Skip to main content
Log in

LH2 Complex from Sulfur Bacteria Allochromatium vinosum – Natural Singlet Oxygen Sensor

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

It was established that in a heterogeneous model system, which consisted of two types of complexes: reaction center or core complex of photosystem 2 of higher plants and LH2 complex of the sulfur bacterium Alc. vinosum, BChl850 oxidation of the LH2 complex could be observed under illumination by the light at a wavelength of 662 nm, which is the red absorption band of Chl. It has been shown that this process induces release of singlet oxygen, which is generated in photosystem II complexes and then partially diffuses into LH2 complex, where it oxidizes BChl850. It was established by HPLC that this results in formation of a product of BChl oxidation, 3-acetylchlorophyll. The process of BChl850 oxidation is inhibited by singlet oxygen quenchers (Trolox and Na ascorbate). It is suggested that the LH2 complex from the sulfur bacterium Alc. vinosum could be used to detect generation of singlet oxygen by the chlorophyll containing samples.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.

Similar content being viewed by others

Abbreviations

AcChl:

3-acetyl-chlorophyll

BChl:

bacteriochlorophyll

Chl:

chlorophyll

LH1 and LH2:

light-harvesting complexes

PSII:

photosystem II

RC:

reaction center

References

  1. Bril, C. (1958) Action of a non-ionic detergent on chromatophores of Rhodopseudomonas spheroids, Biochim. Biophys. Acta, 29, 458, https://doi.org/10.1016/0006-3002(58)90223-3.

    Article  CAS  PubMed  Google Scholar 

  2. Moskalenko, A. A., and Erokhin, Yu. E. (1971) Electrophoresis in Polyacrylamide Gel and its Application in Biology, Agriculture, Medicine, and Food Industry, Moscow.

  3. Moskalenko, A. A., and Erokhin, Yu. E. (1974) Isolation of pigment-liporpotein complexes from purple bacteria using preparative electrophoresis in polyacrylamide gel [in Russian], Mikrobiologiia, 43, 654-658.

    CAS  PubMed  Google Scholar 

  4. Shuvalov, V. A., Klimov, V. V., Krakhmaleva, N. N., Moskalenko, A. A., and Krasnovskii, A. A. (1976) Phototransformation of pheophytin in reaction centers of Rhodospirillum rubrum and Chromatium minutissimum, Dokl Acad Nauk SSSR, 227, 984-987.

    CAS  Google Scholar 

  5. Shuvalov, V. A., Klimov, V. V. (1976) The primary photoreactions in the complex cytochrome-P-890 P-760 (bacteriopheophytin760) of Chromatium minutissimum at low redox potentials, Biochim. Biophys. Acta Bioenerg., 440, 587-599, https://doi.org/10.1016/0005-2728(76)90044-x.

    Article  CAS  Google Scholar 

  6. Freer, A., Prince, S., Sauer, K., Papiz, M., Hawthornthwaite-Lawless, A., et al. (1996) Pigment-pigment interactions and energy transfer in the antenna complex of the photosynthetic bacterium Rhodopseudomonas acidophila, Structure, 4, 449-462, https://doi.org/10.1016/S0969-2126(96)00050-0.

    Article  CAS  PubMed  Google Scholar 

  7. Gabrielsen, M., Gardiner, A., and Cogdell, R. (2009) In the Purple Phototrophic Bacteria (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., eds) Springer, Dordrecht, 28, 135-153, doi: 10.1007/978-1-4020-8815-5_8.

  8. Moskalenko, A. A., and Makhneva, Z. K. (2012) Light-harvesting complexes from purple sulfur bacteria Allochromatium minutissimum assembled without carotenoids, J. Photochem. Photobiol. B Biol., 108, 1-7, https://doi.org/10.1016/j.jphotobiol.2011.11.006.

    Article  CAS  Google Scholar 

  9. Lӧhner, A., Carey, A. M., Hacking, K., Picken, N., Kelly, S., et al. (2015) The origin of the split B800 absorption peak in the LH2 complexes from Allochromatium vinosum, Photosynth. Res., 123, 23-31, https://doi.org/10.1016/j.bbabio.2014.07.022.

    Article  CAS  Google Scholar 

  10. Cogdell, R., and Frank, H. (1987) How carotenoids function in photosynthetic bacteria, Biochim. Biophys. Acta, 895, 63-79, https://doi.org/10.1016/S0304-4173(87)80008-3.

    Article  CAS  PubMed  Google Scholar 

  11. Frank, H., and Cogdell, R. (1996) Carotenoids in photosynthesis, Photochem. Photobiol., 63, 257-264, https://doi.org/10.1111/j.1751-1097.1996.tb03022.x.

