RAS BiologyБиохимия Biochemistry

  • ISSN (Print) 0320-9725
  • ISSN (Online) 3034-5294

CATIONIC ANTISEPTICS DISRUPT THE FUNCTIONING OF THE ELECTRON-TRANSPORT CHAIN AT THE ACCEPTOR SITE IN THE PHOTOSYNTHETIC REACTION CENTRES OF THE PURPLE BACTERIUM Cereibacter sphaeroides

PII
S30345294S0320972525070067-1
DOI
10.7868/S3034529425070067
Publication type
Article
Status
Published
Authors
Volume/ Edition
Volume 90 / Issue number 7
Pages
961-973
Abstract
Electrometric technique revealed that the cationic antiseptic octenidine reduces the generation of transmembrane electrical potential difference in the chromatophores of photosynthetic bacterium Cereibacter sphaeroides. This is also confirmed by measurements of electrochromic shifts of carotenoid absorption bands in chromatophores. In reaction centers (RCs) isolated from chromatophores in the absence of external electron donors and acceptors, the rate of recombination between photooxidized bacteriochlorophyll P and reduced secondary quinone acceptor Q, as measured by absorption changes in the near infrared region, was very weakly dependent on the presence of antiseptics, in contrast to the kinetics in the 400-600 nm spectral range, where absorption changes associated with the oxidation of P and the formation of semiquinone radicals Q and Q, as well as electrochromic shifts of the carotenoid and bacteriopheophytin RC absorption bands are observed. The addition of cationic antiseptics resulted in the appearance of absorption changes in this region with the formation time of about 100-200 ms and a decay time of about 3 s. In the series: picoxidine – chlorhexidine – octenidine – miramistin, the latter was the most effective. The maximum amplitude of such changes was observed in the absorption region of the semiquinone radical around 460 nm. When blocking the electron transfer from Q to Q by o-phenanthroline, the effect disappeared. It is suggested that cationic antiseptics stimulate protonation of Q with the formation of a neutral QH complex.
Keywords
катионные антисептики хроматофоры реакционные центры электрогенез электрометрический метод флеш-фотолиз
Date of publication
04.02.2026
Year of publication
2026
Number of purchasers
0
Views
97

References

  1. 1. Strakhovskaya, M. G., Lukashev, E. P., Korvatovskiy, B. N., Kholina, E. G., Seifullina, N. Kh., Knox, P. P., and Paschenko, V. Z. (2021) The effect of some antiseptic drugs on the energy transfer in chromatophore photosynthetic membranes of purple non-sulfur bacteria Rhodobacter sphaeroides, Photosyn. Res., 147, 197-209, https://doi.org/10.1007/s11120-020-00807-x.
  2. 2. Knox, P. P., Lukashev, E. P., Korvatovskiy, B. N., Strakhovskaya, M. G., Makhneva, Z. K., Bol’shakov, M. A., and Paschenko, V. Z. (2022) Disproportionate effect of cationic antiseptics on the quantum yield and fluorescence lifetime of bacteriochlorophyll molecules in the LH1-RC complex of R. rubrum chromatophores, Photosynth. Res., 153, 103-112, https://doi.org/10.1007/s11120-022-00909-8.
  3. 3. Paschenko, V. Z., Lukashev, E. P., Mamedov, M. D., Korvatovskiy, B. N., and Knox, P. P. (2023) Influence of the antiseptic octenidine on spectral characteristics and energy migration processes in photosystem II core complexes, Photosynth. Res., 155, 93-105, https://doi.org/10.1007/s11120-022-00972-1.
  4. 4. Paschenko, V. Z., Lukashev, E. P., Mamedov, M. D., Gvozdev, D. A., and Knox, P. P. (2024) Effect of cationic antiseptics on fluorescent characteristics and electron transfer in cyanobacterial photosystem I complexes, Photosynth. Res., 159, 241-251, https://doi.org/10.1007/s11120-024-01082-w.
  5. 5. Šlouf, V., Chábera, P., Olsen, J. D., Martin, E. C., Qiac, P., Huntec, C. N., and Polívka, T. (2012) Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties, Proc. Natl. Acad. Sci. USA, 109, 8570, https://doi.org/10.1073/pnas.1201413109.
  6. 6. Kirmaier, C., Holten, D., and Parson, W. W. (1985) Temperature and detection-wavelength dependence of the picosecond electron transfer kinetics measured in Rhodopseudomonas sphaeroides reaction centers – resolution of new spectral and kinetic components in the primary charge-separation process, Biochim. Biophys. Acta, 810, 33-48, https://doi.org/10.1016/0005-2728 (85)90204-X.
  7. 7. Holzapfel, W., Finkele, U., Kaiser, W., Oesterhelt, D., Scheer, H., Stilz, H. U., and Zinth, W. (1989) Observation of a bacteriochlorophyll anion radical during the primary charge separation in a reaction center, Chem. Phys. Lett., 160, 1, https://doi.org/10.1016/0009-2614 (89)87543-8.
  8. 8. Holzwarth, A. R., and Muller, M. G. (1996) Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides. A femtosecond transient absorption study, Biochemistry, 35, 11820-11831, https://doi.org/10.1021/bi9607012.
  9. 9. Camara-Artigas, A., Brune, D., and Allen, J. P. (2002) Interactions between lipids and bacterial reaction centers determined by protein crystallography, Proc. Natl. Acad. Sci. USA, 99, 11055-11060, https://doi.org/10.1073/pnas.162368399.
  10. 10. Milano, F., Dorogi, M., Szebenyi, K., Nagy, L., Maroti, P., Varo, G., Giotta, L., Agostiano, A., and Trotta, M. (2007) Enthalpy/entropy driven activation of the first interquinone electron transfer in bacterial photosynthetic reaction centers embedded in vesicles of physiologically important phospholipids, Bioelectrochemistry, 70, 18-22, https://doi.org/10.1016/j.bioelechem.2006.03.024.
  11. 11. Agostiano, A., Milano, F., and Trotta, M. (2005) Trapping of a long-living charge separated state of photosynthetic reaction centers in proteoliposomes of negatively charged phospholipids, Photosynth. Res., 83, 53-61, https://doi.org/10.1007/s11120-004-3197-6.
  12. 12. 2. Lavergne, J., Matthews, C., and Ginet, N. (1999) Electron and proton transfer on the acceptor side of the reaction center in chromatophores of Rhodobacter capsulatus: evidence for direct protonation of the semiquinone state of QB, Biochemistry, 38, 4542-4552, https://doi.org/10.1021/bi9827621.
  13. 13. Graige, M. S., Paddock, M. I., Feher, G., and Okamura, M. Y. (1999) Observation of the protonated semiquinone intermediate in isolated reaction centers from Rhodobacter sphaeroides: implications for the mechanism of electron and proton transfer in proteins, Biochemistry, 38, 11465-11473, https://doi.org/10.1021/bi990708u.
  14. 14. Woronowicz, K., Sha, D., Frese, R. N., Niederman, R. A. (2011) The accumulation of the light-harvesting 2 complex during remodeling of the Rhodobacter sphaeroides intracytoplasmic membrane results in a slowing of the electron transfer turnover rate of photochemical reaction centers, Biochemistry, 50, 4819-4829, https://doi.org/10.1021/bi101667e.
  15. 15. Clayton, R. K. (1966) Spectroscopic analysis of bacteriochlorophylls in vitro and in vivo, Photochem. Photobiol., 5, 669-677, https://doi.org/10.1111/j.1751-1097.1966.tb05813.x.
  16. 16. Захарова Н.И., Чурбанова И.Ю. (2000) Методы получения реакционных центров фотосинтезирующих пурпурных бактерий, Биохимия, 65, 181-193.
  17. 17. Drachev, L. A., Kaminskaya, O. P., Konstantinov, A. A., Mamedov, M. D., Samuilov, V. D., Semenov, A. Yu., and Skulachev, V. P. (1986) Effects of electron donors and acceptors on the kinetics of the photoelectric responses in Rhodospirillum rubrum and Rhodopseudomas sphaeroides chromatophores, Biochim. Biophys. Acta, 850, 1-9, https://doi.org/10.1016/0005-2728 (86)90002-2.
  18. 18. Drachev, L. A., Kaurov, B. S., Mamedov, M. D., Mulkidjanian, A. Ya., Semenov, A. Yu., Shinkarev, V. P., Skulachev, V. P., and Verkhovsky, M. I. (1989) Flash-induced electrogenic events in the photosynthetic reaction center and bc1 complexes of Rhodobacter sphaeroides chromatophores, Biochim. Biophys. Acta, 973, 189-197, https://doi.org/10.1016/S0005-2728 (89)80421-9.
