Skip to main content
SpringerLink
Log in

Rhodopin Incorporated into the Allochromatium vinosum LH2 Complex Is Able to Generate Singlet Oxygen under Illumination

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract—

DPA membranes from Allochromatium vinosum cells, in which carotenoid biosynthesis was inhibited using diphenylamine (DPA) were obtained, into which rhodopin was incorporated. The LH2 complex with rhodopin content of 85% was isolated. Using a test for the thermal stability of LH2 complexes (DPA and with incorporated rhodopin), it was established that carotenoids of the early stages of biosynthesis (≤1 molecules per complex) did not interfere with rhodopin incorporation. It was found that when the LH2 complex with incorporated rhodopin was irradiated with light at the wavelength of 502 nm, BChl850 was photobleached at a rate close to that in the control LH2 complex. This indicates that rhodopin, after being incorporated into the DPA LH2 complex, is capable of generating singlet oxygen under illumination. Previously obtained data on heterogeneity of the carotenoid composition in DPA LH2 complexes (variation in the number of individual carotenoids molecules per complex in the general population) and our earlier suggestion about the structural role of carotenoids, namely, their ability to stabilize the LH2 complexes, were confirmed. Based on analysis of our results, as well as of the literature data, the interaction of singlet oxygen and carotenoids is discussed.

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

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

Similar content being viewed by others

REFERENCES

  1. Ashikhmin, A.A., Benditkis, A.S., Moskalenko, A.A., and Krasnovsky, A.A., Jr., ζ-Carotene: generation and quenching of singlet oxygen, comparison with phytofluene, Biochemistry (Moscow), 2022, vol. 87, no. 10, pp. 1169–1178. https://doi.org/10.1134/S0006297922100108

    Article  CAS  PubMed  Google Scholar 

  2. Ashikhmin, A.A., Carotenoids of light-harvesting complexes of purple sulfur bacterium Ect. haloalkaliphila, Extended Abstract of Cand. Sci (Biol.) Dissertation, Pushchino: Institute of Fundamental Problems of Biology, Russian Academy of Sciences, 2014.

  3. Ashikhmin, A.A., Makhneva, Z.K., Bolshakov, M.A., and Moskalenko, A.A., The influence of the number of conjugated double bonds in carotenoid molecules on the energy transfer efficiency to bacteriochlorophyll in light-harvesting complexes LH2 from Allochromatium vinosum strain MSU, Doklady Biochem. Biophys., 2018, vol. 483, no. 1, pp. 321–325.

    Article  CAS  Google Scholar 

  4. Ashikhmin, A., Benditkis, A., Moskalenko, A., and Krasnovsky, A.A., Jr., Phytofluene as a highly efficient UV-A photosensitizer of singlet oxygen generation, Biochemistry (Moscow), 2020, vol. 85, pp. 773–780. https://doi.org/10.1134/S0006297920070056

    Article  CAS  PubMed  Google Scholar 

  5. Ashikhmin, A., Makhneva, Z., Bolshakov, M., and Moskalenko, A., Incorporation of spheroidene and spheroidenone into light-harvesting complexes from purple sulfur bacteria, J. Photochem. Photobiol. B. Biol., 2017, vol. 170, pp. 99–107. https://doi.org/https://doi.org/10.1016/j.jphotobiol.2017. 03.020

    Article  CAS  Google Scholar 

  6. Bolshakov, M.A., Ashikhmin, A.A., Makhneva, Z.K., and Moskalenko, A.A. Effect of illumination intensity and inhibition of carotenoid biosynthesis on assembly of peripheral light-harvesting complexes in purple sulfur bacteria Allochromatium vinosum ATCC 17899, Microbiology (Moscow), 2016, vol. 85, no. 4, pp. 420–429.

    Article  CAS  Google Scholar 

  7. Bolshakov M.A. The role of carotenoids in the photooxidation of bacteriochlorophyll in vivo, Extended Abstract of Cand. Sci (Biol.) Dissertation, Pushchino: Institute of Fundamental Problems of Biology, Russian Academy of Sciences, 2012.

