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:

Far-red absorption and light-use efficiency trade-offs in chlorophyll f photosynthesis

Nature Plants volume 6, pages 1044–1053 (2020)Cite this article

Subjects

Abstract

Plants and cyanobacteria use the chlorophylls embedded in their photosystems to absorb photons and perform charge separation, the first step of converting solar energy to chemical energy. While oxygenic photosynthesis is primarily based on chlorophyll a photochemistry, which is powered by red light, a few cyanobacterial species can harness less energetic photons when growing in far-red light. Acclimatization to far-red light involves the incorporation of a small number of molecules of red-shifted chlorophyll f in the photosystems, whereas the most abundant pigment remains chlorophyll a. Due to its different energetics, chlorophyll f is expected to alter the excited-state dynamics of the photosynthetic units and, ultimately, their performances. Here we combined time-resolved fluorescence measurements on intact cells and isolated complexes to show that chlorophyll f insertion slows down the overall energy trapping in both photosystems. While this marginally affects the efficiency of photosystem I, it substantially decreases that of photosystem II. Nevertheless, we show that despite the lower energy output, the insertion of red-shifted chlorophylls in the photosystems remains advantageous in environments that are enriched in far-red light and therefore represents a viable strategy for extending the photosynthetically active spectrum in other organisms, including plants. However, careful design of the new photosynthetic units will be required to preserve their efficiency.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Fig. 1: Spectroscopic data of isolated PSI from C. fritschii.
Fig. 2: Spectroscopic data of isolated FRL PSII from C. fritschii.
Fig. 3: Absorption and emission spectra of intact cells of C. fritschii.
Fig. 4: TRF measurements of intact cells of white-light- and FRL-adapted C. fritschii.
Fig. 5: TRF measurements on intact cells of different organisms.
Fig. 6: Light absorption and energy output of photosynthetic units under a dense plant canopy.

Similar content being viewed by others

Data availability

All raw data are available from the corresponding author (R.C.) upon reasonable request.

References

  1. Bryant, D. A. & Frigaard, N. U. Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol. 14, 488–496 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Björn, L. O., Papageorgiou, G. C., Blankenship, R. E. & Govindjee A viewpoint: why chlorophyll a? Photosynth. Res. 99, 85–98 (2009).

    Article  PubMed  CAS  Google Scholar 

  3. Tomo, T. et al. Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. J. Biol. Chem. 283, 18198–18209 (2008).

    Article  CAS  PubMed  Google Scholar 

  4. Renger, T. & Schlodder, E. The primary electron donor of photosystem II of the cyanobacterium Acaryochloris marina is a chlorophyll d and the water oxidation is driven by a chlorophyll a/chlorophyll d heterodimer. J. Phys. Chem. B 112, 7351–7354 (2008).

    Article  CAS  PubMed  Google Scholar 

  5. Tomo, T., Allakhverdiev, S. I. & Mimuro, M. Constitution and energetics of photosystem I and photosystem II in the chlorophyll d-dominated cyanobacterium Acaryochloris marina. J. Photochem. Photobiol. B 104, 333–340 (2011).

    Article  CAS  PubMed  Google Scholar 

  6. Chen, M. et al. A red-shifted chlorophyll. Science 329, 1318–1320 (2010).

    Article  CAS  PubMed  Google Scholar 

  7. Gan, F. et al. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345, 1312–1317 (2014).

    Article  CAS  PubMed  Google Scholar 

  8. Chen, M., Li, Y., Birch, D. & Willows, R. D. A cyanobacterium that contains chlorophyll f—a red-absorbing photopigment. FEBS Lett. 586, 3249–3254 (2012).

    Article  CAS  PubMed  Google Scholar 

  9. Gan, F., Shen, G. & Bryant, D. A. Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life 5, 4–24 (2015).

    Article  CAS  Google Scholar 

  10. Nürnberg, D. J. et al. Photochemistry beyond the red limit in chlorophyll f-containing photosystems. Science 360, 1210–1213 (2018).

    Article  PubMed  CAS  Google Scholar 

  11. Ho, M. Y., Shen, G., Canniffe, D. P., Zhao, C. & Bryant, D. A. Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353, aaf9178 (2016).

    Article  PubMed  CAS  Google Scholar 

  12. Ho, M. Y., Soulier, N. T., Canniffe, D. P., Shen, G. & Bryant, D. A. Light regulation of pigment and photosystem biosynthesis in cyanobacteria. Curr. Opin. Plant Biol. 37, 24–33 (2017).

    Article  CAS  PubMed  Google Scholar 

  13. Li, Y., Vella, N. & Chen, M. Characterization of isolated photosystem I from Halomicronema hongdechloris, a chlorophyll f-producing cyanobacterium. Photosynthetica 56, 306–315 (2018).

