Photosynthesis Research

, Volume 126, Issue 1, pp 161–169 | Cite as

The Photosystem II D1-K238E mutation enhances electrical current production using cyanobacterial thylakoid membranes in a bio-photoelectrochemical cell

  • Shirley Larom
  • Dan Kallmann
  • Gadiel Saper
  • Roy Pinhassi
  • Avner Rothschild
  • Hen Dotan
  • Guy Ankonina
  • Gadi Schuster
  • Noam Adir
Regular Paper

Abstract

The conversion of solar energy (SEC) to storable chemical energy by photosynthesis has been performed by photosynthetic organisms, including oxygenic cyanobacteria for over 3 billion years. We have previously shown that crude thylakoid membranes from the cyanobacterium Synechocytis sp. PCC 6803 can reduce the electron transfer (ET) protein cytochrome c even in the presence of the PSII inhibitor DCMU. Mutation of lysine 238 of the Photosystem II D1 protein to glutamic acid increased the cytochrome reduction rates, indicating the possible position of this unknown ET pathway. In this contribution, we show that D1-K238E is rather unique, as other mutations to K238, or to other residues in the same vicinity, are not as successful in cytochrome c reduction. This observation indicates the sensitivity of ET reactions to minor changes. As the next step in obtaining useful SEC from biological material, we describe the use of crude Synechocystis membranes in a bio-photovoltaic cell containing an N-acetyl cysteine-modified gold electrode. We show the production of significant current for prolonged time durations, in the presence of DCMU. Surprisingly, the presence of cytochrome c was not found to be necessary for ET to the bio-voltaic cell.

Keywords

Photosynthesis Cyanobacteria Solar energy conversion Cytochrome c Electrochemistry 

Abbreviations

BPC

Bio-photoelectrochemical cell

Chl

Chlorophyll

Cyt c

Horse heart mitochondrial cytochrome c

CV

Cyclic voltammetry

ChAmp

Chronoamperometry

ET

Electron transfer

D1-K238E

K238E mutant of D1 protein

LHC

Light-harvesting complexe(s)

NAC

N-Acetyl cysteine

PS

Photosystem (s)

PSI

Photosystem I

PSII

Photosystem II

RC

Reaction center (s)

RSS

Wild-type D1 protein encoded by psbA2

SAM

Self-assembled monolayer

SEC

Solar energy conversion

Syn

Synechocystis PCC sp. 6803

Supplementary material

11120_2015_75_MOESM1_ESM.tif (187 kb)
The single compartment BPC (bio-photoelectrochemical cell) used for the cyclic voltammetry (CV) and chronoamperometric (ChAmp) experiments. Supplementary material 1 (TIFF 187 kb)
11120_2015_75_MOESM2_ESM.tif (52 kb)
A modified electrode is used to oxidize cyt c. Supplementary material 2 (TIFF 52 kb)
11120_2015_75_MOESM3_ESM.tif (182 kb)
Gas chromatography identifies the light-dependent hydrogen production in the BPC. Supplementary material 3 (TIFF 182 kb)
11120_2015_75_MOESM4_ESM.tif (50 kb)
CV measurements produced under dark or light conditions by the BPC. Supplementary material 4 (TIFF 49 kb)
11120_2015_75_MOESM5_ESM.tif (96 kb)
Thylakoid membranes supply light-dependent current to the BPC for extended time periods. Supplementary material 5 (TIFF 96 kb)

References

  1. Adir N, Axelrod HL, Beroza P, Isaacson RA, Rongey SH, Okamura MY, Feher G (1996) Crystallization and characterization of the photosynthetic reaction center-cytochrome c2 complex from Rhodobacter sphaeroides. Biochemistry 35:2535–2547CrossRefPubMedGoogle Scholar
  2. Amdursky N, Ferber D, Bortolotti CA, Dolgikh DA, Chertkova RV, Pecht I, Sheves M, Cahen D (2014) Solid-state electron transport via cytochrome c depends on electronic coupling to electrodes and across the protein. Proc Natl Acad Sci USA 111:5556–5561PubMedCentralCrossRefPubMedGoogle Scholar
  3. Armond PA, Staehelin LA, Arntzen CJ (1977) Spatial relationship of photosystem I, photosystem II, and the light-harvesting complex in chloroplast membranes. J Cell Biol 73:400–418CrossRefPubMedGoogle Scholar
  4. Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in beta vulgaris. Plant Physiol 24:1–15PubMedCentralCrossRefPubMedGoogle Scholar
  5. Axelrod HL, Abresch EC, Okamura MY, Yeh AP, Rees DC, Feher G (2002) X-ray structure determination of the cytochrome c2: reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol 319:501–515CrossRefPubMedGoogle Scholar
  6. Barber J (2012) Photosystem II: the water-splitting enzyme of photosynthesis. Cold Spring Harb Symp Quant Biol 77:295–307CrossRefPubMedGoogle Scholar
  7. Bartlett PN, Whitaker RG (1987) Strategies for the development of amperometric enzyme electrodes. Biosensors 3:359–379CrossRefPubMedGoogle Scholar
  8. Bashir Q, Scanu S, Ubbink M (2011) Dynamics in electron transfer protein complexes. FEBS J 278:1391–1400CrossRefPubMedGoogle Scholar
  9. Blankenship RE (2014) Molecular mechanisms in photosynthesis, 2nd edn. Wiley, ChichesterGoogle Scholar
  10. Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23:94–97CrossRefPubMedGoogle Scholar
  11. Brudvig GW (2008) Water oxidation chemistry of photosystem II. Philos Trans R Soc Lond Ser B 363:1211–1218 (discussion 1218–1219)CrossRefGoogle Scholar
  12. Bushnell GW, Louie GV, Brayer GD (1990) High-resolution three-dimensional structure of horse heart cytochrome c. J Mol Biol 214:585–595Google Scholar
  13. Debus RJ, Barry BA, Sithole I, Babcock GT, McIntosh L (1988) Directed mutagenesis indicates that the donor to P + 680 in photosystem II is tyrosine-161 of the D1 polypeptide. Biochemistry 27:9071–9074CrossRefPubMedGoogle Scholar
  14. Digleria K, Hill HAO, Lowe VJ, Page DJ (1986) Direct Electrochemistry of Horse-Heart cytochrome-C at amino acid-modified gold electrodes. J Electroanal Chem 213:333–338CrossRefGoogle Scholar
  15. Fedurco M (2000) Redox reactions of heme-containing metalloproteins: dynamic effects of self-assembled monolayers on thermodynamics and kinetics of cytochrome c electron-transfer reactions. Coordin Chem Rev 209:263–331CrossRefGoogle Scholar
  16. Harrold JW Jr, Woronowicz K, Lamptey JL, Awong J, Baird J, Moshar A, Vittadello M, Falkowski PG, Niederman RA (2013) Functional interfacing of Rhodospirillum rubrum chromatophores to a conducting support for capture and conversion of solar energy. J Phys Chem B 117:11249–11259CrossRefPubMedGoogle Scholar
  17. Kargul J, Janna Olmos JD, Krupnik T (2012) Structure and function of photosystem I and its application in biomimetic solar-to-fuel systems. J Plant Physiol 169:1639–1653CrossRefPubMedGoogle Scholar
  18. Kato M, Zhang JZ, Paul N, Reisner E (2014) Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem Soc Rev 43(18):6485–6497CrossRefPubMedGoogle Scholar
  19. Krieger-Liszkay A, Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 37:17339–17344CrossRefPubMedGoogle Scholar
  20. Kulkarni RD, Golden SS (1995) Form II of D1 is important during transition from standard to high light intensity in Synechococcus sp. strain PCC 7942. Photosynth Res 46:435–443CrossRefPubMedGoogle Scholar
  21. Larom S, Salama F, Schuster G, Adir N (2010) Engineering of an alternative electron transfer path in photosystem II. Proc Natl Acad Sci USA 107:9650–9655PubMedCentralCrossRefPubMedGoogle Scholar
  22. Lovley DR (2012) Electromicrobiology. Annu Rev Microbiol 66:391–409CrossRefPubMedGoogle Scholar
  23. McConnell I, Li G, Brudvig GW (2010) Energy conversion in natural and artificial photosynthesis. Chem Biol 17:434–447PubMedCentralCrossRefPubMedGoogle Scholar
  24. McCormick AJ, Bombelli P, Scott AM, Philips AJ, Smith AG, Fisher AC, Howe CJ (2011) Photosynthetic biofilms in pure culture harness solar energy in a mediatorless bio-photovoltaic cell (BPV) system. Energ Environ Sci 4:4699–4709CrossRefGoogle Scholar
  25. Mulo P, Tyystjarvi T, Tyystjarvi E, Govindjee Maenpaa P, Aro EM (1997) Mutagenesis of the D-E loop of photosystem II reaction centre protein D1. Function and assembly of photosystem II. Plant Mol Biol 33:1059–1071CrossRefPubMedGoogle Scholar