  8. Borland, C.F., McGarvey, D.J., Truscott, T.G., Codgell, R.J., and Land, E.J., Photophysical studies of bacteriochlorophyll a and bacteriopheophytin a—singlet oxygen generation, J. Photochem. Photobiol. B: Biol., 1987, vol. 1, no. 1, pp. 93–101. https://doi.org/10.1016/1011-1344(87)80009-X

    Article  CAS  Google Scholar 

  9. Britton, G., Functions of intact carotenoids, in Carotenoids. Natural Functions, Britton, G., Liaaen-Jensen, S., and Pfanger, H., Eds., Birkhauser, 2008, pp. 265–308.

    Google Scholar 

  10. Calvin, M., Function of carotenoids in photosynthesis, Nature, 1955, vol. 176, p. 1215.

    Article  CAS  Google Scholar 

  11. Cogdell, R.J. and Frank, H.A., How carotenoids function in photosynthetic bacteria, Biochim. Biophys. Acta, 1987, vol. 895, pp. 63–79.

    Article  CAS  PubMed  Google Scholar 

  12. Egorov, S.Y., Krasnovskii, A.A., Jr., Vychegzhanina, I.V., Drozdova, N.N., and Krasnovskii, A.A., Generation and quenching of molecular single oxygen by pigment molecules in photosynthetic bacteria, Doklady Biophys., 1990, vol. 310, no. 2, pp. 6–10.

    Google Scholar 

  13. Frank, H.A. and Cogdell, R.J., Carotenoids in photosynthesis, Photochem. Photobiol., 1996, vol. 63, no. 3, pp. 257–264. https://doi.org/10.1111/j.1751-1097.1996.tb03022.x

    Article  CAS  PubMed  Google Scholar 

  14. Frank, H.A. and Cogdell, R.J., Photochemistry and function of carotenoids in bacteria, in The Photochemistry of Carotenoids, Frank, H.A., Young, A.J., Britton, G., and Cogdell, R.J., Eds., Dordrecht, Kluwer Academic, 1993, pp. 36–69.

    Google Scholar 

  15. Freer, A., Prince, S., Sauer, K., Papiz, M., Hawthornthwaite-Lawless, A., McDermott, G., Cogdell, R., and Isaacs, N.W., Pigment–pigment interactions and energy transfer in the antenna complex of the photosynthetic bacterium Rhodopseudomonas acidophila, Structure, 1996, vol. 4, pp. 449–462.

    Article  CAS  PubMed  Google Scholar 

  16. Gabrielsen, M., Gardiner, A.T., and Cogdell, R.J., Peripheral complexes of purple bacteria, in The Purple Phototrophic Bacteria, 2009, vol. 28, pp. 135–153.

  17. Griffiths, M., Sistrom, W., Cohen-Bazire, G., and Stanier, R., Functions of carotenoids in photosynthesis, Nature, 1955, vol. 176, pp. 1211–1215.

    Article  CAS  PubMed  Google Scholar 

  18. Klenina, I.B., Makhneva, Z.K., Moskalenko, A.A., and Proskuryakov, I.I., Selective excitation of carotenoids of the Allochromatium vinosum light-harvesting LH2 complexes leads to oxidation of bacteriochlorophyll, Biochemistry (Moscow), 2022, vol. 87, no. 10, pp. 1130–1137. https://doi.org/10.1134/S0006297922100066

    Article  CAS  PubMed  Google Scholar 

  19. Kondratyeva, Ye.N., Fotosinteziruyushchie bakterii i bakterial’nyi fotosintez (Photosynthetic Bacteria and Bactertial Photosynthesis), Moscow: Mos. Gos. Univ., 1972.

  20. Krasnovskii, A.A., Photoluminescence of singlet oxygen in solutions of the chlorophylls and pheophytins, Biophysics, 1977, vol. 22, no. 5, pp. 960–962.

    Google Scholar 

  21. Krasnovsky, A.A., Jr., Benditkis, A.S., and Kozlov, A.S., Kinetic measurements of singlet oxygen phosphorescence in the solvents lacking hydrogen atoms using the method of time resolved photon counting, Biochemistry (Moscow), 2019, vol. 84, pp. 153–163.