    Article  CAS  Google Scholar 

  14. Kurashov, V. et al. Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered photosystem I complexes. Photosynth. Res. 141, 151–163 (2019).

    Article  CAS  PubMed  Google Scholar 

  15. Ho, M.-Y. et al. Extensive remodeling of the photosynthetic apparatus alters energy transfer among photosynthetic complexes when cyanobacteria acclimate to far-red light. Biochim. Biophys. Acta 1861, 148064 (2020).

    Article  CAS  Google Scholar 

  16. Li, Y. et al. Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim. Biophys. Acta 1857, 107–114 (2016).

    Article  CAS  PubMed  Google Scholar 

  17. Ho, M. Y., Gan, F., Shen, G. & Bryant, D. A. Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II. Characterization of phycobiliproteins produced during acclimation to far-red light. Photosynth. Res. 131, 187–202 (2017).

    Article  CAS  PubMed  Google Scholar 

  18. Loughlin, P., Lin, Y. & Chen, M. Chlorophyll d and Acaryochloris marina: current status. Photosynth. Res. 116, 277–293 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. Zamzam, N., Kaucikas, M., Nurnberg, D., Rutherford, A. W. & van Thor, J. J. Femtosecond infrared spectroscopy of chlorophyll f-containing photosystem I. Phys. Chem. Chem. Phys. 21, 1224–1234 (2019).

    Article  CAS  PubMed  Google Scholar 

  20. Hastings, G. et al. Fourier transform visible and infrared difference spectroscopy for the study of P700 in photosystem I from Fischerella thermalis PCC 7521 cells grown under white light and far-red light: evidence that the A–1 cofactor is chlorophyll f. Biochim. Biophys. Acta 1860, 452–460 (2019).

    Article  CAS  Google Scholar 

  21. Kato, K. et al. Structural basis for the adaptation and function of chlorophyll f in photosystem I. Nat. Commun. 11, 238 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gisriel, C. et al. The structure of photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis. Sci. Adv. 6, eaay6415 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Itoh, S. et al. Harvesting far-red light by chlorophyll f in photosystems I and II of unicellular cyanobacterium strain KC1. Plant Cell Physiol. 56, 2024–2034 (2015).

    Article  CAS  PubMed  Google Scholar 

  24. Akimoto, S., Shinoda, T., Chen, M., Allakhverdiev, S. I. & Tomo, T. Energy transfer in the chlorophyll f-containing cyanobacterium, Halomicronema hongdechloris, analyzed by time-resolved fluorescence spectroscopies. Photosynth. Res. 125, 115–122 (2015).

    Article  CAS  PubMed  Google Scholar 

  25. Schmitt, F. J. et al. Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light. Photosynth. Res. 139, 185–201 (2019).

    Article  CAS  PubMed  Google Scholar 

  26. Kaucikas, M., Nürnberg, D., Dorlhiac, G., Rutherford, A. W. & van Thor, J. J. Femtosecond visible transient absorption spectroscopy of chlorophyll f-containing photosystem I. Biophys. J. 112, 234–249 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ho, M. Y., Gan, F., Shen, G., Zhao, C. & Bryant, D. A. Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335: I. Regulation of FaRLiP gene expression. Photosynth. Res. 131, 173–186 (2017).

    Article  CAS  PubMed  Google Scholar 

  28. Holzwarth, A. R., Schatz, G., Brock, H. & Bittersmann, E. Picosecond transient absorption and fluorescence study of cyanobacterial photosystem I particles. Biophys. J. 64, 1813–1826 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gobets, B. et al. Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophys. J. 81, 407–424 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tian, L., Farooq, S. & Van Amerongen, H. Probing the picosecond kinetics of the photosystem II core complex in vivo. Phys. Chem. Chem. Phys. 15, 3146–3154 (2013).

    Article  CAS  PubMed  Google Scholar 

  31. Vassiliev, S., Lee, C. I., Brudvig, G. W. & Bruce, D. Structure-based kinetic modeling of excited-state transfer and trapping in histidine-tagged photosystem II core complexes from Synechocystis. Biochemistry 41, 12236–12243 (2002).

    Article  CAS  PubMed  Google Scholar 

  32. Miloslavina, Y. et al. Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry 45, 2436–2442 (2006).

    Article  CAS  PubMed  Google Scholar 

  33. Szczepaniak, M. et al. Charge separation, stabilization, and protein relaxation in photosystem II core particles with closed reaction center. Biophys. J. 96, 621–631 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Niedzwiedzki, D. M., Liu, H., Chen, M. & Blankenship, R. E. Excited state properties of chlorophyll f in organic solvents at ambient and cryogenic temperatures. Photosynth. Res. 121, 25–34 (2014).

