Photosynthesis Research

, Volume 40, Issue 2, pp 191–198 | Cite as

Generation and quenching of singlet molecular oxygen by aggregated bacteriochlorophyll d in model systems and chlorosomes

  • A. A. KrasnovskyJr.
  • J. Lopez
  • P. Cheng
  • P. A. Liddell
  • R. E. Blankenship
  • T. A. Moore
  • D. Gust
Regular Paper

Abstract

Both photogeneration and quenching of singlet oxygen by monomeric and aggregated (dimeric and oligomeric) molecules of bacteriochlorophyll (BChl) d have been studied in solution and in chlorosomes isolated from the green photosynthetic bacterium Chlorobium vibrioforme f. thiosulfatophilum. The yield of singlet-oxygen photogeneration by pigment dimers was about 6 times less than for monomers. Singlet oxygen formation was not observed in oligomer-containing solutions or in chlorosomes. To estimate the efficiency of singlet oxygen quenching an effective rate constant for 1O2 quenching by BChl molecules (kqM) was determined using the Stern-Volmer equation and the total concentration of BChl d in the samples. In solutions containing only monomeric BChl, the kqM values coincide with the real values for 1O2 quenching rate constants by BChl molecules. Aggregation weakly influenced the kqM values in pigment solutions. In chlorosomes (which contain both BChl and carotenoids) the kqM value was less than in solutions of BChl alone and much less than in acetone extracts from chlorosomes. Thus 1O2 quenching by BChl and carotenoids is much less efficient in chlorosomes than in solution and is likely caused primarily by BChl molecules which are close to the surface of the large chlorosome particles. The data allow a general conclusion that monomeric and dimeric chlorophyll molecules are the most likely sources of 1O2 formation in photosynthetic systems and excitation energy trapping by the long wavelength aggregates as well as 1O2 physical quenching by monomeric and aggregated chlorophyll can be considered as parts of the protective system against singlet oxygen formation.

Key words

bacteriochlorophyll d bacteriochlorophyll d dimers and oligomers chlorosomes green photosynthetic bacteria singlet oxygen generation and quenching bacteriochlorophyll d triplet state 