    CAS  PubMed  Google Scholar 

  22. Krasnovsky, A.A., Jr., Photoluminescence of singlet oxygen in pigment solutions, Photochem. Photobiol., 1979, vol. 29, no. 1, pp. 960–962. https://doi.org/10.1111/j.1751-1097.1979.tb09255.x

    Article  Google Scholar 

  23. Leiger, K., Linnanto, J.M., Rätsep, M., Timpmann, K., Ashikhmin, A.A., Moskalenko, A.A., Fufina, T.Y., Gabdulkhakov, A.G., and Freiberg, A., Controlling photosynthetic excitons by selective pigment photooxidation, J. Phys. Chem. B, 2019, vol. 123, pp. 29−38.

    Article  CAS  PubMed  Google Scholar 

  24. Löhner, A., Carey, A.M., Hacking, K., Picken, N., Kelly, S., Cogdell, R., and Köhler, J., The origin of the split B800 absorption peak in the LH2 complexes from Allochromatium vinosum, Photosynth. Res., 2015, vol. 123, pp. 23–31.

    Article  PubMed  Google Scholar 

  25. Makhneva, Z., Bolshakov, M., and Moskalenko, A., Heterogeneity of carotenoid content and composition in LH2 of the purple sulphur bacterium Allochromatium minutissimum grown under carotenoid-biosynthesis inhibition, Photosynth. Res., 2008, vol. 98, pp. 633–641.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Makhneva, Z.K., Ashikhmin, A.A., Bolshakov, M.A., and Moskalenko, A.A., 3-Acetyl-chlorophyll formation in light-harvesting complexes of purple bacteria by chemical oxidation, Biochemistry (Moscow), 2016, vol. 81, no. 2, pp. 176–186.

    CAS  PubMed  Google Scholar 

  28. Makhneva, Z.K., Ashikhmin, A.A., Bolshakov, M.A., and Moskalenko, A.A., Bacteriochlorophyll interaction with singlet oxygen in membranes of purple photosynthetic bacteria: does the protective function of carotenoids exist?, Doklady Biochem. Biophys., 2019a, vol. 486, pp. 216–219. https://doi.org/10.1134/S1607672919030141

    Article  CAS  Google Scholar 

  29. Makhneva, Z.K., Ashikhmin, A.A., Bolshakov, M.A., and Moskalenko, A.A., Carotenoids are probably involved in singlet oxygen generation in the membranes of purple photosynthetic bacteria under light irradiation, Microbiology (Moscow), 2020, vol. 89, no. 2, pp. 164–173.

    Article  CAS  Google Scholar 

  30. Makhneva, Z.K., Ashikhmin, A.A., Bolshakov, M.A., and Moskalenko, A.A., Quenchers protect BChl850 from action of singlet oxygen in the membranes of a sulfur photosynthetic bacterium Allochromatium vinosum strain MSU, Microbiology (Moscow), 2019b, vol. 88, no. 1, pp. 79–86.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Makhneva, Z.K., Erokhin, Yu.E., and Moskalenko, A.A., Carotenoid-photosensitized oxidation of bacteriochlorophyll dimers in light-harvesting complexes B800−850 in Allochromatium minutissimum cells, Doklady Biochem. Biophys., 2007, vol. 416, nos. 1−6, pp. 256−259. https://doi.org/10.1134/S1607672907050080

    Article  Google Scholar 

  33. Makhneva, Z.K., Smolova, T.N., Bolshakov, M.A., and Moskalenko, A.A., LH2 complex from sulfur bacteria Allochromatium vinosum—natural singlet oxygen sensor, Biochemistry (Moscow), 2022, vol. 87, pp. 1159–1168. https://doi.org/10.1134/S0006297922100091

  34. Moskalenko, A.A. and Erokhin, Yu.E., Isolation of pigment-lipoprotein complexes from purple bacteria by pre-parative polyacrylamide gel electrophoresis, Mikrobiologiya, 1974, vol. 43, pp. 654–657.

    CAS  Google Scholar 

  35. Moskalenko, A.A. and Karapetyan, N.V., Structural role of carotenoids in photosynthetic membranes, Z. Naturforsch., 1996, vol. 51, pp. 763–771.

    Article  CAS  Google Scholar 

  36. Moskalenko, A.A., Investigation of pigment-lipoprotein complexes from Chromatium minutissimum, Cand. Sci. (B-iol.) Dissertation, Pushchino, 1974.