    Article  CAS  PubMed  Google Scholar 

  35. Krumova, S. B. et al. Monitoring photosynthesis in individual cells of Synechocystis sp. PCC 6803 on a picosecond timescale. Biophys. J. 99, 2006–2015 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Chukhutsina, V., Bersanini, L., Aro, E. M. & Van Amerongen, H. Cyanobacterial flv4-2 operon-encoded proteins optimize light harvesting and charge separation in photosystem II. Mol. Plant 8, 747–761 (2015).

    Article  CAS  PubMed  Google Scholar 

  37. Karapetyan, N. V., Holzwarth, A. R. & Rögner, M. The photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and physiological significance. FEBS Lett. 460, 395–400 (1999).

    Article  CAS  PubMed  Google Scholar 

  38. Gobets, B. & van Grondelle, R. Energy transfer and site of energy trapping in photosystem I. Biochim. Biophys. Acta 1507, 80–99 (2001).

    Article  CAS  PubMed  Google Scholar 

  39. Broess, K., Trinkunas, G., van Hoek, A., Croce, R. & van Amerongen, H. Determination of the excitation migration time in photosystem II. Biochim. Biophys. Acta 1777, 404–409 (2008).

    Article  CAS  PubMed  Google Scholar 

  40. Miyashita, H. et al. Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol. 38, 274–281 (1997).

    Article  CAS  Google Scholar 

  41. Tomo, T. et al. Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc. Natl Acad. Sci. USA 104, 7283–7288 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Itoh, S. et al. Function of chlorophyll d in reaction centers of photosystems I and II of the oxygenic photosynthesis of Acaryochloris marina. Biochemistry 46, 12473–12481 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Cser, K., Deák, Z., Telfer, A., Barber, J. & Vass, I. Energetics of photosystem II charge recombination in Acaryochloris marina studied by thermoluminescence and flash-induced chlorophyll fluorescence measurements. Photosynth. Res. 98, 131–140 (2008).

    Article  CAS  PubMed  Google Scholar 

  44. Schatz, G., Brock, H. & Holzwarth, A. R. Kinetic and energetic model for the primary processes in photosystem II. Biophys. J. 54, 397–405 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Van Grondelle, R., Dekker, J. P., Gillbro, T. & Sundström, V. Energy transfer and trapping in photosynthesis. Biochim. Biophys. Acta 1187, 1–65 (1994).

    Article  CAS  Google Scholar 

  46. Gan, F. & Bryant, D. A. Adaptive and acclimative responses of cyanobacteria to far-red light. Environ. Microbiol. 17, 3450–3465 (2015).

    Article  CAS  PubMed  Google Scholar 

  47. Rippka, R., Deruelles, J. & Waterbury, J. B. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 1–61 (1979).

    Google Scholar 

  48. Zhang, P., Allahverdiyeva, Y., Eisenhut, M. & Aro, E. M. Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by FIv2 and FIv4 in Synechocystis sp. PCC 6803. PLoS ONE 4, e5331 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Zhang, P. et al. Operon flv4–flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24, 1952–1971 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Van Oort, B. et al. Picosecond fluorescence of intact and dissolved PSI–LHCI crystals. Biophys. J. 95, 5851–5861 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. 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  PubMed  CAS  Google Scholar 

  52. Kuhl, H. et al. 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, 20652–20659 (2000).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. Schaefers (Vrije Universiteit Amsterdam) for helping with cell growth and pigment content determination and M. Tros for insightful discussions. This project was supported by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 675006 and by the Netherlands Organization for Scientific Research (NWO) via a Top grant to R.C., and by the EMBO long-term fellowship (EMBO ALTF 292-2017) to L.B.

Author information

Authors and Affiliations

  1. Department of Physics and Astronomy and Institute for Lasers, Life and Biophotonics, Faculty of Sciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands

    Vincenzo Mascoli, Luca Bersanini & Roberta Croce

Authors
  1. Vincenzo Mascoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luca Bersanini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roberta Croce
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L.B. and R.C. conceived the project. V.M. and L.B. performed the experiments. V.M. and L.B. analysed the data. The manuscript was written by V.M. with contributions by R.C. and L.B.

Corresponding author

Correspondence to Roberta Croce.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Robert Blankenship and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–24, tables and references.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mascoli, V., Bersanini, L. & Croce, R. Far-red absorption and light-use efficiency trade-offs in chlorophyll f photosynthesis. Nat. Plants 6, 1044–1053 (2020). https://doi.org/10.1038/s41477-020-0718-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-020-0718-z

This article is cited by

Search

Advanced 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