMed  Google Scholar 

  • 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 51:554–560

    Article  CAS  PubMed  Google Scholar 

  • 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 106:17365–17370

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 1817:1083–1094

    Article  CAS  PubMed  Google Scholar 

  • 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 249:227–230

    CAS  Google Scholar 

  • 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 1777:74–83

    Article  PubMed  Google Scholar 

  • 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 37:17339–17344

    Article  CAS  PubMed  Google Scholar 

  • Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564

    Article  CAS  PubMed  Google Scholar 

  • Loughlin P, Lin Y, Chen M (2013) Chlorophyll d and Acaryochloris marina: current status. Photosynth Res 116:277–293

    Article  CAS  PubMed  Google Scholar 

  • Mäntele W (1993) Reaction-induced infrared difference spectroscopy for the study of protein function and reaction-mechanisms. Trends Biochem Sci 18:197–202

    Article  PubMed  Google Scholar 

  • McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483

    Article  CAS  PubMed  Google Scholar 

  • 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 37:17439–17447

    Article  CAS  PubMed  Google Scholar 

  • 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 1827:255–265

    Article  CAS  PubMed  Google Scholar 

  • 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 1767:327–334

    Article  CAS  PubMed  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402

    Article  CAS  Google Scholar 

  • 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 1016:49–54

    Article  CAS  Google Scholar 

  • Noguchi T (2007) Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution. Photosynth Res 91:59–69

    Article  CAS  PubMed  Google Scholar 

  • Noguchi T (2008) Fourier transform infrared analysis of the photosynthetic oxygen-evolving center. Coord Chem Rev 252:336–346

    Article  CAS  Google Scholar 

  • Noguchi T (2013) Monitoring the reactions of photosynthetic water oxidation using infrared spectroscopy. Biomed Spectrosc Imaging 2:115–128

    CAS  Google Scholar 

  • 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 1847:35–45

    Article  CAS  PubMed  Google Scholar 

  • 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 367–387

    Chapter  Google Scholar 

  • 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 370:241–244

    Article  CAS  PubMed  Google Scholar 

  • 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 38:399–403

    Article  CAS  PubMed  Google Scholar 

  • 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 38:4846–4852

    Article  CAS  PubMed  Google Scholar 

  • Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41:8518–8527

    Article  CAS  PubMed  Google Scholar 

  • 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 103:9790–9800

    Article  CAS  Google Scholar 

  • 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 44:11178–11187

    Article  CAS  PubMed  Google Scholar 

  • Renger G (2007) Oxidative photosynthetic water splitting: energetics, kinetics and mechanism. Photosynth Res 92:407–425

    Article  CAS  PubMed  Google Scholar 

  • 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 112:7351–7354

    Article  CAS  PubMed  Google Scholar 

  • Saito K, Shen JR, Ishikita H (2012) Cationic state distribution over the chlorophyll d-containing PD1/PD2 Pair in photosystem II. Biochim Biophys Acta 1817:1191–1195

    Article  CAS  PubMed  Google Scholar 

  • 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 9:869–878

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 1767:589–595

    Article  CAS  PubMed  Google Scholar 

  • 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 8:3460–3466

    Article  CAS  PubMed  Google Scholar 

  • 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 49:493–501

    Article  CAS  PubMed  Google Scholar 

  • Sivakumar V, Wang RL, Hastings G (2003) Photo-oxidation of P740, the primary electron donor in photosystem I from Acaryochloris marina. Biophys J 85:3162–3172

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 1837:139–148

    Article  CAS  PubMed  Google Scholar 

  • 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 49:5445–5454

    Article  CAS  PubMed  Google Scholar 

  • 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 98:159–167

    Article  CAS  PubMed  Google Scholar 

  • 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 104:7283–7288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 104:333–340

    Article  CAS  PubMed  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60

    Article  CAS  PubMed  Google Scholar 

  • Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14:200–205

    Article  CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Division of Material Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602, Japan

    Yuko Sano & Takumi Noguchi

  2. Faculty of Science, Tokyo University of Science, Tokyo, 162-8601, Japan

    Kaichiro Endo & Tatsuya Tomo

  3. PRESTO, Japan Science and Technology Agency (JST), Saitama, 332-0012, Japan

    Tatsuya Tomo

Authors
  1. Yuko Sano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaichiro Endo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatsuya Tomo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takumi Noguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takumi Noguchi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 188 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sano, Y., Endo, K., Tomo, T. et al. Modified molecular interactions of the pheophytin and plastoquinone electron acceptors in photosystem II of chlorophyll d-containing Acaryochloris marina as revealed by FTIR spectroscopy. Photosynth Res 125, 105–114 (2015). https://doi.org/10.1007/s11120-014-0073-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-014-0073-x

Keywords

Search

Navigation