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.

  • Letter
  • Published:

Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature

Abstract

Photosynthesis makes use of sunlight to convert carbon dioxide into useful biomass and is vital for life on Earth. Crucial components for the photosynthetic process are antenna proteins, which absorb light and transmit the resultant excitation energy between molecules to a reaction centre. The efficiency of these electronic energy transfers has inspired much work on antenna proteins isolated from photosynthetic organisms to uncover the basic mechanisms at play1,2,3,4,5. Intriguingly, recent work has documented6,7,8 that light-absorbing molecules in some photosynthetic proteins capture and transfer energy according to quantum-mechanical probability laws instead of classical laws9 at temperatures up to 180 K. This contrasts with the long-held view that long-range quantum coherence between molecules cannot be sustained in complex biological systems, even at low temperatures. Here we present two-dimensional photon echo spectroscopy10,11,12,13 measurements on two evolutionarily related light-harvesting proteins isolated from marine cryptophyte algae, which reveal exceptionally long-lasting excitation oscillations with distinct correlations and anti-correlations even at ambient temperature. These observations provide compelling evidence for quantum-coherent sharing of electronic excitation across the 5-nm-wide proteins under biologically relevant conditions, suggesting that distant molecules within the photosynthetic proteins are ‘wired’ together by quantum coherence for more efficient light-harvesting in cryptophyte marine algae.

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: Structure and spectroscopy of cryptophyte antenna proteins.
Figure 2: Two-dimensional photon echo data for PC645.
Figure 3: Two-dimensional photon echo data for PE545.

Similar content being viewed by others

References

  1. Green, B. R. & Parson, W. W. eds. Light-Harvesting Antennas in Photosynthesis (Kluwer, Dordrecht, 2003)

    Book  Google Scholar 

  2. Scholes, G. D. Long-range resonance energy transfer in molecular systems. Annu. Rev. Phys. Chem. 54, 57–87 (2003)

    Article  ADS  CAS  Google Scholar 

  3. Jang, S., Newton, M. D. & Silbey, R. J. Multichromophoric Förster resonance energy transfer from B800 to B850 in the light harvesting complex 2: evidence for subtle energetic optimization by purple bacteria. J. Phys. Chem. B 111, 6807–6814 (2007)

    Article  CAS  Google Scholar 

  4. Cheng, Y. C. & Fleming, G. R. Dynamics of light harvesting in photosynthesis. Annu. Rev. Phys. Chem. 60, 241–262 (2009)

    Article  ADS  CAS  Google Scholar 

  5. van Grondelle, R. & Novoderezhkin, V. I. Energy transfer in photosynthesis: experimental insights and quantitative models. Phys. Chem. Chem. Phys. 8, 793–807 (2006)

    Article  CAS  Google Scholar 

  6. Engel, G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782–786 (2007)

    Article  ADS  CAS  Google Scholar 

  7. Lee, H., Cheng, Y. C. & Fleming, G. R. Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science 316, 1462–1465 (2007)

    Article  ADS  CAS  Google Scholar 

  8. Mercer, I. P. et al. Instantaneous mapping of coherently coupled electronic transitions and energy transfers in a photosynthetic complex using angle-resolved coherent optical wave-mixing. Phys. Rev. Lett. 102, 057402 (2009)

    Article  ADS  Google Scholar 

  9. Feynman, R. P. Space-time approach to non-relativistic quantum mechanics. Rev. Mod. Phys. 20, 367–387 (1948)

    Article  ADS  MathSciNet  Google Scholar 

  10. Jonas, D. M. Two-dimensional femtosecond spectroscopy. Annu. Rev. Phys. Chem. 54, 425–463 (2003)

    Article  ADS  CAS  Google Scholar 

  11. Brixner, T., Mancal, T., Stiopkin, I. V. & Fleming, G. R. Phase-stabilized two-dimensional electronic spectroscopy. J. Chem. Phys. 121, 4221–4236 (2004)

    Article  ADS  CAS  Google Scholar 

  12. Cho, M. H. Coherent two-dimensional optical spectroscopy. Chem. Rev. 108, 1331–1418 (2008)

    Article  CAS  Google Scholar 

  13. Abramavicius, D. et al. Coherent multidimensional optical spectroscopy of excitons in molecular aggregates; quasiparticle versus supermolecule perspectives. Chem. Rev. 109, 2350–2408 (2009)

    Article  CAS  Google Scholar 

  14. Spear-Bernstein, L. & Miller, K. R. Unique location of the phycobiliprotein light-harvesting pigment in the cryptophyceae. J. Phycol. 25, 412–419 (1989)

    Article  CAS  Google Scholar 

  15. van der Weij-De Wit, C. D. et al. Phycocyanin sensitizes both photosystem I and photosystem II in cryptophyte Chroomonas CCMP270 cells. Biophys. J. 94, 2423–2433 (2008)

    Article  CAS  Google Scholar 

  16. Wilk, K. E. et al. Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: crystal structure of a cryptophyte phycoerythrin at 1.63-Ångstrom resolution. Proc. Natl Acad. Sci. USA 96, 8901–8906 (1999)

    Article  ADS  CAS  Google Scholar 

  17. Wedemayer, G. J., Kidd, D. G., Wemmer, D. E. & Glazer, A. N. Phycobilins of cryptophycean algae: occurrence of dihydrobiliverdin and mesobiliverdin in cryptomonad biliproteins. J. Biol. Chem. 267, 7315–7331 (1992)

    CAS  PubMed  Google Scholar 

  18. Mirkovic, T. et al. Ultrafast light harvesting dynamics in the cryptophyte phycocyanin 645. Photochem. Photobiol. Sci. 6, 964–975 (2007)

    CAS  PubMed  Google Scholar 

  19. Scholes, G. D. & Rumbles, G. Excitons in nanoscale systems. Nature Mater. 5, 683–696 (2006)

    Article  ADS  CAS  Google Scholar 

  20. Doust, A. B. et al. Developing a structure-function model for the cryptophyte phycoerythrin 545 using ultrahigh resolution crystallography and ultrafast laser spectroscopy. J. Mol. Biol. 344, 135–153 (2004)

    Article  ADS  CAS  Google Scholar 

  21. Scholes, G. D. et al. How solvent controls electronic energy transfer and light harvesting. J. Phys. Chem. B 111, 6978–6982 (2007)

    Article  CAS  Google Scholar 

  22. Rhodes, W. Radiationless transitions in isolated molecules. the effects of molecular size and radiation bandwidth. J. Chem. Phys. 50, 2885–2896 (1969)

    Article  ADS  CAS  Google Scholar 

  23. Cheng, Y. C. & Fleming, G. R. Coherence quantum beats in two-dimensional electronic spectroscopy. J. Phys. Chem. A 112, 4254–4260 (2008)

    Article  CAS  Google Scholar 

  24. Rackovsky, S. & Silbey, R. Electronic-energy transfer in impure solids. 1. 2 molecules embedded in a lattice. Mol. Phys. 25, 61–72 (1973)

    Article  ADS  CAS  Google Scholar 

  25. Hwang, H. & Rossky, P. J. Electronic decoherence induced by intramolecular vibrational motions in a betaine dye molecule. J. Phys. Chem. B 108, 6723–6732 (2004)

    Article  CAS  Google Scholar 

  26. Franco, I., Shapiro, M. & Brumer, P. Femtosecond dynamics and laser control of charge transport in trans-polyacetylene. J. Chem. Phys. 128, 244905 (2008)

    Article  ADS  Google Scholar 

  27. Collini, E. & Scholes, G. D. Coherent intrachain energy migration in a conjugated polymer at room temperature. Science 323, 369–373 (2009)

    Article  ADS  CAS  Google Scholar 

  28. Beljonne, D., Curutchet, C., Scholes, G. D. & Silbey, R. Beyond Förster resonance energy transfer in biological and nanoscale systems. J. Phys. Chem. B 113, 6583–6599 (2009)

    Article  CAS  Google Scholar 

  29. Langhoff, C. A. & Robinson, G. W. Time decay and untangling of vibronically tangled resonances: naphthalene second singlet. Chem. Phys. 6, 34–53 (1974)

    Article  CAS  Google Scholar 

  30. Jang, S. Theory of coherent resonance energy transfer for coherent initial condition. J. Chem. Phys. 131, 164101 (2009)

    Article  ADS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Sciences and Engineering Research Council of Canada and the Australian Research Council. G.D.S. acknowledges the support of an EWR Steacie Memorial Fellowship.

Author Contributions E.C. performed the experiments on PC645 and analysed those data. C.Y.W. performed the experiments on PE545 and analysed those data. K.E.W. prepared the samples. P.M.G.C. and G.D.S. designed the research. P.B. and G.D.S. examined the interpretation of the results. G.D.S. wrote the paper. All authors discussed the results and commented on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gregory D. Scholes.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains a Supplementary Data, Supplementary Figures S1- S9 with Legends, Supplementary Tables S1- S9 and Supplementary References. (PDF 10391 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Collini, E., Wong, C., Wilk, K. et al. Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463, 644–647 (2010). https://doi.org/10.1038/nature08811

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature08811

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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