Abstract
In this minireview, we consider the methods of measurements of the light-induced steady state transmembrane electric potential (Δψ) generation by photosynthetic systems, e.g. photosystem I (PS I). The microelectrode technique and the detection of electrochromic bandshifts of carotenoid pigments are most appropriate for Δψ measurements in situ and in vivo. Direct electrometrical method and Δψ measurements in the photovoltaic system based on membrane filter (MF) sandwiched between semiconductor indium tin oxide electrodes (ITO) are suitable for studies of isolated pigment-protein complexes and small natural vesicles—chromatophores. In the presence of trehalose, ITO|PS I-MF|ITO system allows to keep a steady state level of ∆ψ after 1 h of illumination. According to preliminary experiments, this system is capable of providing steady state light-induced ∆ψ after several months of storage in the dark at room temperature under controlled humidity in the presence of trehalose. The long-term generation of light-induced ∆ψ in relatively simple system may serve as a source of the solar-to-electric energy conversion.
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References
Bailleul B, Cardol P, Breyton C, Finazzi G (2010) Electrochromism: a useful probe to study algal photosynthesis. Photosynth Res 106(1–2):179–189. https://doi.org/10.1007/S11120-010-9579-Z
Bulychev AA, Andrianov VK, Kurella GA, Litvin FF (1976) Photoinduction kinetics of electrical potential in a single chloroplast as studied with micro-electrode technique. BBA - Bioenergetics 430(2):336–351. https://doi.org/10.1016/0005-2728(76)90090-6
Bulychev AA, Andrianov VK, Kurella GA, & Litvin FF (1972). Micro-electrode measurements of the transmembrane potential of chloroplasts and its photoinduced changes. Nature 1972 236:5343, 236(5343), 175–177. https://doi.org/10.1038/236175a0
Cherubin A, Destefanis L, Bovi M, Perozeni F, Bargigia I, De La Cruz Valbuena G et al (2019) Encapsulation of photosystem i in organic microparticles increases its photochemical activity and stability for ex vivo photocatalysis. ACS Sustain Chem Eng 7(12):10435–10444. https://doi.org/10.1021/ACSSUSCHEMENG.9B00738/SUPPL_FILE/SC9B00738_SI_001.PDF
Cruz JA, Sacksteder CA, Kanazawa A, & Kramer DM (2001). Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by ionic strength. Biochemistry, 40(5), 1226–1237. https://doi.org/10.1021/BI0018741
Drachev LA, Frolov VN, Kaulen AD, Kondrashin AA, Samuilov VD, Semenov AY, Skulachev VP (1976) Generation of electric current by chromatophores of Rhodospirillum rubrum and reconstitution of electrogenic function in subchromatophore pigment-protein complexes. Biochimica et Biophysica Acta (BBA) - Bioenergetics 440(3):637–660. https://doi.org/10.1016/0005-2728(76)90048-7
Drachev LA, Kaulen AD, Semenov AY, Severina II, Skulachev VP (1979) Lipid-impregnated filters as a tool for studying the electric current-generating proteins. Anal Biochem 96(1):250–262. https://doi.org/10.1016/0003-2697(79)90580-3
Drachev LA, Semenov AY, Skulachev VP, Smirnova IA, Chamorovsky SK, Kononenko AA et al (1981) Fast stages of photoelectric processes in biological membranes: III. Bacterial photosynthetic redox system. Eur J Biochem 117(3):483–489. https://doi.org/10.1111/j.1432-1033.1981.tb06363.x
Drachev LA, Jasaitis AA, Kaulen AD, Kondrashin AA, Liberman EA, Nemecek IB, et al. (1974). Direct measurement of electric current generation by cytochrome oxidase, H+-ATPase and bacteriorhodopsin. Nature 1974 249:5455, 249(5455), 321–324. https://doi.org/10.1038/249321a0