Abbreviations

BChl

bacteriochlorophyll

MBpd

methyl bacteriopheophorbide

Chl

chlorophyll

TPP

meso-tetraphenylporphyrin

TPPS

meso-tetra (p-sulfophenyl) porphyrin

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References

  1. Asada K and Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Topics in Photosynthesis. Photoinhibition, Vol 9, pp 227–287. Elsevier, AmsterdamGoogle Scholar
  2. Blankenship RE Brune DC and Wittmershaus BP (1988) Chlorosome antennas in green photosynthetic bacteria. In: Stevens SEJr. and Bryant DA (eds) Light Energy Transduction in Photosynthesis. Higher Plants and Bacterial Models, pp 32–46. American Society of Plant Physiologists, Rockville, MDGoogle Scholar
  3. Borland CF, Mc Garvey DJ, Truscott TJ, Cogdell RG and Land EJ (1987) Photophysical studies of bacteriochlorophyll a and bacteriopheophytin a-singlet oxygen generation. J Photochem Photobiol B: Biol 1: 93–101CrossRefGoogle Scholar
  4. Brune DC, Nozava T and Blankenship RE (1987) Antenna organization in green photosynthetic bacteria. 1. Oligomeric Bacteriochlorophyll c as a model for the 740 nm absorbing bacteriochlorophyll c in Chloroflexus aurantiacus chlorosomes. Biochemistry 26: 8644–8652.PubMedGoogle Scholar
  5. Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Ann Rev Plant Physiol 29: 345–348.CrossRefGoogle Scholar
  6. Causgrove P, Brune CS, Wang J, Witmerhaus BP and Blankenship RE (1990) Energy transfer kinetics in whole cells and isolated chlorosomes of green photosynthetic bacteria. Photosynth Res 26: 39–48.Google Scholar
  7. Cheng P, Liddell P, Ma XC and Blankenship RE (1993) Properties of Zn and Mg methyl bacteriopheophorbide-d and their aggregates. Photochem Photobiol 58: 290–295.Google Scholar
  8. Dzhagarov BM, Gurinovich GP, Novichenkov VE, Salokhiddinov KI, Shulga AM and Ganja VA (1990) Photosensitized formation of singlet oxygen and the quantum yield of intersystem crossing in porphyrin and metalloporphyrin molecules. Sov J Chem Phys (Engl translation) 6: 2098–2119.Google Scholar
  9. Egorov S Yu and Krasnovsky AAJr (1990) Laser-induced luminescence of singlet-molecular oxygen. Generation by drugs and pigments of biological importance. SPIE Proc 1403: 611–621Google Scholar
  10. Egorov S Yu, Krasnovsky AAJr, Vychegzanina IV, Drozdova NN and Krasnovsky AA (1990) Photosensitized formation and quenching of singlet molecular oxygen by monomeric and aggregated molecules of the pigments of photosynthetic bacteria. Dokl. AN SSSR (Biophysics) 310: 471–476.Google Scholar
  11. Foote CS (1976) Photosensitized oxygenation and singlet oxygen In: Pryor WA (ed) Free RAdicals in Biology, Vol 2, pp 85–133. Academic Press, New YorkGoogle Scholar
  12. Gerola PD and Olson JM (1986) A new bacteriochlorophyll-a-protein complex associated with chlorosomes of green sulfur bacteria. Biochim Biophys Acta, 848: 69–76PubMedGoogle Scholar
  13. Holt AS (1966) Recently characterized chlorophylls. In: Vernon LP and Seely GR (eds) The Chlorophylls, pp 11–118. Academic Press, New York, LondonGoogle Scholar
  14. Katz JJ, Bowman MK, Michalski TJ and Worcester DL (1991) Chlorophyll aggregation: Chlorophyll/water micelles as models for in vivo long-wavelength chlorophyll. In: Scheer H (ed) Chlorophylls, pp 211–235. CRC Press, Inc, Boca Raton, FLGoogle Scholar
  15. Krasnovsky AAJr (1977) Photoluminescene of singlet oxygen in solutions of chlorophylls and pheophytins. Biofizika 22: 81–89.Google Scholar
  16. Krasnovsky AAJr (1979) Photoluminescence of singlet oxygen in pigment solutions. Photochem Photobiol 29: 29–36.Google Scholar
  17. Krasnovsky AAJr (1986) Singlet oxygen in photosynthesizing organisms. Mendeleev Chemistry J 31: 562–567.Google Scholar
  18. Krasnovsky AA and MIBystrova (1980) Self-assembly of chlorophyll aggregated structures. BioSystems 12: 181–194CrossRefPubMedGoogle Scholar
  19. Krasnovsky AA and YeVPakshina (1959) Photochemical and spectral properties of bacterioviridin of green sulfur bacteria. Dokl AN SSSR (Biochemistry) 127: 913–916.Google Scholar
  20. Krasnovsky AAJr, Cheng P Blankenship RE Moore TA and Gust D (1993) The photophysics of monomeric bacteriochlorophylls-c, d and their derivatives: properties of the triplet state and singlet oxygen generation and quenching. Photochem. Photobiol. 57: 324–330.PubMedGoogle Scholar
  21. Krasnovsky AAJr, Venediktov EA and Chernenko OV (1982) Quenching of singlet oxygen by chlorophylls and porphyrins Biofizika 27: 966–972PubMedGoogle Scholar
  22. Krasnovsky AAJr, Vychegzanina IV, Drozdova NN and Krasnovsky AA (1985) Generation and quenching of singlet molecular oxygen by bacteriochlophylls and bacteriopheophytins-a and -b. Dokl. AN SSSR (Biophysics) 283: 474–477Google Scholar
  23. Krasnovsky AAJr, Egorov S Yu, Nasarova OV., Yartsev EI and Ponomarev GV (1988) Photosensitized formation of singlet molecular oxygen in solutions of water-soluble porphyrins. Direct luminescence measurements. Studia biophys 124: 123–142.Google Scholar
  24. Litvin FF and Sineschekov VA (1975) Molecular organization of chlorophyll and energetics of the initial stages in photosynthesis. In: Govindjee (ed) Bioenergetics of Photosynthesis, pp 619–661. Academic Press, New YorkGoogle Scholar
  25. Melis A (1991) Dinamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106.Google Scholar
  26. Olson JM (1980) Chlorophyll organization in green photosynthetic bacteria. Biochim. Biophys Acta 594: 33–51.PubMedGoogle Scholar
  27. Pierson BK and Castenholz RW (1978) Photosynthetic apparatus and cell membranes of the green bacteria. In: Clayton RK and Sistrom WR (ed) The Photosynthetic Bacteria, pp 179–197. Plenum Press, New YorkGoogle Scholar
  28. Smith KM, Kehres LA and Fajer J (1983) Aggregation of the bacteriochlorophylls c, d and e. Models for the antenna chlorophylls of green and brown photosynthetic bacteria. J Am Chem Soc 105: 1387–1389Google Scholar
  29. Smith KM Bobe FW Goff DA and Abraham RJ (1986) NMR Spectra of porphyrins. 28. Detailed solution structure of a bacteriochlorophyllide d dimer. J Am Chem Soc 108: 1116–1118.Google Scholar
  30. Tanelian C and Wolf C (1988) Mechanism of physical quenching of singlet molecular oxygen by chlorophylls and related compounds of biological interest. Photochem Photobiol 48: 277–280.Google Scholar
  31. Wang J Brune DC and Blankenship RE (1990) Effects of oxidants and reductants on the efficiency of excitation energy transfer in green photosynthetic bacteria. Biochim Biophys Acta 1015: 457–463.PubMedGoogle Scholar
  32. Zuber H and Brunisholz RA (1992) Structure and function of antenna polypeptide and chlorophyll-protein complexes: Principles and variability. In: Scheer H (ed) Chlorophylls, pp 627–704. CRC Press, Inc, Boca Raton, FLGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • A. A. KrasnovskyJr.
    • 1
    • 2
  • J. Lopez
    • 1
  • P. Cheng
    • 1
  • P. A. Liddell
    • 1
  • R. E. Blankenship
    • 1
  • T. A. Moore
    • 1
  • D. Gust
    • 1
  1. 1.Department of Chemistry and Biochemistry, Center for the Study of Early Events in PhotosynthesisArizona State UniversityTempeUSA
  2. 2.Institute of BiochemistryRussian Academy of ScienceMoscowRussia

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