Skip to main content
SpringerLink
Log in

Biophotoelectrochemistry of Photosynthetic Proteins

  • Chapter
  • First Online:
Book cover Biophotoelectrochemistry: From Bioelectrochemistry to Biophotovoltaics

Part of the book series: Advances in Biochemical Engineering/Biotechnology ((ABE,volume 158))

Abstract

This chapter presents biophotoelectrochemical systems where one of nature’s photosynthetic proteins, such as photosystem 1 (PS1), photosystem 2 (PS2), or bacterial reaction centers, are employed to create devices for technological applications. We use recent advances in biophotoelectrodes for energy conversion and sensing to illustrate the fundamental approaches in half-cell design and characterization. The aim is to guide electrochemists and photosynthetic researchers in the development of hybrid systems interfacing photosynthetic proteins with electrodes ranging from biosensors to biophotovoltaic cells. The first part gives an overview of the photosynthetic electron transfer chain with details on photosynthetic proteins and on the properties relevant for technological applications. The second part describes and critically discusses the main applications of biophotoelectrochemical cells based on photosynthetic proteins and exposes the respective requirement in electrode design. The following and final parts present the standard methodologies for the characterization of the biophotoelectrochemical half-cells with the main objectives of enhancing our mechanistic understanding of electron transfer, charge recombination, overpotential in photocurrent generation and protein degradation processes in devices, and thus open the perspectives for novel biophotoelectrochemical concepts and their rational optimization toward practical efficiencies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62(1):515–548. doi:10.1146/annurev-arplant-042110-103811

    Article  CAS  Google Scholar 

  2. Noy D, Moser CC, Dutton PL (2006) Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales. Biochim Biophys Acta 1757(2):90–105. doi:10.1016/j.bbabio.2005.11.010

    Article  CAS  Google Scholar 

  3. Dau H, Zaharieva I (2009) Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation. Acc Chem Res 42(12):1861–1870. doi:10.1021/ar900225y

    Article  CAS  Google Scholar 

  4. de Wijn R, van Gorkom HJ (2002) The rate of charge recombination in photosystem II. Biochim Biophys Acta 1553(3):302–308. doi:10.1016/S0005-2728(02)00183-4

    Article  Google Scholar 

  5. Kuhl H, Kruip J, Seidler A, Krieger-Liszkay A, Bunker M, Bald D, Scheidig AJ, Rögner M (2000) Towards structural determination of the water-splitting enzyme: purification, crystallization, and preliminary crystallographic studies of photosystem II from a thermophilic cyanobacterium. J Biol Chem 275(27):20652–20659. doi:10.1074/jbc.M001321200

    Article  CAS  Google Scholar 

  6. Lubner CE, Applegate AM, Knörzer P, Ganago A, Bryant DA, Happe T, Golbeck JH (2011) Solar hydrogen-producing bionanodevice outperforms natural photosynthesis. Proc Natl Acad Sci U S A 108(52):20988–20991. doi:10.1073/pnas.1114660108

    Article  CAS  Google Scholar 

  7. Yao DC, Brune DC, Vermaas WF (2012) Lifetimes of photosystem I and II proteins in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 586(2):169–173. doi:10.1016/j.febslet.2011.12.010

    Article  CAS  Google Scholar 

  8. 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 3:742. doi:10.1038/ncomms1741

    Article  Google Scholar 

  9. Kothe T, Plumeré N, Badura A, Nowaczyk MM, Guschin DA, Rögner M, Schuhmann W (2013) Combination of a photosystem 1-based photocathode and a photosystem 2-based photoanode to a Z-scheme mimic for biophotovoltaic applications. Angew Chem Int Ed 52(52):14233–14236. doi:10.1002/anie.201303671

    Article  CAS  Google Scholar 

  10. Gerster D, Reichert J, Bi H, Barth JV, Kaniber SM, Holleitner AW, Visoly-Fisher I, Sergani S, Carmeli I (2012) Photocurrent of a single photosynthetic protein. Nat Nanotechnol 7(10):673–676. doi:10.1038/nnano.2012.165

    Article  CAS  Google Scholar 

  11. Moore GF, Brudvig GW (2011) Energy conversion in photosynthesis: a paradigm for solar fuel production. Annu Rev Condens Matter Phys 2(1):303–327. doi:10.1146/annurev-conmatphys-062910-140503

    Article  CAS  Google Scholar 

  12. Kothe T, Schuhmann W, Rögner M, Plumeré N (2015) 9 Semi-artificial photosynthetic Z-scheme for hydrogen production from water. In: Rögner M (ed) Biohydrogen. De Gruyter, Berlin, München, Boston