Efrati A, Tel-Vered R, Michaeli D, Nechushtai R, Willner I (2013) Cytochrome c-coupled photosystem I and photosystem II (PSI/PSII) photo-bioelectrochemical cells. Energy Environ Sci 6(10):2950–2956. https://doi.org/10.1039/C3EE41568F
Fernandez O, Bé Thencourt L, Quero A, Sangwan RS, Clé Ment C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417. https://doi.org/10.1016/j.tplants.2010.04.004
Fu H-Y, Picot D, Choquet Y, Longatte G, Sayegh A, Delacotte J et al (2017) Redesigning the QA binding site of Photosystem II allows reduction of exogenous quinones. Nat Commun 8(1):15274. https://doi.org/10.1038/ncomms15274
Gorka M, Cherepanov DA, Semenov AY, Golbeck JH (2020) Control of electron transfer by protein dynamics in photosynthetic reaction centers. Crit Rev Biochem Mol Biol 55(5):425–468. https://doi.org/10.1080/10409238.2020.1810623
Jackson JB, Crofts AR (1969) The high energy state in chromatophores from Rhodopseudomonas spheroides. FEBS Lett 4(3):185–189. https://doi.org/10.1016/0014-5793(69)80230-9
Joliot P, Joliot A (1989) Characterization of linear and quadratic electrochromic probes in Chlorella sorokiniana and Chlamydomonas reinhardtii. Biochimica et Biophysica Acta (BBA) - Bioenergetics 975(3):355–360. https://doi.org/10.1016/S0005-2728(89)80343-3
Junge W, Witt HT (1968) On the ion transport system of photosynthesis — investigations on a molecular level. Z NATURFORSCH B J Chem Sci 23(2):244–254. https://doi.org/10.1515/ZNB-1968-0222
Kato M, Cardona T, Rutherford AW, Reisner E (2012) Photoelectrochemical water oxidation with photosystem II integrated in a mesoporous indium-tin oxide electrode. J Am Chem Soc 134(20):8332–8335. https://doi.org/10.1021/ja301488d
Kato M, Cardona T, Rutherford AW, Reisner E (2013) Covalent immobilization of oriented photosystem II on a nanostructured electrode for solar water oxidation. J Am Chem Soc 135(29):10610–10613. https://doi.org/10.1021/JA404699H
Kato M, Zhang JZ, Paul N, Reisner E (2014). Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chemical Society Reviews. Royal Society of Chemistry. https://doi.org/10.1039/c4cs00031e
Kurashov V, Gorka M, Milanovsky GE, Johnson TW, Cherepanov DA, Semenov AY, Golbeck JH (2018) Critical evaluation of electron transfer kinetics in P700–FA/FB, P700–FX, and P700–A1 Photosystem I core complexes in liquid and in trehalose glass. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1859(12):1288–1301. https://doi.org/10.1016/j.bbabio.2018.09.367
Li Z, Wang W, Ding C, Wang Z, Liao S, Li C (2017) Biomimetic electron transport via multiredox shuttles from photosystem II to a photoelectrochemical cell for solar water splitting. Energy Environ Sci 10(3):765–771. https://doi.org/10.1039/c6ee03401b
Liberman EA, Skulachev VP (1970) Conversion of biomembrane-produced energy into electric form. IV. General discussion. Biochimica et Biophysica Acta (BBA) - Bioenergetics 216(1):30–42. https://doi.org/10.1016/0005-2728(70)90156-8
Malferrari M, Savitsky A, Mamedov MD, Milanovsky GE, Lubitz W, Möbius K et al (2016) Trehalose matrix effects on charge-recombination kinetics in Photosystem I of oxygenic photosynthesis at different dehydration levels. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1857(9):1440–1454. https://doi.org/10.1016/j.bbabio.2016.05.001
Mamedov MD, Nosikova ES, Vitukhnovskaya LA, Zaspa AA, Semenov AY (2017) Influence of the disaccharide trehalose on the oxidizing side of photosystem II. Photosynthetica 2018 56:1 56(1):236–243. https://doi.org/10.1007/S11099-017-0750-Z