    Article  CAS  PubMed  Google Scholar 

  12. Cogdell, R. J., Howard, T. D., Bittl, R., Schlodder, E., Geisenheimer, I., et al. (2000) How carotenoids protect bacterial photosynthesis, Philos. Trans. R. Soc. B Biol. Sci., 355, 1345-1349, https://doi.org/10.1098/rstb.2000.0696.

    Article  CAS  Google Scholar 

  13. Britton, G. (2008) Carotenoids in Photosynthesis, in Carotenoids. Natural Functions (Britton, G., Liaaen-Jensen, S., and Pfander, H., eds.) Birkhauser Verlag, Switzerland, pp. 265-308, https://doi.org/10.1007/978-3-7643-7499-0_14.

  14. Edge, R., and Truscott, T. G. (2018) Singlet oxygen and free radical reactions of retinoids and carotenoids – a review, Antioxidants, 7, 5-16, https://doi.org/10.3390/antiox7010005.

    Article  CAS  PubMed Central  Google Scholar 

  15. Makhneva, Z. K., Ashikhmin, A. A., Bolshakov, M. A., and Moskalenko, A. A. (2019) Bacteriochlorophyll interaction with singlet oxygen in membranes of purple photosynthetic bacteria: does the protective functions of carotenoids exist? Dokl. Biochem. Biophys., 486, 216-219, https://doi.org/10.1134/S1607672919030141.

    Article  CAS  PubMed  Google Scholar 

  16. Makhneva, Z. K., Ashikhmin, A. A., Bolshakov, M. A., and Moskalenko, A. A. (2020) Carotenoids are probably involved in singlet oxygen generation in the membranes of purple photosynthetic bacteria under light irradiation, Microbiology, 89, 164-173, https://doi.org/10.1134/S0026261720010099.

    Article  CAS  Google Scholar 

  17. Makhneva, Z. K., Bolshakov, M. A., and Moskalenko, A. A. (2021) Carotenoids do not protect bacteriochlorophylls in isolated light-harvesting LH2 complexes of photosynthetic bacteria from destructive interactions with singlet oxygen, Molecules, 26, 5120, https://doi.org/10.3390/molecules26175120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Makhneva, Z. K., Ashikhmin, A. A., Bolshakov, M. A., and Moskalenko, A. A. (2016) 3-Acetyl-cholorophyll formation in light-harvesting complexes of purple bacteria by chemical oxidation, Biochemistry (Moscow), 81, 176-186, https://doi.org/10.1134/S0006297916020115.

    Article  CAS  Google Scholar 

  19. Makhneva, Z. K., and Moskalenko, A. A. (2022) Carotenoids in LH2 complexes of Allochromatium vinosum under illumination are able to generate singlet oxygen which oxidizes BChl850, Microbiology, 91, 409-416, https://doi.org/10.1134/S002626172230021X.

    Article  CAS  Google Scholar 

  20. Bolshakov, M. A., Ashikhmin, A. A., Makhneva, Z. K., and Moskalenko, A. A. (2016) Effect of illumination intensity and inhibition of carotenoid biosynthesis on assembly of peripheral light-harvesting complexes in purple sulfur bacteria Allochromatium vinosum ATCC 17899, Mikrobiologiia, 85, 403-414.

    CAS  Google Scholar 

  21. Bolshakov, M. A., Ashikhmin, A. A., Makhneva, Z. K., and Moskalenko, A. A. (2018) Effect of light with different spectral composition on cell growth and pigment composition of the membranes of purple sulfur bacteria Allochromatium minutissimum and Allochromatium vinosum, Microbiology, 87, 191-199, https://doi.org/10.1134/S0026261718020042.

    Article  CAS  Google Scholar 

  22. Berthold, D. A., Babcock, G. T., and Yocum, C. F. (1981) A highly resolved, oxygen-evolving photosystem II preparations from spinach thylakoids membranes, EPR and electron-transport properties, FEBS Lett., 134, 231-234, https://doi.org/10.1016/0014-5793(81)80608-4.

    Article  CAS  Google Scholar 

  23. Enami, I., Kamino, K., Shen, J. -R., Satoh, K., and Katoh, S. (1989) Isolation and characterization of photosystem II complexes which lack light-harvesting chlorophyll a/b proteins but retain three extrinsic proteins related to oxygen evolution from spinach, Biochem. Biophis. Acta, 977, 33-39, https://doi.org/10.1016/S0005-2728(89)80006-4.

    Article  CAS  Google Scholar 

  24. Nanba, O., and Satoh, K. (1987) Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559, Proc. Natl. Acad. Sci. USA, 84, 109-112, https://doi.org/10.1073/pnas.84.1.109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Khristin, M. S., Nikitishena, O. V., Smolova, T. N., and Zastrizhnaya, O. M. (1997) Extraction of functionally active Photosystem II pigment–protein complexes from pea thylakoids and their purification on Sepharose DEAE 6B, Biol. Membr. (Moscow), 14, 133-142.

