Hydrogen peroxide (H2O2) is known to be generated in Photosystem II (PSII) via enzymatic and non-enzymatic pathways. Detection of H2O2 by different spectroscopic techniques has been explored, however its sensitive detection has always been a challenge in photosynthetic research. During the recent past, fluorescence probes such as Amplex Red (AR) has been used but is known to either lack specificity or limitation with respect to the minimum detection limit of H2O2. We have employed an electrochemical biosensor for real time monitoring of H2O2 generation at the level of sub-cellular organelles. The electrochemical biosensor comprises of counter electrode and working electrodes. The counter electrode is a platinum plate, while the working electrode is a mediator based catalytic amperometric biosensor device developed by the coating of a carbon electrode with osmium-horseradish peroxidase which acts as H2O2 detection sensor. In the current study, generation and kinetic behavior of H2O2 in PSII membranes have been studied under light illumination. Electrochemical detection of H2O2 using the catalytic amperometric biosensor device is claimed to serve as a promising technique for detection of H2O2 in photosynthetic cells and subcellular structures including PSII or thylakoid membranes. It can also provide a precise information on qualitative determination of H2O2 and thus can be widely used in photosynthetic research.

Biomedical Engineering Research Center Tohoku Institute of Technology Sendai Japan

Biomedical Engineering Research Center Tohoku Institute of Technology Sendai Japan ; Center for General Education Tohoku Institute of Technology Sendai Japan

Biomedical Engineering Research Center Tohoku Institute of Technology Sendai Japan ; Graduate Department of Electronics Tohoku Institute of Technology Sendai Japan

Biomedical Engineering Research Center Tohoku Institute of Technology Sendai Japan ; Graduate Department of Environmental Information Engineering Tohoku Institute of Technology Sendai Japan

Department of Biophysics Faculty of Science Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Olomouc Czech Republic

Graduate Department of Environmental Information Engineering Tohoku Institute of Technology Sendai Japan

Zobrazit více v PubMed

Ahammad A. J. S. (2013). Hydrogen peroxide biosensors based on horseradish peroxidase and hemoglobin. J. Biosens. Bioelectron. S9:001 10.4172/2155-6210.S9-001 DOI

Ananyev G., Renger G., Wacker U., Klimov V. (1994). The photoproduction of superoxide radicals and the superoxide-dismutase activity of photosystem II. The possible involvement of cytochrome b559. Photosynth. Res. 41, 327–338. 10.1007/BF00019410 PubMed DOI

Arató A., Bondarava N., Krieger-Liszkay A. (2004). Production of reactive oxygen species in chloride- and calcium-depleted photosystem II and their involvement in photoinhibition. Biochim. Biophys. Acta 1608, 171–180. 10.1016/j.bbabio.2003.12.003 PubMed DOI

Berthold D. A., Babcock G. T., Yocum C. F. (1981). A highly resolved oxygen evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett. 134, 231–234. 10.1016/0014-5793(81)80608-4 DOI

Bolwell G. P., Bindschedler L. V., Blee K. A., Butt V. S., Davies D. R., Gardner S. L., et al. . (2002). The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp. Bot. 53, 1367–1376. 10.1093/jexbot/53.372.1367 PubMed DOI

Camacho C., Matías J. C., Chico B., Cao R., Gómez L., Simpson B. K., et al. (2007). Amperometric biosensor for hydrogen peroxide, using supramolecularly immobilized horseradish peroxidase on the β-cyclodextrin-coated gold electrode. Electroanalysis 19, 2538–2542. 10.1002/elan.200703993 DOI

Chen S., Yin C., Strasser R. J., Govindjee Yang, C., Qiang S. (2012). Reactive oxygen species from chloroplasts contribute to 3-acetyl-5- isopropyltetramic acid-induced leaf necrosis of Arabidopsis thaliana. Plant Physiol. Biochem. 52, 38–51. 10.1016/j.plaphy.2011.11.004 PubMed DOI

Chen S., Yuan R., Chai Y., Xu L., Wang N., Li X., et al. (2006). Amperometric hydrogen peroxide biosensor based on the immobilization of Horseradish Peroxidase (HRP) on the layer-by-layer assembly films of gold colloidal nanoparticles and toluidine blue. Electroanalysis 18, 471–477. 10.1002/elan.200503424 DOI

