Effect of artificial redox mediators on the photoinduced oxygen reduction by photosystem I complexes

  • Anastasia Petrova
  • Mahir Mamedov
  • Boris Ivanov
  • Alexey Semenov
  • Marina Kozuleva
Original Article
  • 7 Downloads

Abstract

The peculiarities of interaction of cyanobacterial photosystem I with redox mediators 2,6-dichlorophenolindophenol (DCPIP) and N,N,N′,N′-tetramethyl-p-phenylenediamine (TMPD) were investigated. The higher donor efficiency of the reduced DCPIP form was demonstrated. The oxidized form of DCPIP was shown to be an efficient electron acceptor for terminal iron–sulfur cluster of photosystem I. Likewise methyl viologen, after one-electron reduction, DCPIP transfers an electron to the molecular oxygen. These results were discussed in terms of influence of these interactions on photosystem I reactions with the molecular oxygen and natural electron acceptors.

Keywords

Redox mediator Oxygen reduction Photosystem I Methyl viologen 2,6-Dichlorophenolindophenol N,N,N′,N′-tetramethyl-p-phenylenediamine Electron acceptor Midpoint potential 

Abbreviations

Asc

Ascorbate

β-DM

n-dodecyl-β-d-maltoside

Chl

Chlorophyll

Em

The midpoint potential

ET

Electron transfer

DCPIP

2,6-dichlorophenolindophenol

DCPIP(H)·

A semi-reduced form of DCPIP

DCPIPH2

The fully reduced form of DCPIP

DCPIPOX

The fully oxidized form of DCPIP

Km

The apparent Michaelis constant

MV

Methyl viologen

Pc

Plastocyanin

PS I, PS II

Photosystem I, photosystem II

RMV

The ratio of the rate of oxygen uptake in the presence of MV to the rate of oxygen uptake in the absence of MV

TMPD

N,N,N′,N′-tetramethyl-p-phenylenediamine

TMPD·+

A semi-oxidized form of TMPD

VO2

Rate of oxygen uptake in the absence of MV

VO2MV

Rate of oxygen uptake in the presence of MV

Notes

Acknowledgements

This work was supported by the Russian Science Foundation (Grant #17-14-01323). In part of higher plant thylakoid membranes (Table 1), the work was supported by the Russian Science Foundation (Grant #14-14-00535). The authors are grateful to Dr. Dmitry Cherepanov for valuable discussion.

Supplementary material

11120_2018_514_MOESM1_ESM.docx (13 kb)
Supplementary Table 1 (DOCX 12 KB)
11120_2018_514_MOESM2_ESM.tif (479 kb)
Supplementary Figure 1—The scheme of redox conversations of TMPD and DCPIP (TIF 479 KB)
11120_2018_514_MOESM3_ESM.tif (104 kb)
Supplementary Figure 2—The effect of ascorbate concentration of O2 uptake rate (VO2) in the absence (squires, solid line) or presence (triangles, dashed line) of MV (A) and the steady-state P700+ level, ΔP700+, in the presence of MV (B). On A, VO2 values in the presence of 1 mM TMPD are shown for comparison (circles). Trimeric PS I at 2 (A) or 5 (B) µg Chl mL−1, pH 7.6. Data are shown as mean of 3 repetitions ± SE (TIF 104 KB)