  37. Moskalenko, A.A., Kuznetsova, N.Yu., and Erokhin, Yu.E., Isolation, spectral and photochemical characteristics of three types of pigment-protein complexes from Chromatium with suppressed carotenoid synthesis, DAN SSSR, 1983, no. 269, pp. 1248–1251.

  38. Moskalenko, A.A., Makhneva, Z.K., Fiedor, L., and Scheer, H., Effects of carotenoid inhibition on the photosynthetic RC–LH1 complex in purple sulphur bacterium Thiorhodospira sibirica, Photosynth. Res., 2005, vol. 86, pp. 71–80. https://doi.org/10.1007/s11120-005-4473-9

    Article  CAS  PubMed  Google Scholar 

  39. Papiz, M.Z., Prince, S.M., Howard, T., Cogdell, R.J., and Isaacs, N.W., The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 E resolution and 100K: new structural features and functionaly relevant motions, Mol. Biol., 2003, vol. 326, pp. 1523–1538.

    Article  CAS  Google Scholar 

  40. Polívka, T. and Frank, H.A., Molecular factors controlling photosynthetic light harvesting by carotenoids, Acc. Chem. Res., 2010, vol. 43, no. 8, pp. 1125–34. https://doi.org/10.1021/ar100030m

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Prince, S.M., Howard, T.D., Myles, D.A., Wilkinson, C., Papiz, M.Z., Freer, A.A., Cogdell, R.J., and Isaacs, N.W., Detergent structure in crystals of the integral membrane light-harvesting complex LH2 from Rhodopseudomonas acidophila strain 10050, J. Mol. Biol., 2003, vol. 326, pp. 307–315.

    Article  CAS  PubMed  Google Scholar 

  42. Prince, S.M., Papiz, M.Z., Freer, A.A., McDermott, G., Hawthornthwaite-Lawless, A.M., Cogdell, R.J., and Isaacs, N.W., Apoprotein structure in the LH2 complex from Rhodopseudomonas acidophila strain 10050: modular assembly and protein pigment interactions, J. Mol. Biol., 1997, vol. 268, pp. 412–423.

    Article  CAS  PubMed  Google Scholar 

  43. Toropygina, O.A., Makhneva, Z.K., and Moskalenko, A.A., Reconstitution of carotenoids into the light-harvesting complex B800–850 of Chromatium minutissimum, Biochemistry (Moscow), 2003a, vol. 68, pp. 901–911. https://doi.org/10.1023/A:1025755116593

    Article  CAS  PubMed  Google Scholar 

  44. Uragami, C., Sato, H., Yukihira, N., Fujiwara, M., and Kosumi, D., Photoprotective mechanisms in the core LH1 antenna pigment-protein complex from the purple photosynthetic bacterium, Rhodospirillum rubrum, J. Photochem. Photobiol. A: Chemistry, 2020, vol. 400, p. 112628. https://doi.org/10.1016/j.jphotochem.2020.112628

    Article  CAS  Google Scholar 

Download references

Funding

The work was carried out in terms of the State Assignment of the Puschino Science Center for Biological Research of the Russian Academy of Sciences no. 122041100204-3.

Author information

Authors and Affiliations

  1. Institute of Basic Biological Problems, Pushchino Scientific Center for Biological Research, Russian Academy of Sciences, 142290, Pushchino, Russia

    Z. K. Makhneva, M. A. Bolshakov, A. A. Ashikhmin & A. A. Moskalenko

Authors
  1. Z. K. Makhneva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Bolshakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Ashikhmin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. A. Moskalenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ААМ, conceptualization, supervision, text and picture preparation; ZKM, experimental research, text editing, and research result discussion; ААА, rhodopin isolation and text editing; MAB, LH2 complex isolation and the article’s final editing for publication.

Corresponding author

Correspondence to A. A. Moskalenko.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflict of interests.

Additional information

Translated by A. Oleskin

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Makhneva, Z.K., Bolshakov, M.A., Ashikhmin, A.A. et al. Rhodopin Incorporated into the Allochromatium vinosum LH2 Complex Is Able to Generate Singlet Oxygen under Illumination. Microbiology 93, 305–313 (2024). https://doi.org/10.1134/S0026261724604731

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261724604731

Keywords:

Search

Navigation