    CAS  Google Scholar 

  26. Khorobrykh, S. A., Khorobrykh, A. A., Klimov, V. V., and Ivanov, B. N. (2002) Photoconsumption of oxygen in Photosystem II preparations under impairment of the water-oxidizing complex, Biochemistry, 67, 683-688, https://doi.org/10.1023/A:1016154506817.

    Article  CAS  PubMed  Google Scholar 

  27. Telfer, A., Bishop, S. M., Phillips, D., and Barber, J. (1994) Isolated photosynthetic reaction-center of photosystem-II as a sensitizer for the formation of singlet oxygen – detection and quantum yield determination using a chemical trapping technique, J. Biol. Chem., 269, 13244-13253.

    Article  CAS  Google Scholar 

  28. Ashikhmin, A., Makhneva, Z., and Moskalenko, A. (2014) The LH2 complexes are assembled in the cells of purple sulfur bacterium Ectothiorhodospira haloalkaliphila with inhibition of carotenoid biosynthesis, Photosynth. Res., 119, 291-303, https://doi.org/10.1007/s11120-013-9947-6.

    Article  CAS  PubMed  Google Scholar 

  29. Makhneva, Z. K., Ashikhmin, A. A., Bolshakov, M. A., and Moskalenko, A. A. (2019) Quenchers protect BChl850 from action of singlet oxygen in the membranes of a sulfur photosynthetic bacteria Allochromatium vinosum strain MSU, Microbiology, 88, 79-86, https://doi.org/10.1134/S0026261719010119.

    Article  CAS  Google Scholar 

  30. Limantara, L., Koehler, P., Wilhelm, B., Porra, R. J., and Scheer, H. (2006) Photostability of bacteriochlorophyll a and derivatives: potential sensitizers for photodynamic tumor therapy, Photochem. Photobiol., 82, 770-780, https://doi.org/10.1562/2005-09-07-RA-676.

    Article  CAS  PubMed  Google Scholar 

  31. Krasnovsky, A. A., Jr. (1979) Photoluminescence of singlet oxygen in pigment solutions, Photochem. Photobiol., 29, 29-36, https://doi.org/10.1111/j.1751-1097.1979.tb09255.x.

    Article  CAS  Google Scholar 

  32. Niedzwiedzki, D. M., Swainsbury, D. J. K., Canniffed, D. P., Hunter, C. N., and Hitchcock, A. (2020) A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection, Proc. Nat. Acad. Sci. USA, 117, 6502-6508, https://doi.org/10.1073/pnas.1920923117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Tamura, H., and Ishikita, H. (2020) Quenching of Singlet oxygen by carotenoids via ultrafast super-exchange dynamics, J. Phys. Chem. A, 124, 5081-5088, https://doi.org/10.1021/acs.jpca.0c02228.

    Article  CAS  PubMed  Google Scholar 

  34. Uragami, C., Sato, H., Yukihira, N., Fujiwara, M., Kosumi, D., Gardiner, A., Cogdell, R., and Hashimoto, H. (2020) Photoprotective mechanisms in the core LH1 antenna pigment-protein complex from the purple photosynthetic bacterium, Rhodospirillum rubrum, J. Photoch. Photobiol. A Chem., 400, 112628, https://doi.org/10.1016/j.jphotochem.2020.112628.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Z. A. Zhuravleva (Institute of Basic Biological Problems, Russian Academy of Sciences) for help in growing bacterial cultures.

Funding

This work was financially supported by the State Budget project no. 122041100204-3.

Author information

Authors and Affiliations

Authors

Contributions

A. A. Moskalenko – concept of the study and supervision of the work; Z. K. Makhneva, T. N. Smolova, M. A. Bolshakov – conducting experiments; Z. K. Makhneva, T. N. Smolova, M. A. Bolshakov, A. A. Moskalenko – discussion of the results of the study; A. A. Moskalenko – writing text of the paper; M. A. Bolshakov – editing of text of the paper.

Corresponding author

Correspondence to Maksim A. Bolshakov.

Ethics declarations

The authors declare no conflict of interests in financial or any other sphere. This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Makhneva, Z.K., Smolova, T.N., Bolshakov, M.A. et al. LH2 Complex from Sulfur Bacteria Allochromatium vinosum – Natural Singlet Oxygen Sensor. Biochemistry Moscow 87, 1159–1168 (2022). https://doi.org/10.1134/S0006297922100091

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297922100091

Keywords

Navigation