Chen W., Li B., Xu C., Wang L. (2009). Chemiluminescence flow biosensor for hydrogen peroxide using DNAzyme immobilized on eggshell membrane as a thermally stable biocatalyst. Biosens. Bioelectron. 24, 2534–2540. 10.1016/j.bios.2009.01.010 PubMed DOI

Cleland R. E., Grace S. C. (1999). Voltammetric detection of superoxide production by photosystem II. FEBS Lett. 457, 348–352. 10.1016/S0014-5793(99)01067-4 PubMed DOI

Ferreira K. N., Iverson T. M., Maghlaoui K., Barber J., Iwata S. (2004). Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838. 10.1126/science.1093087 PubMed DOI

Ford R. C., Evans M. C. W. (1983). Isolation of a photosystem II from higher plants with highly enriched oxygen evolution activity. FEBS Lett. 160, 159–164. 10.1016/0014-5793(83)80957-0 DOI

Foyer C. H., Shigeoka S. (2011). Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 155, 93–100. 10.1104/pp.110.166181 PubMed DOI PMC

Gechev T. S., Van Breusegem F., Stone J. M., Denev I., Laloi C. (2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28, 1091–1101. 10.1002/bies.20493 PubMed DOI

Guskov A., Kern J., Gabdulkhakov A., Broser M., Zouni A., Saenger W. (2009). Cynobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16, 334–342. 10.1038/nsmb.1559 PubMed DOI

Halliwell B., Gutteridge J. M. C. (2007). Free Radicals in Biology and Medicine, 4th Edn. New York, NY: Oxford University Press.

Inoue K. Y., Ino K., Shiku H., Kasai S., Yasukawa T., Mizutani F., et al. . (2010). Electrochemical monitoring of hydrogen peroxide released from leucocytes on horseradish peroxidase redox polymer coated electrode chip. Biosens. Bioelectron. 25, 1723–1728. 10.1016/j.bios.2009.12.014 PubMed DOI

Jia J. (2008). Hydrogen peroxide biosensor based on horseradish peroxidase– Au nanoparticles at a viologen grafted glassy carbon electrode. Microchim. Acta 163, 237–241. 10.1007/s00604-008-0002-9 DOI

Kafi A. K., Wu G., Chen A. (2009). A novel hydrogen peroxide biosensor based on the immobilization of horseradish peroxidase onto Au-modified titanium dioxide nanotube arrays. Biosens. Bioelectron. 24, 566–571. 10.1016/j.bios.2008.06.004 PubMed DOI

Kawakami K., Umena Y., Kamiya N., Shen J.-R. (2011). Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution. J. Photochem. Photobiol. B 104, 9–18. 10.1016/j.jphotobiol.2011.03.017 PubMed DOI

Krieger-Liszkay A. (2005). Singlet oxygen production in photosynthesis. J. Exp. Bot. 56, 337–346. 10.1093/jxb/erh237 PubMed DOI

Lei C. X., Long L. P., Cao Z. L. (2005). An H2O2 biosensor based on immobilization of horseradish peroxidase labeled nano-Au in silica sol-gel/alginate composite film. Anal. Lett. 38, 1721–1734. 10.1080/00032710500207762 DOI

Lei C. X., Wang H., Shen G. L., Yu R. Q. (2004). Immobilization of enzymes on the nano-au film modified glassy carbon electrode for the determination of hydrogen peroxide and glucose. Electroanalysis 16, 736–740. 10.1002/elan.200302877 DOI

Li C. X., Deng K. Q., Shen G. L., Yu R. Q. (2004). Amperometric hydrogen peroxide biosensor based on horseradish peroxidase-labeled nano-Au colloids immobilized on poly(2,6-pyridinedicarboxylic acid) layer by cysteamine. Anal. Sci. 20, 1277–1281. 10.2116/analsci.20.1277 PubMed DOI

Li Z. H., Guedri H., Viguier B., Sun S. G., Marty J. L. (2013). Optimization of hydrogen peroxide detection for a methyl mercaptan biosensor. Sensors 13, 5028–5039. 10.3390/s130405028 PubMed DOI PMC

Lichtenthaler H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148, 350–382. 10.1016/0076-6879(87)48036-1 DOI

