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.
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
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.
Moskalenko, A. A., and Erokhin, Yu. E. (1971) Electrophoresis in Polyacrylamide Gel and its Application in Biology, Agriculture, Medicine, and Food Industry, Moscow.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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
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
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297922100091