Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

In situ mapping of the energy flow through the entire photosynthetic apparatus

Abstract

Absorption of sunlight is the first step in photosynthesis, which provides energy for the vast majority of organisms on Earth. The primary processes of photosynthesis have been studied extensively in isolated light-harvesting complexes and reaction centres, however, to understand fully the way in which organisms capture light it is crucial to also reveal the functional relationships between the individual complexes. Here we report the use of two-dimensional electronic spectroscopy to track directly the excitation-energy flow through the entire photosynthetic system of green sulfur bacteria. We unravel the functional organization of individual complexes in the photosynthetic unit and show that, whereas energy is transferred within subunits on a timescale of subpicoseconds to a few picoseconds, across the complexes the energy flows at a timescale of tens of picoseconds. Thus, we demonstrate that the bottleneck of energy transfer is between the constituents.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The absorption spectrum of the intact C. tepidum cells (solid line) compared with the spectrum of isolated chlorosomes (dashed line) at 77 K.
Figure 2: The selected 2D spectra (absorptive part) of the intact C. tepidum cells measured between 11,900 and 13,200 cm−1 (760–840 nm) at the indicated population times at 77 K.
Figure 3: Decay-associated spectra of the FMO–RC spectral region.
Figure 4: Decay-associated spectra of the chlorosome excitation region.
Figure 5: A scheme of the excitation-energy flow through the entire photosynthetic apparatus of C. tepidum.

Similar content being viewed by others

References

  1. Overmann, J., Cypionka, H. & Pfennig, N. An extremely low-light-adapted phototrophic sulfur bacterium from the Black Sea. Limnol. Oceanogr. 37, 150–155 (1992).

    Article  CAS  Google Scholar 

  2. Beatty, J. T. et al. An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc. Natl Acad. Sci. USA 102, 9306–9310 (2005).

    Article  CAS  Google Scholar 

  3. Pšenčík, J., Butcher, S. & Tuma, R. in Structural Basis of Biological Energy Generation (ed. Hohmann-Marriott, M. F.) 77–109 (Advances in Photosynthesis and Respiration 39, Springer Netherlands, 2014).

    Book  Google Scholar 

  4. Hauska, G., Schoedl, T., Remigy, H. & Tsiotis, G. The reaction center of green sulfur bacteria. Biochim. Biophys. Acta 1507, 260–277 (2001).

    Article  CAS  Google Scholar 

  5. Wen, J., Zhang, H., Gross, M. L. & Blankenship, R. E. 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 (2009).

    Article  CAS  Google Scholar 

  6. Bína, D., Gardian, Z., Vácha, F. & Litvín, R. Native FMO-reaction center supercomplex in green sulfur bacteria: an electron microscopy study. Photosynth. Res. 128, 93–102 (2016).

    Article  Google Scholar 

  7. Milder, M. T. W., Brüggemann, B., van Grondelle, R. & Herek, J. L. Revisiting the optical properties of the FMO protein. Photosynth. Res. 104, 257–274 (2010).

    Article  CAS  Google Scholar 

  8. Mimuro, M. et al. Excitation energy flow in chlorosome antennas of green photosynthetic bacteria. J. Phys. Chem. 93, 7503–7509 (1989).

    Article  CAS  Google Scholar 

  9. Müller, M. G., Griebenow, K. & Holzwarth, A. R. Picosecond energy transfer and trapping kinetics in living cells of the green bacterium Chloroflexus aurantiacus. Biochim. Biophys. Acta 1144, 161–169 (1993).

    Article  Google Scholar 

  10. Causgrove, T. P., Brune, D. C., Wang, J., Wittmershaus, B. P. & Blankenship, R. E. Energy transfer kinetics in whole cells and isolated chlorosomes of green photosynthetic bacteria. Photosynth. Res. 26, 39–48 (1990).

    CAS  PubMed  Google Scholar 

  11. Fetisova, Z. G., Freiberg, A. M. & Timpmann, K. E. Long-range molecular order as an efficient strategy for light harvesting in photosynthesis. Nature 334, 633–634 (1988).

    Article  CAS  Google Scholar 

  12. Brixner, T. et al. Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434, 625–628 (2005).

    Article  CAS  Google Scholar 

  13. Zigmantas, D. et al. Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex. Proc. Natl Acad. Sci. USA 103, 12672–12677 (2006).

    Article  CAS  Google Scholar 

  14. Dostál, J., Vácha, F., Pšenčík, J. & Zigmantas, D. 2D electronic spectroscopy reveals excitonic structure in the baseplate of a chlorosome. J. Phys. Chem. Lett. 5, 1743–1747 (2014).

    Article  Google Scholar 

  15. Augulis, R. & Zigmantas, D. Two-dimensional electronic spectroscopy with double modulation lock-in detection: enhancement of sensitivity and noise resistance. Opt. Express 19, 13126–13133 (2011).

    Article  CAS  Google Scholar 

  16. Dahlberg, P. D., Fidler, A. F., Caram, J. R., Long, P. D. & Engel, G. S. Energy transfer observed in live cells using two-dimensional electronic spectroscopy. J. Phys. Chem. Lett. 4, 3636–3640 (2013).

    Article  CAS  Google Scholar 

  17. Huh, J. et al. Atomistic study of energy funneling in the light-harvesting complex of green sulfur bacteria. J. Am. Chem. Soc. 136, 2048–2057 (2014).

    Article  CAS  Google Scholar 

  18. Blankenship, R. E. et al. Redox regulation of energy transfer efficiency in antennas of green photosynthetic bacteria. Photochem. Photobiol. 57, 103–107 (1993).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  20. Otte, S. C., van der Heiden, J. C., Pfennig, N. & Amesz, J. A comparative study of the optical characteristics of intact cells of photosynthetic green sulfur bacteria containing bacteriochlorophyll c, d or e. Photosynth. Res. 28, 77–87 (1991).

    Article  CAS  Google Scholar 

  21. Permentier, H. P. et al. Composition and optical properties of reaction centre core complexes from the green sulfur bacteria Prosthecochloris aestuarii and Chlorobium tepidum. Photosynth. Res. 64, 27–39 (2000).

    Article  CAS  Google Scholar 

  22. van Stokkum, I. H. M., Larsen, D. S. & van Grondelle, R. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta 1657, 82–104 (2004).

    Article  CAS  Google Scholar 

  23. Vulto, S. I. E., Streltsov, A. M. & Aartsma, T. J. Excited state energy relaxation in the FMO complexes of the green bacterium Prosthecochloris aestuarii at low temperatures. J. Phys. Chem. B 101, 4845–4850 (1997).

    Article  CAS  Google Scholar 

  24. Gulbinas, V. et al. Singlet–singlet annihilation and local heating in FMO complexes. J. Phys. Chem. 100, 17950–17956 (1996).

    Article  CAS  Google Scholar 

  25. Adolphs, J. & Renger, T. How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria. Biophys. J. 91, 2778–2797 (2006).

    Article  CAS  Google Scholar 

  26. Vulto, S. I. E. et al. 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 (1998).

    Article  CAS  Google Scholar 

  27. Pšenčík, J., Ma, Y.-Z., Arellano, J. B., Hála, J. & Gillbro, T. Excitation energy transfer dynamics and excited-state structure in chlorosomes of Chlorobium phaeobacteroides. Biophys. J. 84, 1161–1179 (2003).

    Article  Google Scholar 

  28. Oh-oka, H. et al. Transient absorption spectroscopy of energy-transfer and trapping processes in the reaction center complex of Chlorobium tepidum. J. Phys. Chem. B 102, 8190–8195 (1998).

    Article  CAS  Google Scholar 

  29. Kramer, H., Kingma, H., Swarthoff, T. & Amesz, J. Prompt and delayed fluorescence in pigment–protein complexes of a green photosynthetic bacterium. Biochim. Biophys. Acta 681, 359–364 (1982).

    Article  CAS  Google Scholar 

  30. Francke, C., Otte, S. C., Miller, M., Amesz, J. & Olson, J. M. Energy transfer from carotenoid and FMO protein in subcellular preparations from green sulfur bacteria. Spectroscopic characterization of an FMO–reaction center core complex at low temperature. Photosynth. Res. 50, 71–77 (1996).

    Article  CAS  Google Scholar 

  31. Neerken, S., Permentier, H. P., Francke, C., Aartsma, T. J. & Amesz, J. Excited states and trapping in reaction center complexes of the green sulfur bacterium Prosthecochloris aestuarii. Biochemistry 37, 10792–10797 (1998).

    Article  CAS  Google Scholar 

  32. He, G., Niedzwiedzki, D. M., Orf, G. S., Zhang, H. & Blankenship, R. E. Dynamics of energy and electron transfer in the FMO–reaction center core complex from the phototrophic green sulfur bacterium Chlorobaculum tepidum. J. Phys. Chem. B 119, 8321–8329 (2015).

    Article  CAS  Google Scholar 

  33. van Dorssen, R. J. & Amesz, J. Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. III. Energy transfer in whole cells. Photosynth. Res. 15, 177–189 (1988).

    Article  CAS  Google Scholar 

  34. Pšenčík, J. et al. Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys. J. 87, 1165–1172 (2004).

    Article  Google Scholar 

Download references

Acknowledgements

We thank the group of F. Vácha for cell cultivation and for the isolation of the chlorosomes. We are grateful to D. Bína and H. Lokstein for their help with the cell viability experiments described in the Supplementary Information. The work in Lund was supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation. The work in Prague was supported by the Czech Science Foundation (project P501/12/G055).

Author information

Authors and Affiliations

Authors

Contributions

J.D. designed and performed the experiments, analysed the data and wrote the manuscript, J.P. designed and performed the experiments and wrote the manuscript, D.Z. conceived the idea, designed and performed the experiments and wrote the manuscript.

Corresponding author

Correspondence to Donatas Zigmantas.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 332 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dostál, J., Pšenčík, J. & Zigmantas, D. In situ mapping of the energy flow through the entire photosynthetic apparatus. Nature Chem 8, 705–710 (2016). https://doi.org/10.1038/nchem.2525

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchem.2525

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing