Photosynthesis Research

, Volume 127, Issue 2, pp 161–170 | Cite as

Enhanced photocurrent from Photosystem I upon in vitro truncation of the antennae chlorophyll

  • J. Ridge Carter
  • David R. Baker
  • T. Austin Witt
  • Barry D. Bruce
Regular Paper

Abstract

Current effects on climate change and dwindling fossil fuel reserves require new materials and methods to convert solar energy into a viable clean energy source. Recent progress in the direct conversion of light into photocurrent has been well documented using Photosystem I. In plants, PSI consists of a core complex and multiple light-harvesting complexes, denoted LHCI and LHCII. Most of the methods for isolating PSI from plants involve a selective, detergent solubilization from thylakoids followed by sucrose gradient density centrifugation. These processes isolate one variant of PSI with a specific ratio of Chl:P700. In this study, we have developed a simple and potentially scalable method for isolating multiple PSI variants using Hydroxyapatite chromatography, which has been well documented in other Photosystem I isolation protocols. By varying the wash conditions, we show that it is possible to change the Chl:P700 ratios. These different PSI complexes were cast into a PSI–Nafion–osmium polymer film that enabled their photoactivity to be measured. Photocurrent increases nearly 400 % between highly washed and untreated solutions based on equal chlorophyll content. Importantly, the mild washing conditions remove peripheral Chl and some LHCI without inhibiting the photochemical activity of PSI as suggested by SDS-PAGE analysis. This result could indicate that more P700 could be loaded per surface area for biohybrid devices. Compared with other PSI isolations, this protocol also allows isolation of multiple PSI variants without loss of photochemical activity.

Keywords

Photosystem I Hydroxyapatite Photocurrent Chlorophyll Light-harvesting complex I, II 

Notes

Acknowledgments

We would like to thank the Army Research Laboratories (ARL Contract #W91 1NF-11-2-0029), TN-SCORE sponsored by NSF-EPSCoR (EPS-1004083), and the Gibson Family Foundation for the generous funding for this project. We also appreciate the support and feedback provided by Khoa Nguyen, Prakitchai Chotewutmontri, and Richard Simmerman, and Ed Wright while conducting this research.

