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Unique photosystems in Acaryochloris marina

Abstract

A short overview is given on the discovery of the chlorophyll d-dominated cyanobacterium Acaryochloris marina and the minor pigments that function as key components therein. In photosystem I, chlorophyll d′, chlorophyll a, and phylloquinone function as the primary electron donor, the primary electron acceptor and the secondary electron acceptor, respectively. In photosystem II, pheophytin a serves as the primary electron acceptor. The oxidation potential of chlorophyll d was higher than that of chlorophyll a in vitro, while the oxidation potential of P740 was almost the same as that of P700. These results help us to broaden our view on the questions about the unique photosystems in Acaryochloris marina.

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Abbreviations

BChl:

Bacteriochlorophyll

Chl:

Chlorophyll

HPLC:

High performance liquid chromatography

PBP:

Phycobiliproteins

P680:

The primary electron donor of photosystem II

P700:

The primary electron donor of Chl a-type photosystem I

P740:

The primary electron donor of photosystem I in A. marina

Phe:

Pheophytin

PS:

Photosystem

RC:

Reaction center

References

  • Akimoto S, Murakami A, Yokono M, Koyama K, Tsuchiya T, Miyashita H, Yamazaki I, Mimuro M (2006) Fluorescence properties of the chlorophyll d-dominated cyanobacterium Acaryochloris sp. strain Awaji. J Photochem Photobiol A 178:122–129. doi:10.1016/j.jphotochem.2005.09.031

    Article  CAS  Google Scholar 

  • Akiyama M, Miyashita H, Watanabe T, Kise K, Miyachi S, Kobayashi M (2001) Detection of chlorophyll d′ and pheophytin a in a chlorophyll d-dominating oxygenic photosynthetic prokaryote Acaryochloris marina. Anal Sci 17:205–208. doi:10.2116/analsci.17.205

    PubMed  Article  CAS  Google Scholar 

  • Akiyama M, Miyashita H, Kise H, Watanabe T, Mimuro M, Miyachi S, Kobayashi M (2002) Quest for minor but key chlorophyll molecules in photosynthetic reaction centers—unusual pigment composition in the reaction centers of a chlorophyll d-dominated cyanobacterium Acaryochloris marina. Photosynth Res 74:97–107. doi:10.1023/A:1020915506409

    PubMed  Article  CAS  Google Scholar 

  • Akiyama M, Gotoh T, Kise H, Miyashita H, Mimuro M, Kobayashi M (2004) Stoichiometries of chlorophyll d′/PSI and chlorophyll a/PSII in a chlorophyll d-dominated cyanobacterium Acaryochloris marina. Jpn J Phycol (Supplement for the Proceedings of Algae 2002) 52:67–72

    Google Scholar 

  • Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proc Natl Acad Sci USA 84:5730–5734. doi:10.1073/pnas.84.16.5730

    PubMed  Article  CAS  Google Scholar 

  • Benjamin B, Finazzi G, Benson S, Barber J, Rappaport F, Telfer A (2007) Study of intersystem electron transfer in the chlorophyll d containing cyanobacterium Acaryochloris marina and a reappraisal of the redox properties of P740. Photosynth Res 91:155

    Google Scholar 

  • Boichenko VA, Klimov VV, Miyashita H, Miyachi S (2000) Functional characteristics of chlorophyll d-predominating photosynthetic apparatus in intact cells of Acaryochloris marina. Photosynth Res 65:269–277. doi:10.1023/A:1010637631417

    PubMed  Article  CAS  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. doi:10.1039/b507057k

    PubMed  Article  CAS  Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1984) X-ray structure analysis of a membrane protein complex. Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180:385–398. doi:10.1016/S0022-2836(84)80011-X

    PubMed  Article  CAS  Google Scholar 

  • Diner BA, Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53:551–580. doi:10.1146/annurev.arplant.53.100301.135238

    PubMed  Article  CAS  Google Scholar 

  • Groot ML, Pawlowicz NP, van Wilderen LJGW, Breton J, van Stokkum IHM, van Grondelle R (2005) Initial electron donor and acceptor in isolated photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc Natl Acad Sci USA 102:13087–13092. doi:10.1073/pnas.0503483102

    PubMed  Article  CAS  Google Scholar 

  • Hastings G, Wang R (2008) Vibrational mode frequency calculations of chlorophyll-d for assessing (P740+-P740) FTIR difference spectra obtained using photosystem I particles from Acaryochloris marina. Photosynth Res 95:55–62. doi:10.1007/s11120-007-9228-3

    PubMed  Article  CAS  Google Scholar 

  • Holzwarth AR, Müller MG, Reus M, Nowaczyk M, Sander J, Rögner M (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc Natl Acad Sci USA 103:6895–6900. doi:10.1073/pnas.0505371103

    PubMed  Article  CAS  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. doi:10.1073/pnas.95.22.13319