Lin X. Q., Chen J., Chen Z. H. (2000). Amperometric biosensor for hydrogen peroxide based on immobilization of horseradish peroxidase on methylene blue modified graphite electrode. Electroanalysis 12, 306–310. 10.1002/(sici)1521-4109(20000301) DOI

Liu X., Luo L., Ding Y., Xu Y., Li F. (2011). Hydrogen peroxide biosensor based on the immobilization of horseradish peroxidase on γ-Al2O3 nanoparticles/chitosan film-modified electrode. J. Solid State Electrochem. 15, 447–453. 10.1007/s10008-010-1120-y DOI

Loew N., Wollenberger U., Scheller F. W., Katterle M. (2009). Direct electrochemistry and spectroelectrochemistry of osmium substituted horseradish peroxidase. Bioelectrochemistry 76, 28–33. 10.1016/j.bioelechem.2009.03.015 PubMed DOI

Loll B., Kern J., Saenger W., Zouni A., Biesiadka J. (2005). Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040–1044. 10.1038/nature04224 PubMed DOI

Lu L., Zhang L., Zhang X., Wu Z., Huan S., Shen G., et al. (2010). A MgO nanoparticles composite matrix-based electrochemical biosensor for hydrogen peroxide with high sensitivity. Electroanalysis 22, 471–477. 10.1002/elan.200900429 DOI

Luo L., Zhu L., Xu Y., Shen L., Wang X., Ding Y., et al. (2011). Hydrogen peroxide biosensor based on horseradish peroxidase immobilized on chitosan-wrapped NiFe2O4 nanoparticles. Microchim. Acta 174, 55–61. 10.1007/s00604-011-0591-6 DOI

Mills A., Tommons C., Bailey R. T., Tedford M. C., Crilly P. J. (2007). Reversible, fluorescence-based optical sensor for hydrogen peroxide. Analyst 132, 566–571. 10.1039/b618506a PubMed DOI

Minibayeva F., Kolesnikov O., Chasov A., Beckett R. P., Lüthje S., Vylegzhanina N., et al. . (2009). Wound-induced apoplastic peroxidase activities: their roles in the production and detoxification of reactive oxygen species. Plant Cell. Environ. 32, 497–508. 10.1111/j.1365-3040.2009.01944.x PubMed DOI

Minibayeva F., Kolesnikov O. P., Gordon L. K. (1998). Contribution of a plasma membrane redox system to the superoxide production by wheat root cells Protoplasma 205, 101–106. 10.1007/BF01279299 PubMed DOI

Mori I. C., Schroeder J. I. (2004). Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol. 135, 702–708. 10.1104/pp.104.042069 PubMed DOI PMC

Mouithys-Mickalad A., Deby-Dupont G., Nys M., Lamy M., Deby C. (2001). Oxidative processes in human promonocytic cells (THP-1) after differentiation into macrophages by incubation with Chlamydia pneumoniae extracts. Biochem. Biophys. Res. Commun. 287, 781–788. 10.1006/bbrc.2001.5643 PubMed DOI

Mubarakshina M. M., Ivanov B. N. (2010). The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes. Physiol. Plant. 140, 103–110. 10.1111/j.1399-3054.2010.01391.x PubMed DOI

Nakabayashi Y., Yoshikawa H. (2000). Amperometric biosensors for sensing of hydrogen peroxide based on electron transfer between horseradish peroxidase and ferrocene as a mediator. Anal. Sci. 16, 609–613. 10.2116/analsci.16.609 DOI

Pospíšil P. (2009). Production of reactive oxygen species by photosystem II. Biochim. Biophys. Acta 1787, 1151–1160. 10.1016/j.bbabio.2009.05.005 PubMed DOI

Pospíšil P. (2011). Enzymatic function of cytochrome b559 in photosystem II. J Photochem. Photobiol. B 104, 341–347. 10.1016/j.jphotobiol.2011.02.013 PubMed DOI

Pospíšil P. (2012). Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim. Biophys. Acta 1817, 218–231. 10.1016/j.bbabio.2011.05.017 PubMed DOI

Pospíšil P., Arató A., Krieger-Liszkay A., Rutherford A. W. (2004). Hydroxyl radical generation by Photosystem II. Biochemistry 43, 6783–6792. 10.1021/bi036219i PubMed DOI