  26. Mulo P, Laakso S, Maenpaa P, Aro EM (1998) Stepwise photoinhibition of photosystem II. Studies with Synechocystis species PCC 6803 mutants with a modified D-E loop of the reaction center polypeptide D1. Plant Physiol 117:483–490PubMedCentralCrossRefPubMedGoogle Scholar
  27. Neilson JA, Durnford DG (2010) Evolutionary distribution of light-harvesting complex-like proteins in photosynthetic eukaryotes. Genome 53:68–78CrossRefPubMedGoogle Scholar
  28. Nguyen K, Bruce BD (2014) Growing green electricity: progress and strategies for use of photosystem I for sustainable photovoltaic energy conversion. Biochim Biophys Acta 9:1553–1566CrossRefGoogle Scholar
  29. Pierson HO (1999) Handbook of chemical vapor deposition: principles, technology and applications, 2nd edn. william andrew, NorwichGoogle Scholar
  30. Rappaport F, Lavergne J (2009) Thermoluminescence: theory. Photosynth Res 101:205–216CrossRefPubMedGoogle Scholar
  31. Ronge J, Bosserez T, Martel D, Nervi C, Boarino L, Taulelle F, Decher G, Bordiga S, Martens JA (2014) Monolithic cells for solar fuels. Chem Soc Rev 43(23):7963–7981CrossRefPubMedGoogle Scholar
  32. Schultz DM, Yoon TP (2014) Solar synthesis: prospects in visible light photocatalysis. Science 343:1239176PubMedCentralCrossRefPubMedGoogle Scholar
  33. Shen JR, Kamiya N (2000) Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. Biochemistry 39:14739–14744CrossRefPubMedGoogle Scholar
  34. Silveira CM, Almeida MG (2013) Small electron-transfer proteins as mediators in enzymatic electrochemical biosensors. Anal Bioanal Chem 405:3619–3635CrossRefPubMedGoogle Scholar
  35. Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76:185–196CrossRefPubMedGoogle Scholar
  36. Sugiura M, Boussac A (2014) Some photosystem II properties depending on the D1 protein variants in Thermosynechococcus elongatus. Biochim Biophys Acta 9:1427–1434CrossRefGoogle Scholar
  37. Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330:1413–1415CrossRefPubMedGoogle Scholar
  38. Takano A, Takahashi R, Suzuki H, Noguchi T (2008) Herbicide effect on the hydrogen-bonding interaction of the primary quinone electron acceptor QA in photosystem II as studied by Fourier transform infrared spectroscopy. Photosynth Res 98:159–167CrossRefPubMedGoogle Scholar
  39. Toporik H, Carmeli I, Volotsenko I, Molotskii M, Rosenwaks Y, Carmeli C, Nelson N (2012) Large photovoltages generated by plant photosystem I crystals. Adv Mater 24(2988–2991):2987CrossRefGoogle Scholar
  40. Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature 473:55–60CrossRefPubMedGoogle Scholar
  41. Vinyard DJ, Gimpel J, Ananyev GM, Cornejo MA, Golden SS, Mayfield SP, Dismukes GC (2013) Natural variants of photosystem II subunit D1 tune photochemical fitness to solar intensity. J Biol Chem 288:5451–5462PubMedCentralCrossRefPubMedGoogle Scholar
  42. Willner I, Willner B (2001) Biomaterials integrated with electronic elements: en route to bioelectronics. Trends Biotechnol 19:222–230CrossRefPubMedGoogle Scholar
  43. Willner B, Katz E, Willner I (2006) Electrical contacting of redox proteins by nanotechnological means. Curr Opin Biotechnol 17:589–596CrossRefPubMedGoogle Scholar
  44. Yehezkeli O, Wilner OI, Tel-Vered R, Roizman-Sade D, Nechushtai R, Willner I (2010) Generation of photocurrents by bis-aniline-cross-linked Pt nanoparticle/photosystem I composites on electrodes. J Phys Chem B 114:14383–14388CrossRefPubMedGoogle Scholar
  45. Yehezkeli O, Tel-Vered R, Wasserman J, Trifonov A, Michaeli D, Nechushtai R, Willner I (2012) Integrated photosystem II-based photo-bioelectrochemical cells. Nat Commun 3:742CrossRefPubMedGoogle Scholar
  46. Yehezkeli O, Tel-Vered R, Michaeli D, Nechushtai R, Willner I (2013) Photosystem I (PSI)/Photosystem II (PSII)-based photo-bioelectrochemical cells revealing directional generation of photocurrents. Small 9:2970–2978CrossRefPubMedGoogle Scholar
  47. Yehezkeli O, Tel-Vered R, Michaeli D, Willner I, Nechushtai R (2014) Photosynthetic reaction center-functionalized electrodes for photo-bioelectrochemical cells. Photosynth Res 120:71–85CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Shirley Larom
    • 1
  • Dan Kallmann
    • 1
    • 2
    • 3
    • 5
  • Gadiel Saper
    • 1
    • 2
    • 3
    • 5
  • Roy Pinhassi
    • 1
    • 2
    • 3
    • 5
  • Avner Rothschild
    • 3
  • Hen Dotan
    • 3
  • Guy Ankonina
    • 4
  • Gadi Schuster
    • 1
  • Noam Adir
    • 5
  1. 1.Faculty of BiologyTechnion-Israel Institute of TechnologyHaifaIsrael
  2. 2.Grand Technion Energy ProgramTechnion-Israel Institute of TechnologyHaifaIsrael
  3. 3.Faculty of Material Science and EngineeringTechnion-Israel Institute of TechnologyHaifaIsrael
  4. 4.Photovoltaics LabTechnion-Israel Institute of TechnologyHaifaIsrael
  5. 5.Schulich Faculty of ChemistryTechnion-Israel Institute of TechnologyHaifaIsrael

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