References

  1. Asada K, Nakano Y (1978) Affinity for oxygen in photoreduction of molecular oxygen and scavenging of hydrogen peroxide in spinach chloroplasts. Photochem Photobiol 28:917–920.  https://doi.org/10.1111/j.1751-1097.1978.tb07040.x CrossRefGoogle Scholar
  2. Ball EG (1937) Studies on oxidation-reduction. 23. Ascorbic acid. J Biol Chem 118:219–239Google Scholar
  3. Boucher N, Carpentier R (1993) Heat-stress stimulation of oxygen uptake by Photosystem I involves the reduction of superoxide radicals by specific electron donors. Photosynth Res 35:213–218.  https://doi.org/10.1007/BF00016552 CrossRefPubMedGoogle Scholar
  4. Díaz-Quintana A, Leibl W, Bottin H, Sétif P (1998) Electron transfer in Photosystem I reaction centers follows a linear pathway in which iron—sulfur cluster FB is the immediate electron donor to soluble ferredoxin. Biochemistry 37:3429–3439.  https://doi.org/10.1021/BI972469L CrossRefPubMedGoogle Scholar
  5. Dvoranová D, Barbieriková Z, Dorotíková S et al (2015) Redox processes of 2,6-dichlorophenolindophenolate in different solvents. A combined electrochemical, spectroelectrochemical, photochemical, and theoretical study. J Solid State Electrochem 19:2633–2642.  https://doi.org/10.1007/s10008-015-2823-x CrossRefGoogle Scholar
  6. Fujii T, Yokoyama E, Inoue K, Sakurai H (1990) The sites of electron donation of Photosystem I to methyl viologen. Biochim Biophys Acta BBA 1015:41–48.  https://doi.org/10.1016/0005-2728(90)90213-N CrossRefGoogle Scholar
  7. Golbeck JH (1999) A comparative analysis of the spin state distribution of in vitro and in vivo mutants of PsaC. A biochemical argument for the sequence of electron transfer in Photosystem I as FX → FA → FB → ferredoxin/flavodoxin. Photosynth Res 61:107–144.  https://doi.org/10.1023/A:1006281802710 CrossRefGoogle Scholar
  8. Gopta OA, Tyunyatkina AA, Kurashov VN et al (2008) Effect of redox mediators on the flash-induced membrane potential generation in Mn-depleted photosystem II core particles. Eur Biophys J 37:1045–1050.  https://doi.org/10.1007/s00249-007-0231-6 CrossRefPubMedGoogle Scholar
  9. Gourovskaya KN, Mamedov MD, Vassiliev IR et al (1997) Electrogenic reduction of the primary electron donor P700 + in photosystem I by redox dyes. FEBS Lett 414:193–196.  https://doi.org/10.1016/S0014-5793(97)00994-0 CrossRefPubMedGoogle Scholar
  10. Hervás M, Navarro JA (2011) Effect of crowding on the electron transfer process from plastocyanin and cytochrome c6 to photosystem I: a comparative study from cyanobacteria to green algae. Photosynth Res 107:279–286.  https://doi.org/10.1007/s11120-011-9637-1 CrossRefPubMedGoogle Scholar
  11. Hormann H, Neubauer C, Asada K, Schreiber U (1993) Intact chloroplasts display pH 5 optimum of O2-reduction in the absence of methyl viologen: Indirect evidence for a regulatory role of superoxide protonation. Photosynth Res 37:69–80.  https://doi.org/10.1007/BF02185440 CrossRefPubMedGoogle Scholar
  12. Ivanov B, Asada K, Kramer DM, Edwards G (2005) Characterization of photosynthetic electron transport in bundle sheath cells of maize. I. Ascorbate effectively stimulates cyclic electron flow around PSI. Planta 220:572–581.  https://doi.org/10.1007/s00425-004-1367-6 CrossRefPubMedGoogle Scholar
  13. Jajoo A, Bharti S (1993) Effect of anions on photosystem 1-mediated electron transport in spinach chloroplasts. J Exp Bot 44:785–790.  https://doi.org/10.1093/jxb/44.4.785 CrossRefGoogle Scholar
  14. Ke B (1967) Photoreduction sites for 2,6-dichlorophenolindophenol in chloroplasts. Plant Physiol 42:1310–1312CrossRefPubMedPubMedCentralGoogle Scholar
  15. Kozuleva MA, Ivanov BN (2010) Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids. Photosynth Res 105:51–61.  https://doi.org/10.1007/s11120-010-9565-5 CrossRefPubMedGoogle Scholar
  16. Kozuleva MA, Ivanov BN (2016) The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain. Plant Cell Physiol 57:1397–1404.  https://doi.org/10.1093/pcp/pcw035 PubMedGoogle Scholar
  17. Kozuleva MA, Petrova AA, Mamedov MD et al (2014) O2 reduction by photosystem I involves phylloquinone under steady-state illumination. FEBS Lett 588:4364–4368.  https://doi.org/10.1016/j.febslet.2014.10.003 CrossRefPubMedGoogle Scholar
  18. Kozuleva MA, Vetoshkina DV, Petrova AA et al (2015) The study of oxygen reduction in photosystem I of higher plants using electron donors for this photosystem in intact thylakoids. Biochem Mosc Suppl Ser Membr Cell Biol 9:246–251.  https://doi.org/10.1134/S1990747814060026 Google Scholar
