Skip to main content
Log in

Carotenoids are Probably Involved in Singlet Oxygen Generation in the Membranes of Purple Photosynthetic Bacteria under Light Irradiation

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

Abstract

The possibility of singlet oxygen generation in five species of photosynthetic bacteria under irradiation with light was studied using the Singlet Oxygen Sensor Green (SOSG) dye that, when singlet oxygen is bound, is transformed into a fluorescent endoperoxide form. Irradiation was carried out using light of different spectral composition: red (absorption of bacteriochlorophyll, BChl) and white (absorption of BChl and carotenoids). No singlet oxygen generation was detected under red light irradiation, which indicated that BChl was not involved in this process. Under white light, as the irradiation time increased, an increase in SOSG fluorescence was recorded in the membranes of four bacterial species: Allochromatium vinosum MSU, Rhodobacter sphaeroides G1C, Rba. blasticus K-1 and Rhodopseudomonas faecalis. In Rba. sphaeroides, no increase in SOSG fluorescence was observed. It is assumed that in the white light this process occurs due to the pigments that absorb in the blue-green region of the spectrum, i.e. carotenoids with 8‒11 conjugated double bonds (neurosporene, spheroidene, lycopene, and rhodopin). Similar to Trolox, SOSG may slow down the bleaching process of BChl850 in the membranes of Alc. vinosum strain MSU and may therefore effectively perform the role of a singlet oxygen trap.

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.

Institutional subscriptions

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

Similar content being viewed by others

REFERENCES

  1. Arellano, J.B., Yousef, Y.A., Melø, T.B., Mahamad, S.B., Cogdell, R.J., and Naqvi K.R., Formation and geminate quenching of singlet oxygen in purple bacterial reaction center, J. Photochem. Photobiol., 2007, vol. 87, pp. 105–112.

    Article  CAS  Google Scholar 

  2. 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, Dokl. Biochem. Biophys., 2018, vol. 483, pp. 321–325.

    Article  CAS  Google Scholar 

  3. Bancirova, M., Sodium azide as a specific quencher of singlet oxygen during chemiluminescent detection by luminol and Cypridina luciferin analogues, Luminescence. 2011, vol. 26, pp. 685–688.

    Article  CAS  Google Scholar 

  4. Berghoff, B.A., Glaeser, J., Nuss, A.M., Zobawa, M., Lottspeich, F., and Klug, G., Anoxygenic photosynthesis and photooxidative stress: a particular challenge for Roseobacter,Environ. Microbiol., 2011, vol. 13, pp. 775–791.

    Article  CAS  Google Scholar 

  5. Bol’shakov, M.A., Role of carotenoids in the process of in vivo bacteriochlorophyll photootxidation, Extended Abstract Cand. Sci. (Biol.) Dissertation, Pushchini, 2012.

  6. Bortolus, P. and Monti S., Physical quenching and chemical reaction of singlet molecular oxygen with Azo dyes, J. Organic. Chem., 1989, vol. 54, pp. 534–540.

    Article  CAS  Google Scholar 

  7. Chi, S.C., Mothersole, D.J., Dilbeck, P., Niedzwiedzki, D.M., Zhang, H., Qian, P., Vasilev, C., Grayson, K.J., Jakson, P.J., Martin, C.E., Ying, L., and Neil Hunter, C., Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway, Biochim. Biophys.Acta–Bioenergetics, 2015, vol. 1847, pp. 189–201.

    Article  CAS  Google Scholar 

  8. Cogdell, R.J., Gardiner, A.T., Roszak, A.W., Law, C.J., Southall, J., and Isaacs, N.W., Rings, ellipses and horseshoes: how purple bacteria harvest solar energy, Photosynth. Res., 2004, vol. 81, pp. 207–214.

    Article  CAS  Google Scholar 

  9. Cohen-Bazire, G., Sistrom, W.R., and Stanier, R.Y., Kinetic studies of pigment synthesis by non-sulfur purple bacteria, J. Cell. Comp. Physiol., 1957, vol. 49, pp. 25–68.

    Article  CAS  Google Scholar 

  10. Cong, H., Niedzwiedzki, D.M., Gibson, G.N., LaFountain, A.M., Kelsh, R.M., Gardiner, A.T., Cogdell, R.J., and Frank, H.A., Ultrafast time resolved carotenoid to-bacteriochlorophyll energy transfer in LH2 complexes from photosynthetic bacteria, J. Phys. Chem. B, 2008, vol. 112, pp. 10689–10703.