    Google Scholar 

  13. Tel-Vered R, Willner I (2014) Photo-bioelectrochemical cells for energy conversion, sensing, and optoelectronic applications. ChemElectroChem 1(11):1778–1797. doi:10.1002/celc.201402133

    Article  CAS  Google Scholar 

  14. Swainsbury DJK, Friebe VM, Frese RN, Jones MR (2014) Evaluation of a biohybrid photoelectrochemical cell employing the purple bacterial reaction centre as a biosensor for herbicides. Biosens Bioelectron 58:172–178. doi:10.1016/j.bios.2014.02.050

    Article  CAS  Google Scholar 

  15. Giardi MT, Pace E (2005) Photosynthetic proteins for technological applications. Trends Biotechnol 23(5):257–263. doi:10.1016/j.tibtech.2005.03.003

    Article  CAS  Google Scholar 

  16. Lambreva MD, Giardi MT, Rambaldi I, Antonacci A, Pastorelli S, Bertalan I, Husu I, Johanningmeier U, Rea G (2013) A powerful molecular engineering tool provided efficient Chlamydomonas mutants as bio-sensing elements for herbicides detection. PLoS One 8(4), e61851. doi:10.1371/journal.pone.0061851

    Article  CAS  Google Scholar 

  17. Rea G, Polticelli F, Antonacci A, Scognamiglio V, Katiyar P, Kulkarni SA, Johanningmeier U, Giardi MT (2009) Structure-based design of novel Chlamydomonas reinhardtii D1-D2 photosynthetic proteins for herbicide monitoring. Protein Sci 18(10):2139–2151. doi:10.1002/pro.228

    Article  CAS  Google Scholar 

  18. Hartmann V, Kothe T, Pöller S, El-Mohsnawy E, Nowaczyk MM, Plumeré N, Schuhmann W, Rögner M (2014) Redox hydrogels with adjusted redox potential for improved efficiency in Z-scheme inspired biophotovoltaic cells. Phys Chem Chem Phys 16(24):11936. doi:10.1039/c4cp00380b

    Article  CAS  Google Scholar 

  19. Mersch D, Lee CY, Zhang JZ, Brinkert K, Fontecilla-Camps JC, Rutherford AW, Reisner E (2015) Wiring of photosystem II to hydrogenase for photoelectrochemical water splitting. J Am Chem Soc 137(26):8541–8549. doi:10.1021/jacs.5b03737

    Article  CAS  Google Scholar 

  20. Krassen H, Schwarze A, Friedrich B, Ataka K, Lenz O, Heberle J (2009) Photosynthetic hydrogen production by a hybrid complex of photosystem I and [NiFe]-hydrogenase. ACS Nano 3(12):4055–4061. doi:10.1021/nn900748j

    Article  CAS  Google Scholar 

  21. Zhao F, Conzuelo F, Hartmann V, Li H, Nowaczyk MM, Plumeré N, Rögner M, Schuhmann W (2015) Light induced H2 evolution from a biophotocathode based on photosystem 1 - Pt nanoparticles complexes integrated in solvated redox polymers films. J Phys Chem B 119(43):13726–13731. doi:10.1021/acs.jpcb.5b03511

    Article  CAS  Google Scholar 

  22. Nguyen K, Bruce BD (2014) Growing green electricity: progress and strategies for use of photosystem I for sustainable photovoltaic energy conversion. Biochim Biophys Acta 1837(9):1553–1566. doi:10.1016/j.bbabio.2013.12.013

    Article  CAS  Google Scholar 

  23. Das R, Kiley PJ, Segal M, Norville J, Yu AA, Wang L, Trammell SA, Reddick LE, Kumar R, Stellacci F, Lebedev N, Schnur J, Bruce BD, Zhang S, Baldo M (2004) Integration of photosynthetic protein molecular complexes in solid-state electronic devices. Nano Lett 4(6):1079–1083. doi:10.1021/nl049579f

    Article  CAS  Google Scholar 

  24. Mershin A, Matsumoto K, Kaiser L, Yu D, Vaughn M, Nazeeruddin MK, Bruce BD, Graetzel M, Zhang S (2012) Self-assembled photosystem-I biophotovoltaics on nanostructured TiO2 and ZnO. Sci Rep 2:234. doi:10.1038/srep00234

    Article  Google Scholar 

  25. Ocakoglu K, Krupnik T, van den Bosch B, Harputlu E, Gullo MP, Olmos JDJ, Yildirimcan S, Gupta RK, Yakuphanoglu F, Barbieri A, Reek JNH, Kargul J (2014) Photosystem I-based biophotovoltaics on nanostructured hematite. Adv Funct Mater 24(47):7467–7477. doi:10.1002/adfm.201401399