Pospíšil P., Šnyrychová I., Kruk J., Strzałka K., Nauš J. (2006). Evidence that cytochrome b559 is involved in superoxide production in Photosystem II: effect of synthetic short-chain plastoquinones in a cytochrome b559 tobacco mutant. Biochem. J. 397, 321–327. 10.1042/BJ20060068 PubMed DOI PMC

Prasad A., Pospíšil P. (2012). Ultra-weak photon emission induced by visible light and ultraviolet A radiation via photoactivated skin chromophores: in-vivo charge coupled device imaging. J. Biomed. Opt. 17:085004. 10.1117/1.JBO.17.8.085004 PubMed DOI

Radi A. E., Muñoz-Berbel X., Cortina-Puig M., Marty J. L. (2009). A third generation hydrogen peroxide biosensor based on horseradish peroxidase covalently immobilized on electrografted organic film on screen-printed carbon electrode. Electroanalysis 21, 1624–1629. 10.1002/elan.200904587 DOI

Rappaport F., Diner B. A. (2008). Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in Photosystem II. Coord. Chem. Rev. 252, 259–272. 10.1016/j.ccr.2007.07.016 DOI

Sagi M., Fluhr R. (2001). Superoxide production by plant homologues of the Gp91phox NADPH oxidase. modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126, 1281–1290. 10.1104/pp.126.3.1281 PubMed DOI PMC

Sagi M., Fluhr R. (2006). Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141, 336–340. 10.1104/pp.106.078089 PubMed DOI PMC

Sanford A. L., Morton S. W., Whitehouse K. L., Oara H. M., Lugo-Morales L. Z., Roberts J. G., et al. . (2011). Voltammetric detection of hydrogen peroxide at carbon fiber microelectrodes. Anal Chem. 82, 5205–5210. 10.1021/ac100536s PubMed DOI PMC

Schmitt F. J., Renger G., Friedrich T., Kreslavksi V. D., Zharmukhadmedov S. K., Los D. A., et al. . (2014). Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim. Biophys. Acta 1837, 385–848. 10.1016/j.bbabio.2014.02.005 PubMed DOI

Schröder W. P., Åkerlund H.-E. (1990). Hydrogen peroxide production in photosystem II preparations, in Current Research in Photosynthesis, Vol. 1, ed Baltscheffsky M. (Dordrecht: Kluwer Academic Publisher; ), 901–904.

Senel M. C., Cevik E., Abasıyanık M. F. (2010). Amperometric hydrogen peroxide biosensor based on covalent immobilization of horseradish peroxidase on ferrocene containing polymeric mediator. Sens. Actuators. B Chem. 145, 444–450. 10.1016/j.snb.2009.12.055 DOI

Shao N., Krieger-Liszkay A., Schroda M., Beck Christoph F. (2007). A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo. Plant J. 50, 475–487. 10.1111/j.1365-313X.2007.03065.x PubMed DOI

Šnyrychová I., Ayaydin F., Hideg É. (2009). Detecting hydrogen peroxide in leaves in vivo—a comparison of methods. Physiol. Plant. 135, 1–18. 10.1111/j.1399-3054.2008.01176.x PubMed DOI

Svedruzic D., Jónsson S., Toyota C. G., Reinhardt L. A., Ricagno S, Lindqvist, Y., et al. . (2005). The enzymes of oxalate metabolism: unexpected structures and mechanisms. Arch. Biochem. Biophys. 433, 176–192. 10.1016/j.abb.2004.08.032 PubMed DOI

Tian F., Xu B., Zhu L., Zhu G. (2001). Hydrogen peroxide biosensor with enzyme entrapped within electrodeposited polypyrrole based on mediated sol–gel derived composite carbon electrode. Anal. Chim. Acta 443, 9–16. 10.1016/S0003-2670(01)01187-4 DOI

Tiwari A., Pospísil P. (2009). Superoxide oxidase and reductase activity of cytochrome b559 in photosystem II. Biochim. Biophys. Acta 1787, 985–994. 10.1016/j.bbabio.2009.03.017 PubMed DOI

Tiwari I., Singh M. (2011). Preparation and characterization of methylene blue-SDS-multiwalled carbon nanotubes nanocomposite for the detection of hydrogen peroxide. Microchim. Acta 174, 223–230. 10.1007/s00604-011-0620-5 DOI