    Article  CAS  Google Scholar 

  11. Dilbeck, P.L., Tang, Q., Mothersole, D.J., Martin, E.C., Hunter, C.N., Bocian, D.F., Holten, D., and Niedzwiedzki, D.M., Quenching capabilities of long-chain carotenoids in light-harvesting-2 complexes from Rhodobacter sphaeroides with an engineered carotenoid synthesis pathway, J. Phys. Chem. B, 2016, vol. 120, pp. 5429–5443.

    Article  CAS  Google Scholar 

  12. Dworkin, M., Endogenous photosensitization in a carotenoidless mutant of Rhodopseudomonas spheroids,J. Gen. Physiol., 1958, vol. 41, pp. 1099–1112.

    Article  CAS  Google Scholar 

  13. Fatima, K., Masood, N., and Luqman, S., Quenching of singlet oxygen by natural and synthetic antioxidants and assessment of electronic UV/Visible absorption spectra for alleviating or enhancing the efficacy of photodynamic therapy, Biomed. Res. Ther., 2016, vol. 3, pp. 514–527.

    Article  Google Scholar 

  14. Foote, C.S., Chang, Y.C., and Denny, R.W., Chemistry of singlet oxygen. X. Carotenoid quenching parallels biological protection, J. Amer. Chem. Soc., 1970, vol. 92, pp. 5216–5218.

    Article  CAS  Google Scholar 

  15. Fraser, N.J., Hashimoto, H., and Cogdell, R.J., Carotenoids and bacterial photosynthesis: the story so far..., Photosynth. Res., 2001, vol. 70, pp. 249–256.

    Article  CAS  Google Scholar 

  16. Gabrielsen, M., Gardiner, A.T., and Cogdell, R.J., Peripheral complexes of purple bacteria, in The Purple Phototrophic Bacteria, Hunter C.N., Daldal F., Thurnauer, M.C., and Beatty, J.T., Eds., 2009, Ch. 8, pp. 135–153.

    Google Scholar 

  17. Glaeser, J. and Klug, G., Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes, Microbiology (SGM), 2005, vol. 151, pp. 1927–1938.

    Article  CAS  Google Scholar 

  18. Griffith, M., Sistrom, W.R., Cohen-Bazire, G., and Stanier, R.Y., Functions of carotenoids in photosynthesis, Nature, 1955, vol. 176, pp. 1211–1214.

    Article  Google Scholar 

  19. Gutiérrez, I., Criado, S., Bertolotti, S., Norman, A., and Garcia, N., Dark and photoinduced interactions between trolox, a polar-solvent-soluble model for vitamin E, and riboflavin, J. Photochem. Photobiol., 2001, vol. 62, pp. 133–139.

    Article  Google Scholar 

  20. Hashimoto, H., Uragami, C., Yukihira, N., Gardiner, A.T., and Cogdell, R.J., Understanding/unravelling carotenoid excited singlet states, J. R. Soc. Interface, 2018, vol. 15, article 20180026. https://doi.org/10.1098/rsif.2018.0026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hoff, A.J. and Deisenhofer, J., Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of purple bacteria, Physics Rep., 1997, vol. 287, pp. l–247.

    Article  Google Scholar 

  22. Kim, S., Fujitsuka, M., and Majima, T., Photochemistry of singlet oxygen sensor green, J. Phys. Chem. B, 2013, vol. 117, pp. 13985–13992.

    Article  CAS  Google Scholar 

  23. Kochevar, I.E., Singlet oxygen signaling: from intimate to global, Sci. STKE, 2004, vol. 221. pe7. https://doi.org/10.1126/stke.2212004pe7

    Article  Google Scholar 

  24. Koh, E. and Fluhr, R., Singlet oxygen detection in biological systems: uses and limitations, Plant Signal. Behav., 2016, vol. 11, article e1192742. https://doi.org/10.1080/15592324.2016.1192742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

  26. Kraljic, I. and Mohsni, S.El., A new method for the detection of singlet oxygen in aqueous solutions, Photochem. Photobiol., 1978, vol. 28, pp. 577–581.

    Article  CAS  Google Scholar 

  27. Krieger-Liszkay, A. and Trebst, A., Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction centre, J. Exp. Bot., 2006, vol. 57, pp. 1677–1684.

