Skip to main content
SpringerLink
Log in

Stereochemical determination of chlorophyll-d molecule from Acaryochloris marina and its modification to a self-aggregative chlorophyll as a model of green photosynthetic bacterial antennae

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Acaryochloris marina is a unique photosynthetic prokaryote containing chlorophyll(Chl)-d as a major photoactive pigment (over 95%). The molecular structure of Chl-d is proposed as the 3-formyl analog of Chl-a. However, the stereochemistry of Chl-d at the 132-, 17- and 18-positions has not yet been established unambiguously. In the first part of this paper, we describe the determination of their stereochemistries to be 132-(R)-, 17-(S)- and 18-(S)-configurations by using 1H-1H NOE correlations in 1H-NMR and circular dichroism spectra as well as chemical modification of Chl-a to produce stereochemically defined Chl derivatives. In the second part of the paper, we report a facile synthesis of a self-aggregative Chl by modifying isolated Chl-d. Since Chl-d was characterized by its reactive 3-formyl group, the formyl group was reduced with t-BuNH2BH3 to afford the desirable Chl, 3-deformyl-3-hydroxymethyl-pyrochlorophyll-d (31-OH-pyroChl-d). The synthetic 31-OH-pyroChl-d molecules spontaneously self-organized to form well-ordered aggregates in a non-polar organic solvent. The self-aggregates are a good model of major light-harvesting antenna systems of green photosynthetic bacteria, chlorosomes, in terms of the following three findings. (1) Both the red-shifted electronic absorption band above 750 nm and its induced reverse S-shape CD signal around 750 nm were observed in 0.5% (v/v) THF-cyclohexane. (2) The stretching mode of the 13-carbonyl group was downshifted by about 35 cm−1 from the wavenumber of its free carbonyl. (3) The self-aggregates were quite stable on titration of pyridine to the suspension, in comparison with those of natural chlorosomal bacteriochlorophyll-d possessing the 3-(1-hydroxyethyl) group.

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

Similar content being viewed by others

References

  1. R. E. Blankenship and K. Matsuura, in Light-Harvesting Antennas, ed. B. R. Green and W. W. Parson, Kluwer Academic Publishers, The Netherlands, 2003, pp. 195–217.

  2. J. M. Olson, Chlorophyll organization and function in green photosynthetic bacteria Photochem. Photobiol. 1998 67 61–75.

    Article  CAS  Google Scholar 

  3. R. E. Blankenship, J. M. Olson and M. Miller, Antenna complexes from green photosynthetic bacteria, in Anoxygenic Photosynthetic Bacteria, ed. R. E. Blankenship, M. T. Madigan and C. E. Bauer, Kluwer Academic Publishers, The Netherlands, 1995, pp. 399–435.

    Chapter  Google Scholar 

  4. H. Tamiaki, Supramolecular structure in extramembraneous antennae of green photosynthetic bacteria Coord. Chem. Rev. 1996 148 183–197.

    Article  CAS  Google Scholar 

  5. L. A. Staehelin, J. R. Golecki and G. Drews, Supramolecular organization of chlorosomes (Chlorobium vesicles) and of their membrane attachment sites in Chlorobium limicola Biochim. Biophys. Acta 1980 589 30–45.

    Article  CAS  Google Scholar 

  6. L. A. Staehelin, J. R. Golecki, R. C. Fuller and G. Drews, Visualization of the supramolecular architecture of chlorosomes (Chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus Arch. Microbiol. 1978 119 269–278.

    Article  Google Scholar 

  7. K. M. Smith, Chlorosome chlorophylls (bacteriochlorophylls c, d, and e): Structures, partial syntheses, and biosynthetic proposals, in The Porphyrin Handbook, ed. K. M. Kadish, K. M. Smith and R. Guilard, Elsevier Science, USA, 2003, vol. 13, pp. 157–182.

    Chapter  Google Scholar 

  8. T. Mizoguchi, Y. Saga and H. Tamiaki, Isolation and structure determination of a complete set of bacteriochlorophyll-d homologs and epimers from a green sulfur bacterium Chlorobium vibrioforme and their aggregation properties in hydrophobic solvents Photochem. Photobiol. Sci. 2002 1 780–787.

    Article  CAS  Google Scholar 

  9. H. Tamiaki, Self-aggregates of natural and modified chlorophylls as photosynthetic light-harvesting antenna systems: Substituent effect on the B-ring Photochem. Photobiol. Sci. 2005 4 675–680.

    Article  CAS  Google Scholar 

  10. T. Miyatake and H. Tamiaki, Self-aggregates of bacteriochlorophylls-c, d and e in a light-harvesting antenna system of green photosynthetic bacteria: Effect of stereochemistry at the chiral 3-(1-hydroxyethyl) group on the supramolecular arrangement of chlorophyllous pigments J. Photochem. Photobiol. C: Photochem. Rev. 2005 6 89–107.

    Article  CAS  Google Scholar 

  11. T. S. Balaban, H. Tamiaki and A. R. Holzwarth, Chlorins programmed for self-assembly, in Supramolecular Dye Chemistry, ed. F. Würthner, Springer, Heidelberg, (Topics Curr. Chem., vol. 258), 2005, pp. 1-38.

    Google Scholar 

  12. 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 

  13. 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 

  14. V. Huber, M. Katterle, M. Lysetska, F. Würthner, Reversible self-organization of semisynthetic zinc chlorins into well-defined rod antennae Angew. Chem., Int. Ed. 2005 44 3147–3151.

