Active transport of Ca2+ by an artificial photosynthetic membrane

Abstract

Transport of calcium ions across membranes and against a thermodynamic gradient is essential to many biological processes, including muscle contraction, the citric acid cycle, glycogen metabolism, release of neurotransmitters, vision, biological signal transduction and immune response. Synthetic systems that transport metal ions across lipid or liquid membranes are well known1,2,3,4,5,6, and in some cases light has been used to facilitate transport7. Typically, a carrier molecule located in a symmetric membrane binds the ion from aqueous solution on one side and releases it on the other. The thermodynamic driving force is provided by an ion concentration difference between the two aqueous solutions, coupling to such a gradient in an auxiliary species, or photomodulation of the carrier by an asymmetric photon flux7. Here we report a different approach, in which active transport is driven not by concentration gradients, but by light-induced electron transfer in a photoactive molecule that is asymmetrically disposed across a lipid bilayer. The system comprises a synthetic, light-driven transmembrane Ca2+ pump based on a redox-sensitive, lipophilic Ca2+-binding shuttle molecule whose function is powered by an intramembrane artificial photosynthetic reaction centre. The resulting structure transports calcium ions across the bilayer of a liposome to develop both a calcium ion concentration gradient and a membrane potential, expanding Mitchell's concept of a redox loop mechanism for protons8 to include divalent cations. Although the quantum yield is relatively low (1 per cent), the Ca2+ electrochemical potential developed is significant.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Schematic representation of a liposome-based, light-powered transmembrane Ca2+ pump.
Figure 2: Transmembrane Ca2+ transport.
Figure 3: Light-induced formation of a membrane potential.

References

  1. 1

    Bartsch, R. A. & Way, J. D. Chemical Separations with Liquid Membranes (American Chemical Society, Washington, 1996)

    Google Scholar 

  2. 2

    Hirose, T., Baldwin, B. W. & Wang, Z. H. Kemp's triacid derivatives as versatile divalent metal ion transport agents and their utilization as chromoionophores. Recent Res. Dev. Pure Appl. Chem. 2, 527–546 (1998)

    CAS  Google Scholar 

  3. 3

    de Gyves, J. & de Miguel, E. R. Metal ion separations by supported liquid membranes. Indust. Eng. Chem. Res. 38, 2182–2202 (1999)

    CAS  Article  Google Scholar 

  4. 4

    Lamrabte, A., Janot, J. M., Bienvenue, E., Momenteau, M. & Seta, P. Photoinitiated vectorial transmembrane electron transfer in bilayers sensitized by a face to face triporphyrin acting as a molecular electronic device. Amplification due to ionic coupling. Photochem. Photobiol. 54, 123–126 (1991)

    CAS  Article  Google Scholar 

  5. 5

    Zhao, Z.-G. & Tollin, G. Chlorophyll photosensitized electron tranfser reactions in lipid bilayer vesicles: Generation of proton gradients across the bilayer coupled to quinone reduction and hydroquinone oxidation. Photochem. Photobiol. 55, 611–619 (1992)

    CAS  Article  Google Scholar 

  6. 6

    Dadfarnia, S., Shamsipur, M., Tamaddon, F. & Sharghi, H. Extraction and membrane transport of metal ions by some synthetic 9,10-anthraquinone and 9-anthrone derivatives. A selective system for calcium transport. J. Membr. Sci. 78, 115–122 (1993)

    CAS  Article  Google Scholar 

  7. 7

    Longin, T. L., Goyette, M. L. & Koval, C. A. Liquid membranes with light switches. Chem. Innov. 31, 23–30 (2001)

    CAS  Google Scholar 

  8. 8

    Mitchell, P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. Camb. Phil. Soc. 41, 445–502 (1966)

    CAS  Article  Google Scholar 

  9. 9

    Sullivan, B. W. & Faulkner, D. J. New Perspectives in Sponge Biology (ed. Rützler, K.) 45–50 (Smithsonian Institution Press, Washington, 1990)

    Google Scholar 

  10. 10

    Steinberg-Yfrach, G. et al. Artificial photosynthetic reaction centers in liposomes: Photochemical generation of transmembrane proton potential. Nature 385, 239–241 (1997)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Steinberg-Yfrach, G. et al. Light-driven production of ATP catalysed by F0F1-ATP synthase in an artificial photosynthetic membrane. Nature 392, 479–482 (1998)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Minta, A., Kao, J. P. Y. & Tsien, R. Y. Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J. Biol. Chem. 264, 8171–8178 (1989)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the US Department of Energy and the Harrington Arthritis Research Center.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Devens Gust.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bennett, I., Farfano, H., Bogani, F. et al. Active transport of Ca2+ by an artificial photosynthetic membrane. Nature 420, 398–401 (2002). https://doi.org/10.1038/nature01209

Download citation

Further reading

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

Sign up for the Nature Briefing newsletter for a daily update on COVID-19 science.
Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing