Skip to main content
Log in

Chemical oxidation of the FMO antenna protein from Chlorobaculum tepidum

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Effect of chemical oxidation by ferricyanide on bacteriochlorophyll a (BChl a) in the Fenna–Matthews–Olson protein (FMO) was studied using absorbance and fluorescence spectroscopy at ambient and cryogenic temperatures. Partially selective oxidation of pigments bound to the antenna complex was achieved and the probable absorption wavelength corresponding to the recently discovered bacteriochlorophyll No. 8 of 806 nm was obtained by comparative analysis of the effect of chemical oxidation and the effect of different isolation procedures. Formation of a stable product identified as a chlorophyll a derivative occurred upon chemical oxidation. This new pigment remained bound within the pigment–protein complex, and exhibited an efficient energy transfer to BChl a. Furthermore, complex effects of the pigment oxidation upon the fluorescence yield of the FMO protein were observed. Utility of this approach based on chemical modifications for the investigation of the native regulatory mechanisms involved in the energy transfer in the FMO protein is discussed.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

BChl a :

Bacteriochlorophyll a

da-Chl a :

3-Desvinyl-3-acetyl chlorophyll a

DDQ:

2,3-Dichloro-5,6-dicyano-p-benzoquinone

FeCy:

Ferricyanide

FMO:

Fenna–Matthews–Olson protein

LH:

Purple-bacterial light-harvesting complex

RC:

Reaction center

References

  • Ben-Shem A, Frolow F, Nelson N (2004) Evolution of photosystem I-from symmetry through pseudosymmetry to asymmetry. FEBS Lett 564:274–280

    Article  PubMed  CAS  Google Scholar 

  • Blankenship RE, Matsuura K (2003) Antenna complexes from green photosynthetic bacteria. In: Green BR, Parsons WW (eds) Light-harvesting antennas. Kluwer Academic Publishers, Dordrecht, pp 1–23

    Google Scholar 

  • Bryant DA, Costas AMG, Maresca JA, Chew AGM, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–526

    Article  PubMed  CAS  Google Scholar 

  • Caycedo-Soler F, Chin AW, Almeida J, Huelga SF, Plenio MB (2012) The nature of the low energy band of the Fenna–Matthews–Olson complex: vibronic signatures. J Chem Phys 136:15510221

    Article  Google Scholar 

  • Chauvet JP, Viovy R, Santus R, Land EJ (1981) One-electron Oxidation of photosynthetic pigments in micelles-bacteriochlorophyll a, chlorophyll a, chlorophyll b and pheophytin a. J Phys Chem 85:3449–3456

    Article  CAS  Google Scholar 

  • Cho M, Vaswani HM, Brixner T, Stenger J, Fleming GR (2005) Exciton analysis in 2D electronic spectroscopy. J Phys Chem B 109:10542–10556

    Article  PubMed  CAS  Google Scholar 

  • Cotton TM, Van Duyne RP (1979) An electrochemical investigation of the redox properties of bacteriochlorophyll and bacteriopheophytin in aprotic solvents. J Am Chem Soc 101:7605–7612

    Article  CAS  Google Scholar 

  • Fajer J, Borg DC, Forman A, Felton RH, Dolphin D, Vegh L (1974) The cation radicals of free base and zinc bacteriochlorin, bacteriochlorophyll, and bacteriopheophytin. Proc Natl Acad Sci USA 71:994–998

    Article  PubMed  CAS  Google Scholar 

  • Fajer J, Brune DC, Davis MS, Forman A, Spaulding LD (1975) Primary charge separation in bacterial photosynthesis: oxidized chlorophylls and reduced pheophytin. Proc Natl Acad Sci USA 72:4956–4960

    Article  PubMed  CAS  Google Scholar 

  • Fenna RE, Matthews BW (1975) Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium-limicola. Nature 258:573–577

    Article  CAS  Google Scholar 

  • Fidler AF, Caram JR, Hayes D, Engel GS (2012) Towards a coherent picture of excitonic coherence in the Fenna–Matthews–Olson complex. J Phys B 45:154013

    Article  Google Scholar 

  • Gomez I, Sieiro C, Ramirez JM, Gomez-Amores S, del Campo FF (1982) The antenna system of Rhodospirillum rubrum: radical formation upon dark oxidation of bulk bacteriochlorophyll. FEBS Lett 144:117–120

    Article  CAS  Google Scholar 

  • Hayes D, Engel GS (2011) Extracting the excitonic Hamiltonian of the Fenna–Matthews–Olson complex using three-dimensional third-order electronic spectroscopy. Biophys J 100:2043–2052

    Article  PubMed  CAS  Google Scholar 

  • Hohmann-Marriott MF, Blankenship RE (2007) Variable fluorescence in green sulfur bacteria. Biochim Biophys Acta 1767:106–113

    Article  PubMed  CAS  Google Scholar 

  • Kropacheva TN, Hoff AJ (2001) Electrochemical oxidation of bacteriochlorophyll a in reaction centers and antenna complexes of photosynthetic bacteria. J Phys Chem B 105:5536–5545

    Article  CAS  Google Scholar 

  • Law CJ, Cogdell RJ (1998) The effect of chemical oxidation on the fluorescence of the LH1 (B880) complex from the purple bacterium Rhodobium marinum. FEBS Lett 432:27–30

    Article  PubMed  CAS  Google Scholar 

  • Milder MTW, Brüggemann B, van Grondelle R, Herek JL (2010) Revisiting the optical properties of the FMO protein. Photosynth Res 104:257–274

    Article  PubMed  CAS  Google Scholar 

  • Moix J, Wu J, Huo P, Coker D, Cao J (2011) Efficient energy transfer in light-harvesting systems, III: the influence of the eighth bacteriochlorophyll on the dynamics and efficiency in FMO. J Phys Chem Lett 2:3045–3052

    Article  CAS  Google Scholar 

  • Montaño GA, Wu HM, Lin S, Brune DC, Blankenship RE (2003) Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry 42:10246–10251

    Article  PubMed  Google Scholar 

  • Müh F, Madjet MEA, Adolphs J, Abdurahman A, Rabenstein B, Ishikita H, Knapp EW, Renger T (2007) α-Helices direct excitation energy flow in the Fenna–Matthews–Olson protein. Proc Natl Acad Sci USA 104:16862–16867

    Article  PubMed  Google Scholar 

  • Olbrich C, Jansen TLC, Liebers J, Aghtar M, Strümpfer J, Schulten K, Knoester J, Kleinekathöfer U (2011) From atomistic modeling to excitation transfer and two-dimensional spectra of the FMO light-harvesting complex. J Phys Chem B 115:8609–8621

    Article  PubMed  CAS  Google Scholar 

  • Olson JM (2004) The FMO protein. Photosynth Res 80:181–187

    Article  PubMed  CAS  Google Scholar 

  • Picorel R, Lefebvre S, Gingras G (1984) Oxido-reduction of B800–850 and B880 holochoromes isolated from 3 species of photosynthetic bacteria as studied by electron-paramagnetic resonance and optical spectroscopy. Eur J Biochem 142:305–311

    Article  CAS  Google Scholar 

  • Schmidt am Busch M, Müh F, Madjet ME, Renger T (2011) The eighth bacteriochlorophyll completes the excitation energy funnel in the FMO protein. J Phys Chem Lett 2:93–98

    Article  CAS  Google Scholar 

  • Smith JRL, Calvin M (1966) Studies on the chemical and photochemical oxidation of bacteriochlorophyll. J Am Chem Soc 88:4500–4506

    Article  Google Scholar 

  • Tronrud DE, Wen JZ, Gay L, Blankenship RE (2009) The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosynth Res 100:79–87

    Article  PubMed  CAS  Google Scholar 

  • Vulto SIE, de Baat MA, Louwe RJW, Permentier HP, Neef T, Miller M, van Amerongen H, Aartsma TJ (1998) Exciton simulations of optical spectra of the FMO complex from the green sulfur bacterium Chlorobium tepidum at 6 K. J Phys Chem B 102:9577–9582

    Article  CAS  Google Scholar 

  • Wahlund TM, Woese CR, Castenholz RW, Madigan MT (1991) A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch Microbiol 156:81–90

    Article  CAS  Google Scholar 

  • Wen JZ, Zhang H, Gross ML, Blankenship RE (2009) Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting. Proc Natl Acad Sci USA 106:6134–6139

    Article  PubMed  CAS  Google Scholar 

  • Wen JZ, Zhang H, Gross ML, Blankenship RE (2011) Native electrospray mass spectrometry reveals the nature and stoichiometry of pigments in the FMO photosynthetic antenna protein. Biochemistry 50:3502–3511

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, LoBrutto R, Lin S, Blankenship RE (1994) Redox effects on the bacteriochlorophyll a-containing Fenna–Matthews–Olson protein from Chlorobium tepidum. Photosynth Res 41:89–96

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Jianzhong Wen for providing us with the detergent-isolated FMO samples. Funding for this work was provided by U.S. Department of Energy Grant DE-FG02-10ER15846 to R.E.B. from the Photosynthetic Systems program of the Basic Energy Sciences Division.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert E. Blankenship.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bina, D., Blankenship, R.E. Chemical oxidation of the FMO antenna protein from Chlorobaculum tepidum . Photosynth Res 116, 11–19 (2013). https://doi.org/10.1007/s11120-013-9878-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9878-2

Keywords

Navigation