References

  1. Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291:25–29CrossRefGoogle Scholar
  2. Amunts A, Drory O, Nelson N (2007) The structure of a plant Photosystem I supercomplex at 3.4 Å resolution. Nature 447:58–63. doi:10.1038/nature05687 PubMedCrossRefGoogle Scholar
  3. Amunts A, Toporik H, Borovikova A, Nelson N (2010) Structure determination and improved model of plant Photosystem I. J Biol Chem 285:3478–3486. doi:10.1074/jbc.M109.072645 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Armaroli N, Balzani V (2006) The future of energy supply: challenges and opportunities. Angew Chemi Int Ed 45:2–17Google Scholar
  5. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedPubMedCentralCrossRefGoogle Scholar
  6. Baker DR et al (2014a) Comparative photoactivity and stability of isolated cyanobacterial monomeric and trimeric Photosystem I. J Phys Chem B 118:2703–2711. doi:10.1021/jp407948p PubMedCrossRefGoogle Scholar
  7. Baker DR, Simmerman RF, Sumner JJ, Bruce BD, Lundgren CA (2014b) Photoelectrochemistry of Photosystem I bound in nafion. Langmuir. doi:10.1021/la503132h Google Scholar
  8. Bruce BD, Malkin R (1988) Subunit stoichiometry of the chloroplast Photosystem I complex. J Biol Chem 263:7302–7308PubMedGoogle Scholar
  9. Ciesielski PN, Scott AM, Faulkner CJ, Berron BJ, Cliffel DE, Jennings GK (2008) Functionalized nanoporous gold leaf electrode films for the immobilization of Photosystem I. ACS Nano 2:2465–2472. doi:10.1021/nn800389k PubMedCrossRefGoogle Scholar
  10. Ciesielski PN et al (2010a) Photosystem I: based biohybrid photoelectrochemical cells. Bioresour Technol 101:3047–3053. doi:10.1016/j.biortech.2009.12.045 PubMedCrossRefGoogle Scholar
  11. Ciesielski PN, Faulkner CJ, Iwin JM, Gregory JM, Tolk NH, Cliffel DE, Jennings GK (2010b) Enhanced photocurrent by Photosystem I multilayer assemblies. Adv Funct Mater 20:4048–4054. doi:10.1002/adfm.201001193 CrossRefGoogle Scholar
  12. Cummings LJ, Snyder MA, Brisack K (2009) Protein chromatography on hydroxyapatite columns. Methods Enzymol 463:387–404. doi:10.1016/S0076-6879(09)63024-X PubMedCrossRefGoogle Scholar
  13. Drop B, Webber-Birungi M, Fusetti F, Kouril R, Redding KE, Boekema EJ, Croce R (2011) Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 286:44878–44887. doi:10.1074/jbc.M111.301101 PubMedPubMedCentralCrossRefGoogle Scholar
  14. Fromme P, Jordan P, Krauss N (2001) Structure of Photosystem I. Biochim Biophys Acta 1507:5–31. doi:10.1016/S0005-2728(01)00195-5 PubMedCrossRefGoogle Scholar
  15. Gagnon P (2010) Hydroxyapatite for biomolecule purification. Genet Eng and Biotechnol News 30(7):28Google Scholar
  16. Gerster D et al (2012) Photocurrent of a single photosynthetic protein. Nat Nanotechnol 7:673–676. doi:10.1038/nnano.2012.165 PubMedCrossRefGoogle Scholar
  17. Gunther D, LeBlanc G, Praisi D, Zhang JR, Cliffel DE, Bolotin KI, Jennings GK (2013) Photosystem I on graphene as a highly transparent, photoactive electrode. Langmuir 29:4177–4180. doi:10.1021/la305020c PubMedCrossRefGoogle Scholar
  18. Haworth P, Watson JL, Arntzen CJ (1983) The detection, isolation and characterization of a light-harvesting complex which is specifically associated with Photosystem I. Biochim Biophys Acta 724:151–158CrossRefGoogle Scholar
  19. Hiyama T (2004) Isolation of Photosystem I particles from spinach. Methods Mol Biol 274:11–17. doi:10.1385/1-59259-799-8:011 PubMedGoogle Scholar
  20. Hiyama T, Ke B (1972) Difference spectra and extinction coefficients of P700. Biochim Biophys Acta 267:160–171. doi:10.1016/0005-2728(72)90147-8 PubMedCrossRefGoogle Scholar
  21. Ikeuchi M, Hirano A, Inoue Y (1991) Correspondence of apoproteins of light-harvesting chlorophyll a/b complexes associated with Photosystem I to cab genes: evidence for a novel type IV apoprotein. Plant Cell Physiol 32:103–112Google Scholar
  22. Khrouchtchova A et al (2005) A previously found thylakoid membrane protein of 14 kDa (TMP14) is a novel subunit of plant Photosystem I and is designated PSI-P. FEBS Lett 579:4808–4812PubMedCrossRefGoogle Scholar
  23. Kirst H, Garcia-Cerdan JG, Zurbriggen A, Ruehle T, Melis A (2012) Truncated Photosystem chlorophyll antenna size in the green microalga Chlamydomonas reinhardtii upon deletion of the TLA3-CpSRP43 gene. Plant Physiol 160:2251–2260. doi:10.1104/pp.112.206672 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Knoetzel J, Mant A, Haldrup A, Jensen PE, Scheller HV (2002) PSI-O, a new 10-kDa subunit of eukaryotic Photosystem I. FEBS Lett 510:145–148PubMedCrossRefGoogle Scholar
  25. Kuritz T, Lee I, Owens ET, Humayun M, Greenbaum E (2005) Molecular photovoltaics and the photoactivation of mammalian cells. IEEE Trans Nanobiosci 4:196–200CrossRefGoogle Scholar
  26. LeBlanc G, Chen G, Gizzie EA, Jennings GK, Cliffel DE (2012) Enhanced photocurrents of Photosystem I films on p-doped silicon. Adv Mater 24:5959–5962. doi:10.1002/adma.201202794 PubMedCrossRefGoogle Scholar
  27. Lee JW, Zipfel W, Owens TG (1992) Quenching of chlorophyll excited states in Photosystem I by quinones: Stern–Volmer analysis of fluorescence and photochemical yield. J Lumin 51:79–89CrossRefGoogle Scholar
  28. Li M, Semchonok DA, Boekema EJ, Bruce BD (2014) Characterization and evolution of tetrameric Photosystem I from the thermophilic cyanobacterium Chroococcidiopsis sp. TS-821. Plant Cell. doi:10.1105/tpc.113.120782 Google Scholar
  29. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280. doi:10.1016/j.plantsci.2009.06.005 CrossRefGoogle Scholar
  30. Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566PubMedPubMedCentralCrossRefGoogle Scholar
  31. Mullet JE, Burke JJ, Arntzen CJ (1980) Chlorophyll proteins of Photosystem I. Plant Physiol 65:814–822PubMedPubMedCentralCrossRefGoogle Scholar
  32. Nelson N (2009) Plant photosystem I—the most efficient nano-photochemical machine. J Nanosci Nanotechnol 9:1709–1713Google Scholar
  33. Nelson N, Ben-Shem A (2005) The structure of Photosystem I and evolution of photosynthesis. BioEssays 27:914–922. doi:10.1002/bies.20278 PubMedCrossRefGoogle Scholar
  34. Nguyen K, Bruce BD (2014) Growing green electricity: progress and strategies for use of Photosystem I for sustainable photovoltaic energy conversion. Biochim Biophys Acta. doi:10.1016/j.bbabio.2013.12.013 Google Scholar
  35. Shiozawa JA, Alberte RS, Thornber JP (1974) The P700-chlorophyll a-protein. Isolation and some characteristics of the complex in higher plants. Arch Biochem Biophys 165:388–397PubMedCrossRefGoogle Scholar
  36. Zilber AL, Malkin R (1992) Organization and topology of Photosystem I subunits. Plant Physiol 99:901–911PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • J. Ridge Carter
    • 1
  • David R. Baker
    • 2
  • T. Austin Witt
    • 1
  • Barry D. Bruce
    • 1
    • 3
  1. 1.Department of Biochemistry and Cellular and Molecular BiologyUniversity of TennesseeKnoxvilleUSA
  2. 2.Sensors and Electron Devices DirectorateUnited States Army Research LaboratoryAdelphiUSA
  3. 3.Program in Energy Science and EngineeringUniversity of TennesseeKnoxvilleUSA

Personalised recommendations