  19. 19. Jackson, J. B., and Crofts, A. R. (1971) The kinetics of light induced carotenoid changes in Rhodopseudomonas sphaeroides and their relation to electrical field generation across the chromatophore membrane, Eur. J. Biochem., 18, 120-130, https://doi.org/10.1111/j.1432-1033.1971.tb01222.x.
  20. 20. Drachev, L. A., Kaulen, A. D., Semenov, A. Y., Severina, I. I., and Skulachev, V. P. (1979) Lipid-impregnated filters as a tool for studying the electric current-generating proteins, Anal. Biochem., 96, 250-262, https://doi.org/10.1016/0003-2697 (79)90580-3.
  21. 21. Skulachev, V. P. (1982) A single turnover study of photoelectric current-generating proteins, Methods Enzymol., 88, 35-45, https://doi.org/10.1016/0076-6879 (82)88010-5.
  22. 22. Jackson, J. B., and Crofts, A. R. (1969) Bromothymol blue and bromocresol purple as indicators of pH changes in chromatophores of Rhodospirillum rubrum, Eur. J. Biochem., 10, 226-237, https://doi.org/10.1111/j.1432-1033.1969. tb00678.x.
  23. 23. Witt, H. T. (1979) Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field, Biochim. Biophys. Acta, 505, 355-427, https://doi.org/10.1016/0304-4173 (79)90008-9.
  24. 24. Malferrari, M., Malferrari, D., Francia, F., Galletti, P., Tagliavini, E., and Venturoli, G. (2015) Ionic liquids effects on the permeability of photosynthetic membranes probed by the electrochromic shift of endogenous carotenoids, Biochim. Biophys. Acta, 1848, 2898-2909, https://doi.org/10.1016/j.bbamem.2015.09.006.
  25. 25. Saphon, S., Jackson, J. B., and Witt, H. T. (1975) Electrical potential changes, H+ translocation and phosphorylation induced by short flash excitation in Rhodopseudomonas sphaeroides chromatophores, Biochim. Biophys. Acta, 408, 67-82, https://doi.org/10.1016/0005-2728 (75)90159-0.
  26. 26. Gibasiewicz, K., and Pajzderska, M. (2008) Primary radical pair P+H– lifetime in Rhodobacter sphaeroides with blocked electron transfer to QA. Effect of o-phenanthroline, J. Phys. Chem. B, 112, 1858-1865, https://doi.org/10.1021/jp075184j.
  27. 27. Okamura, M. Y., Feher, G., and Nelson, N. (1982) Reaction centers, in Photosynthesis Energy conversion by plants and bacteria, (Govindjee, ed.) Vol. 1, Acad. Press, N-Y – London – Paris, pp. 197-254.
  28. 28. Li, J., Gilroy, D., Tiede, D. M., and Gunner, M. R. (1998) Kinetic phases in the electron transfer from P+QA–QB to P+QAQB– and the associated processes in Rhodobacter sphaeroides R-26 reaction centers, Biochemistry, 37, 2818-2829, https://doi.org/10.1021/bi971699x.
  29. 29. Pingale, S. S., Ware, A. P., and Gadre, S. R. (2018) Unveiling electrostatic portraits of quinones in reduction and protonation states, J. Chem. Sci., 130, 50, https://doi.org/10.1007/s12039-018-1450-3.
  30. 30. Takahashi, E., and Wraight, C. A. (1996) Potentiation of proton transfer function by electrostatic interactions in photosynthetic reaction centers from Rhodobacter sphaeroides: first results from site-directed mutation of the H subunit, Proc. Natl. Acad. Sci. USA, 93, 2640-2645, https://doi.org/10.1073/pnas.93.7.2640.
  31. 31. Gunner, M. R., Madeo, J., and Zhu, Z. (2008) Modification of quinone electrochemistry by the proteins in the biological electron transfer chains: examples from photosynthetic reaction centers, J. Bioenerg. Biomembr., 40, 509-519, https://doi.org/10.1007/s10863-008-9179-1.
  32. 32. Okamura, M. Y., Paddock, M. L., Graige, M. S., and Feher, G. (2000) Proton and electron transfer in bacterial reaction centers, Biochim. Biophys. Acta, 1458, 148-163, https://doi.org/10.1016/S0005-2728 (00)00065-7.
  33. 33. Scheiner, S., and Hillenbrand, E. A. (1985) Modification of pK values caused by change in H-bond geometry, Proc. Natl. Acad. Sci. USA, 82, 2741-2745, https://doi.org/10.1073/pnas.82.9.274.
  34. 34. Nagy, L., Milano, F., Dorogi, M., Agostiano, A., Laczkó, G., Szebényi, K., Váró, G., Trotta, M., and Maróti, P. (2004) Protein/lipid interaction in the bacterial photosynthetic reaction center: phosphatidylcholine and phosphatidylglycerol modify the free energy levels of the quinones, Biochemistry, 43, 12913-12923, https://doi.org/10.1021/bi0489356.
  35. 35. Chernysheva, M. G., Shnitko, A. V., Skrabkova, H. S., and Badun, G. A. (2021) Peculiarities of alkylamidopropyldimethylbenzylammonium (miramistin) in the relationship to lysozyme in comparison with quaternary ammonium surfactants: coadsorption at the interfaces, enzymatic activity and molecular docking, Colloids Surf. A, 629, 127503, https://doi.org/10.1016/j.colsurfa.2021.127503.
  36. 36. Rzycki, M., Drabik, D., Szostak-Paluch, K., Hanus-Lorenz, B., and Kraszewski, S. (2021) Unraveling the mechanism of octenidine and chlorhexidine on membranes: does electrostatics matter? Biophys. J., 120, 3392-3408, https://doi.org/10.1016/j.bpj.2021.06.027.
  37. 37. Malanovic, N., Ön, A., Pabst, G., Zellner, A., and Lohner, K. (2020) Octenidine: novel insights into the detailed killing mechanism of Gram-negative bacteria at a cellular and molecular level, Int. J. Antimicrob. Agents, 56, 10646, https://doi.org/10.1016/j.ijantimicag.2020.106146.
  38. 38. Osmanov, A., Farooq, Z., Richardson, M. D., and Denning, D. W. (2020) The antiseptic miramistin: a review of its comparative in vitro and clinical activity, FEMS Microbiol. Rev., 44, 399-417, https://doi.org/10.1093/femsre/fuaa012.
QR
Translate

Indexing

Scopus

Scopus

Scopus

Crossref

Scopus

Higher Attestation Commission

At the Ministry of Education and Science of the Russian Federation

Scopus

Scientific Electronic Library