Mamedov MD, Milanovsky GE, Malferrari M, Vitukhnovskaya LA, Francia F, Semenov AY, Venturoli G (2021) Trehalose matrix effects on electron transfer in Mn-depleted protein-pigment complexes of Photosystem II. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1862(7):148413. https://doi.org/10.1016/j.bbabio.2021.148413
Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191(4784):144–148. https://doi.org/10.1038/191144a0
Möbius K, Savitsky A, Malferrari M, Francia F, Mamedov MD, Semenov AY et al (2020) Soft dynamic confinement of membrane proteins by dehydrated trehalose matrices: high-field EPR and fast-laser studies. Appl Magn Reson 51(9–10):773–850. https://doi.org/10.1007/S00723-020-01240-Y
Musazade E, Voloshin R, Brady N, Mondal J, Atashova S, Zharmukhamedov SK, Huseynova I, Ramakrishna S, Najafpour MM, Shen JR, Bruce BD, Allakhverdiev SI (2018) Biohybrid solar cells: Fundamentals, progress, and challenges. J Photochem Photobiol C Photochem Rev 35:134–156. https://doi.org/10.1016/J.JPHOTOCHEMREV.2018.04.001
Ohtake S, Wang YJ (2011) Trehalose: current use and future applications. J Pharm Sci 100(6):2020–2053. https://doi.org/10.1002/JPS.22458
Remiš D, Bulychev AA, Kurella GA (1986) The electrical and chemical components of the protonmotive force in chloroplasts as measured with capillary and pH-sensitive microelectrodes. Biochimica et Biophysica Acta (BBA) - Bioenergetics 852(1):68–73. https://doi.org/10.1016/0005-2728(86)90057-5
Saboe PO, Conte E, Farell M, Bazan GC, Kumar M (2017). Biomimetic and bioinspired approaches for wiring enzymes to electrode interfaces. Energy and Environmental Science. Royal Society of Chemistry. https://doi.org/10.1039/c6ee02801b
Sokol KP, Robinson WE, Warnan J, Kornienko N, Nowaczyk MM, Ruff A et al (2018) Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase. Nature Energy 3(11):944–951. https://doi.org/10.1038/s41560-018-0232-y
Stieger KR, Feifel SC, Lokstein H, Hejazi M, Zouni A, Lisdat F (2016) Biohybrid architectures for efficient light-to-current conversion based on photosystem I within scalable 3D mesoporous electrodes. J Mater Chem A 4(43):17009–17017. https://doi.org/10.1039/C6TA07141D
Teodor AH, Bruce BD (2020) Putting photosystem I to work: truly green energy. Trends Biotechnol 38(12):1329–1342. https://doi.org/10.1016/J.TIBTECH.2020.04.004
Zaspa AA, Vitukhnovskaya LA, Mamedova AM, Semenov AY, Mamedov MD (2020) Photovoltage generation by photosystem II core complexes immobilized onto a Millipore filter on an indium tin oxide electrode. J Bioenerg Biomembr 52(6):495–504. https://doi.org/10.1007/S10863-020-09857-1
Zaspa A, Vitukhnovskaya L, Mamedova A, Allakhverdiev SI, Semenov A, Mamedov M (2022) Voltage generation by photosystem I complexes immobilized onto a millipore filter under continuous illumination. Int J Hydrogen Energy 47(22):11528–11538. https://doi.org/10.1016/j.ijhydene.2022.01.175
Zhang JZ, Reisner E (2020). Advancing photosystem II photoelectrochemistry for semi-artificial photosynthesis. Nature Reviews Chemistry. Nature Research. https://doi.org/10.1038/s41570-019-0149-4
Funding
This work was financially supported by RSF grant 22–23-20165 to L.V. This work was supported by Lomonosov Moscow State University Program of Development and FRCCP RAS state task (AAAA-A19-119012990175–9).
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Mamedov, M.D., Milanovsky, G.E., Vitukhnovskaya, L. et al. Measurements of the light-induced steady state electric potential generation by photosynthetic pigment-protein complexes. Biophys Rev 14, 933–939 (2022). https://doi.org/10.1007/s12551-022-00966-2
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DOI: https://doi.org/10.1007/s12551-022-00966-2