    PubMed  Article  CAS  Google Scholar 

  • Itoh S, Iwaki M, Noguti T, Kawamori A, Mino H, Hu Q, Iwasaki I, Miyashita H, Kurano N, Miyachi S, Shen R (2001) Photosystem I and II reaction centers of a new oxygenic organism Acaryochloris marina that use chlorophyll d. In: PS2001 Proceedings of the 12th international congress on photosynthesis, CSIRO, Melbourne, Australia, pp S6–S028

  • 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. doi:10.1021/bi7008085

    PubMed  Article  CAS  Google Scholar 

  • Itoh S, Uzumaki T, Takaichi S, Iwaki M, Kumazaki S, Itoh K, Mino H (2008) Unidirectional electron transfer in chlorophyll d-containing photosystem I reaction center complex of Acaryochloris marina. In: Allen J, Gantt E, Golbeck J, Osmond B (eds) Energy from the sun. Springer, pp 93–96

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917. doi:10.1038/35082000

    PubMed  Article  CAS  Google Scholar 

  • Kato Y, Nakamura A, Suzawa T, Watanabe T (2008) Unexpected difference in the P700 redox potential among oxygenic photosynthetic organisms revealed by spectroelectrochemistry. In: Allen J, Gantt E, Golbeck J, Osmond B (eds) Energy from the sun. Springer, pp 109–112

  • Ke B (2001) The primary electron donor of photosysten I-P700, Photosynthesis: photobiochemistry and photobiophysics. Kluwer Academic, Dordrecht, pp 463–478

    Google Scholar 

  • Kobayashi M, Watanabe T, Nakazato M, Ikegami I, Hiyama T, Matsunaga T, Murata N (1988) Chlorophyll a′/P700 and pheophytin a/P680 stoichiometries in higher plants and cyanobacteria bacteria determined by HPLC analysis. Biochim Biophys Acta 936:81–89. doi:10.1016/0005-2728(88)90254-X

    Article  CAS  Google Scholar 

  • Kobayashi M, van de Meent EJ, Amesz J, Ikegami I, Watanabe T (1991) Bacteriochlorophyll g epimer as a possible reaction center component of heliobacteria. Biochim Biophys Acta 1057:89–96. doi:10.1016/S0005-2728(05)80087-8

    Article  CAS  Google Scholar 

  • Kobayashi M, Watanabe S, Gotoh T, Koizumi H, Itoh Y, Akiyama M, Shiraiwa Y, Tsuchiya T, Miyashita H, Mimuro M, Yamashita T, Watanabe T (2005) Minor but key chlorophylls in photosystem II. Photosynth Res 84:201–207. doi:10.1007/s11120-005-0474-y

    PubMed  Article  CAS  Google Scholar 

  • Kobayashi M, Akiyama M, Kise H, Watanabe T (2006) Spectroscopy and structure determination. In: Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Springer, Dordrecht, pp 79–94

    Google Scholar 

  • Kobayashi M, Ohashi S, Iwamoto K, Shiraiwa Y, Kato Y, Watanabe T (2007) Redox potential of chlorophyll d in vitro. Biochim Biophys Acta 1767:596–602. doi:10.1016/j.bbabio.2007.02.015

    PubMed  Article  CAS  Google Scholar 

  • Kobayashi M, Ohashi S, Fukuyo S, Kasahara M, Watanabe T (2008) The oxidation potential of Chl a is the lowest—a new scheme for O2 evolution in PS II. In: Allen J, Gantt E, Golbeck J, Osmond B (eds) Energy from the sun. Springer, pp 113–116

  • Kumazaki S, Abiko K, Ikegami I, Iwaki M, Itoh S (2002) Energy equilibration and primary charge separation in chlorophyll d-based photosystem I reaction center isolated from Acaryochloris marina. FEBS Lett 530:153–157. doi:10.1016/S0014-5793(02)03446-4

    PubMed  Article  CAS  Google Scholar 

  • Mimuro M, Akimoto S, Yamazaki I, Miyashita H, Miyachi S (1999) Fluorescence properties of chlorophyll d-dominating prokaryotic alga, Acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1412:37–46. doi:10.1016/S0005-2728(99)00048-1

    PubMed  Article  CAS  Google Scholar 

  • Mimuro M, Hirayama K, Uezono K, Miyashita H, Miyachi S (2000) Uphill energy transfer in a chlorophyll d-dominating oxygenic photosynthetic prokaryote, Acaryochloris marina. Biochim Biophys Acta 1456:27–34. doi:10.1016/S0005-2728(99)00095-X

    PubMed  Article  CAS  Google Scholar 

  • Mimuro M, Akimoto S, Gotoh T, Yokono M, Akiyama M, Tsuchiya T, Miyashita H, Kobayashi M, Yamazaki I (2004) Identification of the primary electron donor in PS II of the Chl d-dominated cyanobacterium Acaryochloris marina. FEBS Lett 556:95–98. doi:10.1016/S0014-5793(03)01383-8

    PubMed  Article  CAS  Google Scholar 

  • Mino H, Kawamori A, Aoyama D, Tomo T, Iwaki M, Itoh S (2005) Proton ENDOR study of the primary donor P740+, a special pair of chlorophyll d in photosystem I reaction center of Acaryochloris marina. Chem Phys Lett 411:262–266. doi:10.1016/j.cplett.2005.06.033