    Article  CAS  Google Scholar 

  26. 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. doi:10.1021/ja404699h

    Article  CAS  Google Scholar 

  27. 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(45):14383–14388. doi:10.1021/jp100454u

    Article  CAS  Google Scholar 

  28. Ciesielski PN, Faulkner CJ, Irwin MT, Gregory JM, Tolk NH, Cliffel DE, Jennings GK (2010) Enhanced photocurrent production by photosystem I multilayer assemblies. Adv Funct Mater 20(23):4048–4054. doi:10.1002/adfm.201001193

    Article  CAS  Google Scholar 

  29. Badura A, Esper B, Ataka K, Grunwald C, Wöll C, Kuhlmann J, Heberle J, Rögner M (2006) Light-driven water splitting for (bio-)hydrogen production: photosystem 2 as the central part of a bioelectrochemical device. Photochem Photobiol 82(5):1385. doi:10.1562/2006-07-14-RC-969

    Article  CAS  Google Scholar 

  30. 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. doi:10.1039/c3ee41568f

    Article  CAS  Google Scholar 

  31. Friebe VM, Delgado JD, Swainsbury DJK, Gruber JM, Chanaewa A, van Grondelle R, von Hauff E, Millo D, Jones MR, Frese RN (2016) Plasmon-enhanced photocurrent of photosynthetic pigment proteins on nanoporous silver. Adv Funct Mater 26:285–292. doi:10.1002/adfm.201504020

    Article  CAS  Google Scholar 

  32. Tan SC, Crouch LI, Jones MR, Welland M (2012) Generation of alternating current in response to discontinuous illumination by photoelectrochemical cells based on photosynthetic proteins. Angew Chem Int Ed 51(27):6667–6671. doi:10.1002/anie.201200466

    Article  CAS  Google Scholar 

  33. Kothe T, Pöller S, Zhao F, Fortgang P, Rögner M, Schuhmann W, Plumeré N (2014) Engineered electron-transfer chain in photosystem 1 based photocathodes outperforms electron-transfer rates in natural photosynthesis. Chem Eur J 20(35):11029–11034. doi:10.1002/chem.201402585

    Article  CAS  Google Scholar 

  34. Stieger KR, Feifel SC, Lokstein H, Lisdat F (2014) Advanced unidirectional photocurrent generation via cytochrome c as reaction partner for directed assembly of photosystem I. Phys Chem Chem Phys 16(29):15667–15674. doi:10.1039/c4cp00935e

    Article  CAS  Google Scholar 

  35. Manocchi AK, Baker DR, Pendley SS, Nguyen K, Hurley MM, Bruce BD, Sumner JJ, Lundgren CA (2013) Photocurrent generation from surface assembled photosystem I on alkanethiol modified electrodes. Langmuir 29(7):2412–2419. doi:10.1021/la304477u

    Article  CAS  Google Scholar 

  36. Feifel SC, Stieger KR, Lokstein H, Lux H, Lisdat F (2015) High photocurrent generation by photosystem I on artificial interfaces composed of π-system-modified graphene. J Mater Chem A 3(23):12188–12196. doi:10.1039/C5TA00656B

    Article  CAS  Google Scholar 

  37. Börner RA (2016) Isolation and cultivation of anaerobes. Adv Biochem Eng Biotechnol. doi:10.1007/10_2016_1

    Google Scholar 

  38. Limoges B, Marchal D, Mavré F, Savéant JM (2006) Electrochemistry of immobilized redox enzymes: kinetic characteristics of NADH oxidation catalysis at diaphorase monolayers affinity immobilized on electrodes. J Am Chem Soc 128(6):2084–2092. doi:10.1021/ja0569196

    Article  CAS  Google Scholar 

  39. Heering HA, Hirst J, Armstrong FA (1998) Interpreting the catalytic voltammetry of electroactive enzymes adsorbed on electrodes. J Phys Chem B 102(35):6889–6902. doi:10.1021/jp981023r

    Article  CAS  Google Scholar 

  40. Proux-Delrouyre V, Demaille C, Leibl W, Sétif P, Bottin H, Bourdillon C (2003) Electrocatalytic investigation of light-induced electron transfer between cytochrome c6 and photosystem I. J Am Chem Soc 125(45):13686–13692. doi:10.1021/ja0363819

    Article  CAS  Google Scholar 

  41. Munge B, Das SK, Ilagan R, Pendon Z, Yang J, Frank HA, Rusling JF (2003) Electron transfer reactions of redox cofactors in spinach photosystem I reaction center protein in lipid films on electrodes. J Am Chem Soc 125(41):12457–12463. doi:10.1021/ja036671p