Tripathi V. S., Kandimalla V. B., Ju H. (2006). Amperometric biosensor for hydrogen peroxide based on ferrocene-bovine serum albumin and multiwall carbon nanotube modified ormosil composite. Biosens. Bioelectron. 21, 1529–1535. 10.1016/j.bios.2005.07.006 PubMed DOI

Wang G. H., Zhang L. M. (2006). Using novel polysaccharide-silica hybrid material to construct an amperometric biosensor for hydrogen peroxide. J. Phys. Chem. B 110, 24864–24868. 10.1021/jp0657078 PubMed DOI

Wang H. S., Pan Q. X., Wang G. X. (2005). A biosensor based on immobilization of horseradish peroxidase in chitosan matrix cross-linked with glyoxal for amperometric determination of hydrogen peroxide. Sensors 5, 266–276. 10.3390/s5040266 DOI

Yadav D. K., Pospíšil P. (2012). Role of chloride ion in hydroxyl radical production in photosystem II under heat stress: electron paramagnetic resonance spin-trapping study. J. Bioenerg. Biomembr. 44, 365–372. 10.1007/s10863-012-9433-4 PubMed DOI

Yadav D. K., Prasad A., Kruk J., Pospíšil P. (2014). Evidence for the involvement of loosely bound plastosemiquinones in superoxide anion radical production in photosystem II. PLoS ONE 9:e115466. 10.1371/journal.pone.0115466 PubMed DOI PMC

Yang Z., Zong X., Ye Z., Zhao B., Wang Q., Wang P. (2010). The application of complex multiple forklike ZnO nanostructures to rapid and ultrahigh sensitive hydrogen peroxide biosensors. Biomaterials 31, 7534–7541. 10.1016/j.biomaterials.2010.06.019 PubMed DOI

Yao H., Li N., Wei Y. L., Zhu J. J. (2005). A H2O2 biosensor based on immobilization of horseradishperoxidase in a gelatine network matrix. Sensors 5, 277–283. 10.3390/s5040277 DOI

Yasukawa T., Uchida I., Matsue T. (1998). Permeation of redox species through a cell membrane of a single, living algal protoplast studied by microamperometry. Biochim. Biophys. Acta 1369, 152–158. 10.1016/S0005-2736(97)00220-4 PubMed DOI

Yasukawa T., Uchida I., Matsue T. (1999). Microamperometric measurements of photosynthetic activity in a single algal protoplast. Biophys. J. 76, 1129–1135. 10.1016/S0006-3495(99)77277-2 PubMed DOI PMC

Zastrizhnaya O. M., Khorobrykh A. A., Khristin M. S., Klimov V. V. (1997). Photoinduced production of hydrogen peroxide at the acceptor side of photosystem II. Biochemistry 62, 357–361.

Zhang H. L., Lai G. S., Han D. Y., Yu A. M. (2008). An amperometric hydrogen peroxide biosensor based on immobilization of horseradish peroxidase on an electrode modified with magnetic dextran microspheres. Anal. Bioanal. Chem. 390, 971–977. 10.1007/s00216-007-1748-3 PubMed DOI

Zhang S., Weng J., Pan J., Tu T., Yao S., Xu C. (2003). Study on the photo-generation of superoxide radicals in Photosystem II with EPR spin trapping techniques. Photosynth. Res. 75, 41–48. 10.1023/A:1022439009587 PubMed DOI

Zulfugarov I. S., Tovuu A., Eu Y. J., Dogsom B., Poudyal R. S., Nath K., et al. . (2014). Production of superoxide from Photosystem II in a rice (Oryza sativa L.) mutant lacking PsbS. BMC Plant Biol. 14:242. 10.1186/s12870-014-0242-2 PubMed DOI PMC

Bioactive Compounds and Their Impact on Protein Modification in Human Cells

Reactive Oxygen Species Imaging in U937 Cells

Drought Tolerance of Soybean (Glycine max L. Merr.) by Improved Photosynthetic Characteristics and an Efficient Antioxidant Enzyme Activities Under a Split-Root System

Reactive Oxygen Species as a Response to Wounding: In Vivo Imaging in Arabidopsis thaliana

Production of Reactive Oxygen Species by Photosystem II as a Response to Light and Temperature Stress