    Article  CAS  Google Scholar 

  15. M. Kunieda, T. Mizoguchi and H. Tamiaki, Diastereoselective self-aggregation of synthetic 3-(1-hydroxyethyl)-bacteriopyrochlorophyll-a as a novel photosynthetic antenna model absorbing near the infrared region Photochem. Photobiol. 2004 79 55–61.

    Article  CAS  Google Scholar 

  16. P. Cheng, P. A. Liddell, S. X. C. Ma and R. E. Blankenship, Properties of zinc and magnesium methyl bacteriopheophorbide d and their aggregates Photochem. Photobiol. 1993 58 290–295.

    Article  CAS  Google Scholar 

  17. T. S. Balaban, A. R. Holzwarth, K. Schaffner, G.-J. Boender, H. J. M. de Groot, CP-MAS 13C-NMR dipolar correlation spectroscopy of 13C-enriched chlorosomes and isolated bacteriochlorophyll c aggregates of Chlorobium tepidum: the self-organization of pigments is the main structural feature of chlorosomes Biochemistry 1995 34 15259–15266.

    Article  CAS  Google Scholar 

  18. W. M. Manning and H. H. Strain, Chlorophyll d, a green pigment of red algae J. Biol. Chem. 1943 151 1–19.

    Article  CAS  Google Scholar 

  19. A. S. Holz and H. V. Morley, A proposed structure for chlorophyll d Can. J. Chem. 1959 37 507–514.

    Article  Google Scholar 

  20. H. Miyashita, H. Ikemoto, N. Kurano, K. Adachi, M. Chihara and S. Miyachi, Chlorophyll d as a major pigment Nature 1996 383 402.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. A. Murakami, H. Miyashita, M. Iseki, K. Adachi and M. Mimuro, Chlorophyll d in an epiphytic cyanobacterium of red algae Science 2004 303 1633.

    Article  CAS  Google Scholar 

  23. H. Morishita and H. Tamiaki, Synthesis of regioselectively 18O-labelled chlorophyll derivatives at the 31- and/or 131-positions through one-pot exchange of carbonyl oxygen atoms Tetrahedron 2005 61 6097–6107.

    Article  CAS  Google Scholar 

  24. T. M. Wahlund, C. R. Woese, R. W. Castenholz and M. T. Madigan, A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. Nov. Arch. Microbiol. 1991 156 81–90.

    Article  CAS  Google Scholar 

  25. Y. Saga, H. Oh-oka, T. Hayashi and H. Tamiaki, Presence of exclusively bacteriochlorophyll-c containing substrain in the culture of green sulfur photosynthetic bacterium Chlorobium vibrioforme strain NCIB 8327 producing bacteriochlorophyll-d Anal. Sci. 2003 19 1575–1579.

    Article  CAS  Google Scholar 

  26. P. D. Gerola and J. M. Olson, A new bacteriochlorophyll a-protein complex associated with chlorosomes of green sulfur bacteria Biochim. Biophys. Acta 1985 848 69–76.

    Article  Google Scholar 

  27. T. Watanabe, M. Nakazato, H. Mazaki, A. Hongu, M. Konno, S. Saitoh and K. Honda, Chlorophyll a epimer and pheophytin a in green leaves Biochim. Biophys. Acta 1985 807 110–117.

    Article  CAS  Google Scholar 

  28. J. J. Katz, G. D. Norman, W. A. Svec and H. H. Strain, Chlorophyll diastereoisomers. The nature of chlorophylls a′ and b′ and evidence for bacteriochlorophyll epimers from proton magnetic resonance studies J. Am. Chem. Soc. 1968 90 6841–6845.

    Article  CAS  Google Scholar 

  29. H.-C. Chow, R. Serlin and C. E. Strouse, The crystal and molecular structure and absolute configuration of ethyl chlorophyllide a dihydrate. A model for the different spectral forms of chlorophyll a J. Am. Chem. Soc. 1975 97 7230–7237.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  31. S. Yagai, T. Miyatake, Y. Shimono and H. Tamiaki, Supramolecular structure of self-assembled synthetic zinc-131-oxo-chlorins possessing a primary, secondary or tertiary alcoholic 31-hydroxy group: Visible spectroscopic and molecular modeling studies Photochem. Photobiol. 2001 73 153–163.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

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

    Tadashi Mizoguchi, Ayumi Shoji, Michio Kunieda & Hitoshi Tamiaki

  2. Department of Technology and Ecology, Hall of Global Environmental Research, Kyoto University, Kyoto, 606-8501, Japan

    Hideaki Miyashita, Tohru Tsuchiya & Mamoru Mimuro

  3. Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, 606-8501, Japan

    Hideaki Miyashita, Tohru Tsuchiya & Mamoru Mimuro

Authors
  1. Tadashi Mizoguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ayumi Shoji
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michio Kunieda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hideaki Miyashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tohru Tsuchiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mamoru Mimuro
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hitoshi Tamiaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hitoshi Tamiaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mizoguchi, T., Shoji, A., Kunieda, M. et al. Stereochemical determination of chlorophyll-d molecule from Acaryochloris marina and its modification to a self-aggregative chlorophyll as a model of green photosynthetic bacterial antennae. Photochem Photobiol Sci 5, 291–299 (2006). https://doi.org/10.1039/b514088a

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b514088a

Search

Navigation