  19. Malavath T, Caspy I, Netzer-El SY et al (2018) Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis. Biochim Biophys Acta BBA.  https://doi.org/10.1016/j.bbabio.2018.02.002 PubMedGoogle Scholar
  20. Mamedov MD, Gourovskaya KN, Vassiliev IR et al (1998) Electrogenicity accompanies photoreduction of the iron-sulfur clusters FA and FB in photosystem I. FEBS Lett 431:219–223.  https://doi.org/10.1016/S0014-5793(98)00759-5 CrossRefPubMedGoogle Scholar
  21. Mamedov MD, Mamedova AA, Chamorovsky SK, Semenov AY (2001) Electrogenic reduction of the primary electron donor P700 by plastocyanin in photosystem I complexes. FEBS Lett 500:172–176.  https://doi.org/10.1016/S0014-5793(01)02615-1 CrossRefPubMedGoogle Scholar
  22. Mamedova AA, Mamedov MD, Gourovskaya KN et al (1999) Electrometrical study of electron transfer from the terminal F A/FB iron-sulfur clusters to external acceptors in photosystem I. FEBS Lett 462:421–424.  https://doi.org/10.1016/S0014-5793(99)01570-7 CrossRefPubMedGoogle Scholar
  23. Mano J, Hideg É, Asada K (2004) Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I. Arch Biochem Biophys 429:71–80.  https://doi.org/10.1016/J.ABB.2004.05.022 CrossRefPubMedGoogle Scholar
  24. Marchanka A, Gastel M van (2012) Reversed freeze quench method near the solvent phase transition. J Phys Chem A 116:3899–3906.  https://doi.org/10.1021/jp300555x CrossRefPubMedGoogle Scholar
  25. Milanovsky GE, Petrova AA, Cherepanov DA, Semenov AY (2017) Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors. Photosynth Res 133:185–199.  https://doi.org/10.1007/s11120-017-0366-y CrossRefPubMedGoogle Scholar
  26. Nikandrov VV, Van Chan N, Brin GP, Krasnovskií AA (1978) Methylviologen photoreduction by chloroplasts. Mol Biol (Mosk) 12:1278–1287Google Scholar
  27. Parrett KG, Mehari T, Warren PG, Golbeck JH (1989) Purification and properties of the intact P-700 and F Xcontaining Photosystem I core protein. Biochimica et Biophysica Acta (BBA)-Bioenergetics 973(2):324–332CrossRefGoogle Scholar
  28. Shen G, Antonkine ML, van der Est A, Vassiliev IR, Brettel K, Bittl R, Zech SG, Zhao J, Stehlik D, Bryant DA, Golbeck JH (2002) Assembly of Photosystem I II. RUBREDOXIN IS REQUIRED FOR THE IN VIVO ASSEMBLY OF FX IN SYNECHOCOCCUS SP. PCC 7002 AS SHOWN BY OPTICAL AND EPR SPECTROSCOPY. J Biological Chem 277(23):20355–20366CrossRefGoogle Scholar
  29. Takahashi M, Asada K (1982) Dependence of oxygen affinity for Mehler reaction on photochemical activity of chloroplast thylakoids. Plant Cell Physiol 23:1457–1461.  https://doi.org/10.1093/oxfordjournals.pcp.a076495 CrossRefGoogle Scholar
  30. Thomas DD, Keller H, McConnell HM (1963) Exciton magnetic resonance in Wurster’s Blue Perchlorate. J Chem Phys 39:2321–2329.  https://doi.org/10.1063/1.1701437 CrossRefGoogle Scholar
  31. Thomas PG, Quinn PJ, Williams WP (1986) The origin of photosystem-I-mediated electron transport stimulation in heat-stressed chloroplasts. Planta 167:133–139.  https://doi.org/10.1007/BF00446380 CrossRefPubMedGoogle Scholar
  32. Tóth SZ, Schansker G, Garab G (2013) The physiological roles and metabolism of ascorbate in chloroplasts. Physiol Plant 148:161–175.  https://doi.org/10.1111/ppl.12006 CrossRefPubMedGoogle Scholar
  33. Trubitsin BV, Mamedov MD, Semenov AY, Tikhonov AN (2014) Interaction of ascorbate with photosystem I. Photosynth Res 122:215–231.  https://doi.org/10.1007/s11120-014-0023-7 CrossRefPubMedGoogle Scholar
  34. Vassiliev IR, Jung YS, Mamedov MD et al (1997) Near-IR absorbance changes and electrogenic reactions in the microsecond-to-second time domain in photosystem I. Biophys J 72:301–315.  https://doi.org/10.1016/S0006-3495(97)78669-7 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Vassiliev IR, Jung Y-S, Yang F, Golbeck JH (1998) PsaC subunit of photosystem I is oriented with iron-sulfur cluster FB as the immediate electron donor to ferredoxin and flavodoxin. Biophys J 74:2029–2035.  https://doi.org/10.1016/S0006-3495(98)77909-3 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Yang X, Zhang YH, Yang ZL et al (2009) pH dependence of photosynthetic behavior of plant photosystem I particles. Russ J Plant Physiol 56:599–606.  https://doi.org/10.1134/S1021443709050033 CrossRefGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.A.N. Belozersky Institute of Physical-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchinoRussia
  3. 3.Department of Molecular Biology and Ecology of Plants, The George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

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