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Covalently linked zinc chlorophyll dimers as a model of a chlorophyllous pair in photosynthetic reaction centers

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Abstract

A heterodimer, where zinc pyropheophorbide-a was linked with zinc pyropheophorbide-d through ethylene glycol diester, was prepared, as well as the corresponding homodimers. The synthetic dimers were complexed with methanol in benzene to give folded dimers by mutual Zn?O(Me)-H?O?C131 bonding. Such complexes had furthest red (Qy) absorption bands at longer wavelengths than the monomeric species. These red-shifts were ascribable to excitonic coupling of the Qy transition states in the chlorin π-π stacking conformer. In the heterodimeric system, a minor band was observed at the shorter wavelength side of the main Qy band. This observation can be explained by an additional contribution of Qy vibronic state to the exciton-coupled states. Based on the experimental results, a pair of chlorophyll(Chl)-d with Chl-a as well as a Chl-d homopair were proposed as dimers in reaction centers of Chl-d dominating cyanobacteria.

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References

  1. J. Deisenhofer, O. Epp, K. Miki, R. Huber and H., Michel, Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution Nature 1985 318 618–624

    Article  CAS  PubMed  Google Scholar 

  2. P. Jordan, P. Fromme, H. T. Witt, O. Klukas, W. Saenger, N. Krauß Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution Nature 2001 411 909–917

    Article  CAS  PubMed  Google Scholar 

  3. B. Loll, J. Kern, W. Saenger, A. Zouni and J., Biesiadka, Toward complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 2005 438 1040–1044

    Article  CAS  PubMed  Google Scholar 

  4. L. L. Shipman, T. M. Cotton, J. R. Norris and J. J., Katz, New proposal for structure of special-pair chlorophyll Proc. Natl. Acad. Sci. USA 1976 73 1791–1794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. R. J. Abraham and A. E. Rowan, Nuclear magnetic resonance spectroscopy of chlorophyll, in Chlorophylls, ed. H. Scheer, CRC Press, Boca Raton, FL, 1991, pp. 797-834

    Google Scholar 

  6. K. Uehara, Y. Hioki and M., Mimuro, The chlorophyll a aggregate absorbing near 688 nm is selectively formed in aqueous tetrahydrofuran Photochem. Photobiol. 1993 58 127–132

    Article  CAS  Google Scholar 

  7. T. Ochiai, T. Asaoka, T. Kato, S. Osaka, T. Dewa, K. Yamashita, H. Hashimoto and M., Nango, Molecular assembly of Zn porphyrin complexes onto a gold electrode using synthetic light-harvesting model polypeptides Tetrahedron Lett. 2007 48 8468–8471

    Article  CAS  Google Scholar 

  8. D. G. Johnson, W. A. Svec and M. R., Wasielewski, Solvent polarity dependent photophysics of a fixed-distance, symmetric chlorophyll dimer. A model of the special pair in photosynthetic reaction centers Isr. J. Chem. 1988 28 193–203

    Article  CAS  Google Scholar 

  9. L. Jaquinod, M. O. Senge, R. K. Pandey, T. P. Forsyth and K. M., Smith, Planar bischlorophyll derivatives with a completely conjugated π-system: model compounds for the special pair in photosynthesis Angew. Chem., Int. Ed. Engl. 1996 35 1840–1842

    Article  CAS  Google Scholar 

  10. G. Li, M. P. Dobhal, A. Graham, M. Shibata, G. Zheng, A. Kozyrev and R. K., Pandey, Thermolysis of vic-dihydroxybacteriochlorins: effect of the nature of substrates in directing the formation of chlorin-chlorin dimers with fixed and flexible orientations and their preliminary in vitro photosensitizing efficacy J. Org. Chem. 2003 68 3762–3772

    Article  CAS  PubMed  Google Scholar 

  11. G. Zheng, R. K. Pandey, T. P. Forsyth, A. N. Kozyrev, T. J. Dougherty and K. M., Smith, Synthesis and spectroscopic studies of some novel porphyrin-pyropheophorbide dimers and trimers with fixed distances Tetrahedron Lett. 1997 38 2409–2412

    Article  CAS  Google Scholar 

  12. R. F. Kelley, M. J. Tauber, T. M. Wilson and M. R., Wasielewski, Controlling energy and charge transfer in linear chlorophyll dimers Chem. Commun. 2007 4407–4409

    Google Scholar 

  13. A. N. Kozyrev, V. Suresh, S. Das, M. O. Senge, M. Shibata, T. J. Dougherty and R. K., Pandey, Syntheses and spectroscopic studies of novel chlorins with fused quinoxaline or benzimidazole ring systems and the related dimers with extended conjugation Tetrahedron 2000 56 3353–3364

    Article  CAS  Google Scholar 

  14. A. S. Brandis, A. N. Kozyrev and A. F., Mironov, Synthesis and study of chlorin and porphyrin dimers with ether linkage Tetrahedron 1992 48 6485–6494

    Article  CAS  Google Scholar 

  15. A. Osuka, S. Marumo, Y. Wada, I. Yamazaki, Y. Shirakawa and Y., Nishimura, Synthesis of 1,3-dioxane-bridged pyropheophorbide-diimide and pyropheophorbide dimer and their intramolecular electron and energy transfer Bull. Chem. Soc. Jpn. 1995 68 2909–2915

    Article  CAS  Google Scholar 

  16. G. Zheng, M. Aoudia, D. Lee, M. A. Rodgers, K. M. Smith, T. J. Dougherty and R. K., Pandey, Chlorin-based symmetrical and unsymmetrical dimers with amide linkage: effect of the substituents on photodynamic and photophysical properties J. Chem. Soc., Perkin Trans. 1 2000 3113–3121

    Google Scholar 

  17. A. Osuka, Y. Wada and S., Shinoda, Covalently linked pyropheophorbide dimers as models of the special pair in the photosynthetic reaction center Tetrahedron 1996 52 4311–4326

    Article  CAS  Google Scholar 

  18. M. R. Wasielewski, M. H. Studier and J. J., Katz, Covalently linked chlorophyll a dimer: A biomimetic model of special pair of chlorophyll Proc. Natl. Acad. Sci. USA 1976 73 4282–4286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. S. G. Boxer and G. L., Closs, A covalently bound dimeric derivative of pyrochlorophyllide a. A possible model for reaction center chlorophyll J. Am. Chem. Soc. 1976 98 5406–5408

    Article  CAS  Google Scholar 

  20. M. R. Wasielewski and W. A., Svec, Synthesis of covalently linked dimeric derivatives of chlorophyll a, pyrochlorophyll a, chlorophyll b, and bacteriochlorophyll a J. Org. Chem. 1980 45 1969–1974

    Article  CAS  Google Scholar 

  21. R. R. Bucks and S. G., Boxer, Synthesis and spectroscopic properties of a novel cofacial chlorophyll-based dimer J. Am. Chem. Soc. 1982 104 340–343

    Article  CAS  Google Scholar 

  22. M. R. Wasielewski, Energy and electron transfer in covalently linked chlorophyll-containing donor-acceptor molecules, in Chlorophylls, ed. H. Scheer, CRC Press, Boca Raton, FL, 1991, pp. 269-286

    Google Scholar 

  23. P. Hildebrandt, H. Tamiaki, A. R. Holzwarth and K., Schaffner, Resonance Raman spectroscopic study of metallochlorin aggregates. Implication for supramolecular structure in chlorosomal BChl c antennae of green bacteria J. Phys. Chem. 1994 98 2192–2197

    Article  CAS  Google Scholar 

  24. H. Tamiaki, M. Amakawa, Y. Shimono, R. Tanikaga, A. R. Holzwarth and K., Schaffner, Synthetic zinc and magnesium chlorin aggregates as models for supramolecular antenna complexes in chlorosomes of green photosynthetic bacteria Photochem. Photobiol. 1996 63 92–99

    Article  CAS  Google Scholar 

  25. H. Tamiaki, T. Miyatake, R. Tanikaga, A. R. Holzwarth and K., Schaffner, Self-assembly of an artificial light-harvesting antenna: energy transfer from a zinc chlorin to a bacteriochlorin in a supramolecular aggregate Angew. Chem., Int. Ed. Engl. 1996 35 772–774

    Article  CAS  Google Scholar 

  26. A. Osuka, Y. Wada, K. Maruyama and H., Tamiaki, Synthesis of a covalently linked bacteriopyropheophorbide-pyropheophorbide hybrid dimer Heterocycles 1997 44 165–168

    Article  CAS  Google Scholar 

  27. T. Miyatake, H. Tamiaki, A. R. Holzwarth and K., Schaffner, Artificial light-harvesting antennae: singlet excitation energy transfer from zinc chlorin aggregate to bacteriochlorin in homogeneous hexane solution Photochem. Photobiol. 1999 69 448–456

    Article  CAS  Google Scholar 

  28. N. Kosaka and H., Tamiaki, Synthesis of a novel cyclic chlorophyll hetero-dyad as a model compound for stacked chlorophylls found in photosynthetic systems Eur. J. Org. Chem. 2004 2325–2330

    Google Scholar 

  29. M. Helmreich, A. Hirsch and N., Jux, Synthesis of novel pyropheophorbide a-fullerene conjugates J. Porphyrins Phthalocyanines 2005 9 130–137

    Article  CAS  Google Scholar 

  30. Y. Saga and H., Tamiaki, Facile synthesis of chlorophyll analog possessing a disulfide bond and formation of self-assembled monolayer on gold surface J. Photochem. Photobiol., B 2004 73 29–34

    Article  CAS  Google Scholar 

  31. H. Tamiaki, S. Takeuchi, S. Tsudzuki, T. Miyatake and R., Tanikaga, Self-aggregation of synthetic zinc chlorins with a chiral 1-hydroxyethyl group as a model for in vivo epimeric bacteriochlorophyll-c and d aggregates Tetrahedron 1998 54 6699–6718