    Article  CAS  Google Scholar 

  42. Alcantara K, Munge B, Pendon Z, Frank HA, Rusling JF (2006) Thin film voltammetry of spinach photosystem II. Proton-gated electron transfer involving the Mn 4 cluster. J Am Chem Soc 128(46):14930–14937. doi:10.1021/ja0645537

    Article  CAS  Google Scholar 

  43. Faulkner R, Bard AJ (2001) Electrochemical methods: fundamentals and applications, 2nd edn. Wiley, New York

    Google Scholar 

  44. Artero V, Saveant JM (2014) Toward the rational benchmarking of homogeneous H2-evolving catalysts. Energy Environ Sci 7(11):3808–3814. doi:10.1039/C4EE01709A

    Article  CAS  Google Scholar 

  45. Allen H, Hill O, Walton NJ, Whitford D (1985) The coupling of heterogeneous electron transfer to photosystem 1. J Electroanal Chem Interfacial Electrochem 187(1):109–119. doi:10.1016/0368-1874(85)85579-9

    Article  Google Scholar 

  46. Kato M, Zhang JZ, Paul N, Reisner E (2014) Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem Soc Rev 43(18):6485–6497. doi:10.1039/c4cs00031e

    Article  CAS  Google Scholar 

  47. Boschloo G, Hagfeldt A (2009) Characteristics of the iodide/triiodide redox mediator in dye-sensitized solar cells. Acc Chem Res 42(11):1819–1826. doi:10.1021/ar900138m

    Article  CAS  Google Scholar 

  48. Gratzel M (2001) Molecular photovoltaics that mimic photosynthesis. Pure Appl Chem 73(3):459–467. doi:10.1351/pac200173030459

    Article  CAS  Google Scholar 

  49. Larom S, Salama F, Schuster G, Adir N (2010) Engineering of an alternative electron transfer path in photosystem II. Proc Natl Acad Sci U S A 107(21):9650–9655. doi:10.1073/pnas.1000187107

    Article  CAS  Google Scholar 

  50. Heinz S, Liauw P, Nickelsen J, Nowaczyk M (2016) Analysis of photosystem II biogenesis in cyanobacteria. Biochim Biophys Acta 1857(3):274–287. doi:10.1016/j.bbabio.2015.11.007

    Article  CAS  Google Scholar 

  51. Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta 1817(1):209–217. doi:10.1016/j.bbabio.2011.04.014

    Article  CAS  Google Scholar 

  52. Plumeré N (2012) Single molecules: a protein in the spotlight. Nat Nanotechnol 7(10):616–617. doi:10.1038/nnano.2012.175

    Article  Google Scholar 

  53. Hwang ET, Sheikh K, Orchard KL, Hojo D, Radu V, Lee CY, Ainsworth E, Lockwood C, Gross MA, Adschiri T, Reisner E, Butt JN, Jeuken LJC (2015) A decaheme cytochrome as a molecular electron conduit in dye-sensitized photoanodes. Adv Funct Mater 25(15):2308–2315. doi:10.1002/adfm.201404541

    Article  CAS  Google Scholar 

  54. Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37(3):239–247

    Article  CAS  Google Scholar 

  55. Plumeré N (2013) Interferences from oxygen reduction reactions in bioelectroanalytical measurements: the case study of nitrate and nitrite biosensors. Anal Bioanal Chem 405(11):3731–3738. doi:10.1007/s00216-013-6827-z

    Article  Google Scholar 

  56. Plumeré N, Henig J, Campbell WH (2012) Enzyme-catalyzed O2 removal system for electrochemical analysis under ambient air: application in an amperometric nitrate biosensor. Anal Chem 84(5):2141–2146. doi:10.1021/ac2020883

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Ruhr-University Bochum, Bochum, Germany

    Nicolas Plumeré & Marc M. Nowaczyk

Authors
  1. Nicolas Plumeré
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marc M. Nowaczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicolas Plumeré .

Editor information

Editors and Affiliations

  1. School of Biomedical Sciences, University of Leeds, Leeds, LS2 9JT, United Kingdom

    Lars J.C. Jeuken

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Plumeré, N., Nowaczyk, M.M. (2016). Biophotoelectrochemistry of Photosynthetic Proteins. In: Jeuken, L. (eds) Biophotoelectrochemistry: From Bioelectrochemistry to Biophotovoltaics. Advances in Biochemical Engineering/Biotechnology, vol 158. Springer, Cham. https://doi.org/10.1007/10_2016_7

Download citation

Publish with us

Policies and ethics

Search

Navigation