    Article  CAS  Google Scholar 

  28. Limantarai, L., Koehler, P., Wilhelm, B., Robert, J., Porra, R.J., and Scheer, H., Photostability of bacteriochlorophyll a and derivatives: potential sensitizers for photodynamic tumor therapy, Photochem. Photobiol., 2006, vol. 82, pp. 770–780.

    Article  Google Scholar 

  29. 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, pp. 176–186.

    CAS  PubMed  Google Scholar 

  30. Makhneva, Z.K., Ashikhmin, A.A., Bolshakov, M.A., and Moskalenko, A.A., Protection of BChl850 from action of singlet oxygen in the membranes of sulfur photosynthetic bacterium Allochromatium vinosum strain MSU by quenchers, Microbiology (Moscow), 2019, vol. 88, pp. 79–86.

    Article  CAS  Google Scholar 

  31. Makhneva, Z.K., Bolshakov, M.A., Ashikhmin, A.A., Erokhin, Y.E., and Moskalenko, A.A., Influence of blue light on the structure stability of antenna complexes from Allochromatium minutissimum with different content of carotenoids, Biochemistry (Moscow) Supplement. Series A:Membrane and Cell Biology, 2009, vol. 3, pp. 123–127.

    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, Dokl. Biochem. Biophys., 2007, vol. 416, pp. 256–259.

    Article  Google Scholar 

  33. 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.

    Article  CAS  Google Scholar 

  34. Moskalenko, A.A., Pigment-protein complexes and their interaction in the structures of the bacterial and plant photosynthesis apparatus, Doctoral (Biol.) Dissertation, Pushchino, 1993.

  35. Nuyanzina-Boldareva, E.N., Kalashnikov, A.M., Gaisin, V.A., Sukhacheva, M.V., Kuznetsov, B.B., and Gorlenko, V.M., Characterization of a new strain of a purple nonsulfur bacterium from a thermal spring, Microbiology (Moscow), 2014, vol. 83, pp. 39–46.

    Article  CAS  Google Scholar 

  36. Ohara, K., Kikuchi, K., Origuchi, T., and Nagaoka, S., Singlet oxygen quenching by trolox C in aqueous micelle solutions, J. Photochem. Photobiol. B., 2009, vol. 97, pp. 132–137.

    Article  CAS  Google Scholar 

  37. Prasad, A., Sedlářová, M., and Pospíšil, P., Singlet oxygen imaging using fluorescent probe Singlet Oxygen Sensor Green in photosynthetic organisms, Sci. Rep., 2018, vol. 8, article 13685. https://doi.org/10.1038/s41598-018-31638-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Redmond, R.W. and Gamlin, J.N., A compilation of singlet oxygen yields from biologically relevant molecules, Photochem. Photobiol., 1999, vol. 70, pp. 391–475.

    Article  CAS  Google Scholar 

  39. Uchoa, A.F., Knox, P.P., Turchielle, R., Seifullina, N.Kh., and Baptista, S.M., Singlet oxygen generation in the reaction centers of Rhodobacter sphaeroides,Eur. Biophys., 2008, vol. 37, pp. 843–850.

    Article  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to Professor V.M. Gorlenko (Winogradsky Institute of Microbiology, FRC of Biotechnology, Russian Academy of Sciences, Moscow) for providing Rba. blasticus K-1 and Rps. faecalis cultures; to Professor S. Takaichi (Nippon Medical School, Tokyo, Japan) for providing the Rba.sphaeroides G1C culture, as well as to Z.A. Zhuravleva (IBBP, Russian Academy of Sciences) for assistance in growing bacteria and obtaining membranes.

Funding

This work was supported in part by the Russian Foundation for Basic Research (projects nos. 18-04-00684_a; 18-34-00416_mol_a; 17-04-00929_a). The results presented in Figs. 1–3 were obtained in the framework of the state assignment no. AAAA-A17-117030110140-5.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. A. Moskalenko.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Babchenko

Accepted abbreviations: BChl, bacteriochlorophyll; Crt, carotenoid; LH, light-harvesting; RC, reaction center; Alc.,Allochromatium; Rba.,Rhodobacter; Rps., Rhodopseudomonas;Rsb., Roseobacter; SOSG, Singlet Oxygen Sensor Green.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Makhneva, Z.K., Ashikhmin, A.A., Bolshakov, M.A. et al. Carotenoids are Probably Involved in Singlet Oxygen Generation in the Membranes of Purple Photosynthetic Bacteria under Light Irradiation. Microbiology 89, 164–173 (2020). https://doi.org/10.1134/S0026261720010099

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261720010099

Keywords:

Navigation