    Article  CAS  Google Scholar 

  32. R. Shibata and H., Tamiaki, Self-aggregation of synthetic zinc chlorophyll derivative possessing a perfluoroalkyl group in a fluorinated solvent Bioorg. Med. Chem. 2006 14 2235–2241

    Article  CAS  PubMed  Google Scholar 

  33. H. Tamiaki, S. Miyata, Y. Kureishi and R., Tanikaga, Aggregation of synthetic zinc chlorins with several esterified alkyl chains as models of bacteriochlorophyll-c homologs Tetrahedron 1996 52 12421–12432

    Article  CAS  Google Scholar 

  34. H. Tamiaki, S. Yagai and T., Miyatake, Synthetic zinc tetrapyrroles complexing with pyridine as a single axial ligand Bioorg. Med. Chem. 1998 6 2171–2178

    Article  CAS  PubMed  Google Scholar 

  35. J. K. Hoober, L. L. Eggink and M., Chen, Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts Photosynth. Res. 2007 94 387–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. A. Satake and Y., Kobuke, Artificial photosynthetic systems: assemblies of slipped cofacial porphyrins and phthalocyanines showing strong electron coupling Org. Biomol. Chem. 2007 5 1679–1691

    Article  CAS  PubMed  Google Scholar 

  37. P. Nieuwenburg, R. J. Clarke, Z.-L. Cai, M. Chen, A. W. D. Larkum, N. M. Cabral, K. P. Ghiggino and J. R., Reimers, 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. 2003 77 628–637

    Article  CAS  PubMed  Google Scholar 

  38. H. Tamiaki, R. Shibata and T., Mizoguchi, The 17-propionate function of (bacterio)chlorophylls: biological implication of their long esterifying chains in photosynthetic systems Photochem. Photobiol. 2007 83 152–162

    CAS  PubMed  Google Scholar 

  39. R. S. Gloag, R. J. Ritchie, M. Chen, A. W. D. Larkum and R. G., Quinnell, Chromatic photoacclimation, photosynthetic electron transport and oxygen evolution in the chlorophyll d-containing oxyphotobacterium Acaryochloris marina Biochim. Biophys. Acta 2007 1767 127–135

    Article  CAS  PubMed  Google Scholar 

  40. S. Itoh, H. Mino, K. Itoh, T. Shigenaga, T. Uzumaki and M., Iwaki, Function of chlorophyll d in reaction centers of photosystems I and II of the oxygenic photosynthesis of Acaryochloris marina Biochemistry 2007 46 12473–12481

    Article  CAS  PubMed  Google Scholar 

  41. T. Tomo, T. Okubo, S. Akimoto, M. Yokono, H. Miyashita, T. Tsutiya, T. Noguchi and M., Mimuro, Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium Proc. Natl. Acad. Sci. USA 2007 104 7283–7288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. E. Schlodder, M. Cetin, H.-J. Eckert, F.-J. Schmitt, J. Baber and A., Telfer, Both chlorophylls a and d are essential for the photochemistry Biochim. Biophys. Acta 2007 1767 589–595

    Article  CAS  PubMed  Google Scholar 

  43. M. Kobayashi, S. Ohashi, K. Iwamoto, Y. Shiraiwa, Y. Kato and T., Watanabe, Redox potential of chlorophyll d in vitro Biochim. Biophys. Acta 2007 1767 596–602

    Article  CAS  PubMed  Google Scholar 

  44. R. J. Cogdell, A. Gall, J. Köhler The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes Quarterly Rev. Biophys. 2006 39 227–324

    Article  CAS  Google Scholar 

  45. H. Tamiaki, T. Watanabe and T., Miyatake, Facile synthesis of 131-oxo-porphyrins possessing 3-vinyl or 3-formyl group, protochlorophyll-a/d derivatives by 17,18-dehydrogenation of chlorins J. Porphyrins Phthalocyanines 1999 3 45–52

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Bioscience and Biotechnology, Faculty of Science and Engineering, Ritsumeikan University, Kusatsu, Shiga, 525-8577, Japan

    Hitoshi Tamiaki, Kazuhiro Fukai, Hideki Shimazu, Katsunori Nishide & Michio Kunieda

  2. Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya, 464-8602, Japan

    Yutaka Shibata & Shigeru Itoh

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  1. Hitoshi Tamiaki
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  2. Kazuhiro Fukai
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  3. Hideki Shimazu
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  4. Katsunori Nishide
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  5. Yutaka Shibata
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Correspondence to Hitoshi Tamiaki.

Additional information

This paper was published as part of the themed issue of contributions from the 7th International Conference on Tetrapyrrole Photoreceptors in Photosynthetic Organisms held in Kyoto, December 2007.

Electronic supplementary information (ESI) available: 1H NMR and IR data of 1a with and without methanol. See DOI: 10.1039/b802353k

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Tamiaki, H., Fukai, K., Shimazu, H. et al. Covalently linked zinc chlorophyll dimers as a model of a chlorophyllous pair in photosynthetic reaction centers. Photochem Photobiol Sci 7, 1231–1237 (2008). https://doi.org/10.1039/b802353k

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