    Article  CAS  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402. doi:10.1038/383402a0

    Article  CAS  Google Scholar 

  • Miyashita H, Adachi K, Kurano N, Ikemoto H, Chihara M, Miyachi S (1997) Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol 38:274–281

    CAS  Google Scholar 

  • Murakami A, Miyashita H, Iseki M, Adachi K, Mimuro M (2004) Chlorophyll d in an epiphytic cyanobacterium of red algae. Science 303:1633. doi:10.1126/science.1095459

    PubMed  Article  CAS  Google Scholar 

  • Nakamura A, Suzawa T, Kato Y, Watanabe T (2005) Significant species-dependence of P700 redox potential as verified by spectroelectrochemistry: comparison of spinach and Theromosynechococcus elongatus. FEBS Lett 579:2273–2276. doi:10.1016/j.febslet.2005.02.076

    PubMed  Article  CAS  Google Scholar 

  • Nieuwenburg P, Clarke RJ, Cai ZL, Chen M, Larkum AWD, Cabral NM, Ghiggino KP, Reimers JR (2003) Examination of the photophysical processes of chlorophyll d leading to a clarification of proposed uphill energy transfer processes in cells of Acaryochloris marina. Photochem Photobiol 77:628–637. doi :10.1562/0031-8655(2003)077<0628:EOTPPO>2.0.CO;2

    PubMed  Article  CAS  Google Scholar 

  • Ohashi S, Tsuchiya T, Iwamoto K, Miyashita H, Watanabe T, Shiraiwa Y, Mimuro M, Kobayashi M (2007) Succession of co-factors in photosystem I. Photosynth Res 91:270

    Google Scholar 

  • Ohashi S, Tsuchiya T, Iwamoto K, Miyashita H, Watanabe T, Shiraiwa Y, Mimuro M, Kobayashi M (2008a) Succession of co-factors in photosystem I. In: Allen J, Gantt E, Golbeck J, Osmond B (eds) Energy from the sun. Springer, pp 1177–1180

  • Ohashi S, Kasahara M, Fukuyo S, Nakazato M, Iwamoto K, Shiraiwa Y, Kato Y, Watanabe T, Kobayashi M (2008b) Redox potential of chlorophyll d. In: Allen J, Gantt E, Golbeck J, Osmond B (eds) Energy from the sun. Springer, pp 105–108

  • Ohkubo S, Miyashita H, Murakami A, Takeyama H, Tsuchiya T, Mimuro M (2006) Molecular detection of epiphytic Acaryochloris spp. on marine macroalgae. Appl Environ Microbiol 72:7912–7915. doi:10.1128/AEM.01148-06

    PubMed  Article  CAS  Google Scholar 

  • Raszewski G, Saenger W, Renger T (2005) Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys J 88:986–998. doi:10.1529/biophysj.104.050294

    PubMed  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. doi:10.1021/bi048314c

    PubMed  Article  CAS  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. doi:10.1021/jp801900e

    PubMed  Article  CAS  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. doi:10.1016/j.bbabio.2007.02.018

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  • Swingley WD, Chen M, Cheung PC, Conrad AL, Dejesa LC, Hao J, Honchak BM, Karbach LE, Kurdoglu A, Lahiri S, Mastrian SD, Miyashita H, Page L, Ramakrishna P, Satoh S, Sattley WM, Shimada Y, Taylor HL, Tomo T, Tsuchiya T, Wang ZT, Raymond J, Mimuro M, Blankenship RE, Touchman JW (2008) Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proc Natl Acad Sci USA 105:2005–2010. doi:10.1073/pnas.0709772105

    PubMed  Article  CAS  Google Scholar 

  • Telfer A, Pascal A, Barber J, Schenderlein M, Schlodder E, Çetin M (2007) Electron transfer reactions in photosystem I and II of the chlorophyll d containing cyanobacterium, Acaryochloris marina. Photosynth Res 91:143

    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. doi:10.1073/pnas.0701847104

    PubMed  Article  CAS  Google Scholar 

  • Tomo T, Kato Y, Suzuki T, Akimoto S, Okubo T, Noguchi T, Hasegawa K, Tsuchiya T, Tanaka K, Fukuya M, Dohmae N, Watanabe T, Mimuro M (2008) Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. J Biol Chem 283:18198–18209. doi:10.1074/jbc.M801805200

    PubMed  Article  CAS  Google Scholar 

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Correspondence to Masami Kobayashi.

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Ohashi, S., Miyashita, H., Okada, N. et al. Unique photosystems in Acaryochloris marina . Photosynth Res 98, 141 (2008). https://doi.org/10.1007/s11120-008-9383-1

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  • DOI: https://doi.org/10.1007/s11120-008-9383-1

Keywords

  • Acaryochloris marina
  • Chlorophyll a
  • Chlorophyll d
  • Chlorophyll d′
  • Cyanobacteria
  • Pheophytin a