The Primary Steps of Photosynthesis

FEB 01, 1994

The two important initial steps of photosynthesis—electron transfer and energy transfer—occur with great speed and efficiency. New techniques in laser optics and genetic engineering are helping us to understand why.

DOI: 10.1063/1.881413

Graham R. Fleming

Rienk van Grondelle

Photosynthesis, the process by which plants convert solar energy into chemical energy, results in about 10 billion tons of carbon entering the biosphere annually as carbohydrate—equivalent to about eight times mankind’s energy consumption in 1990. The apparatus used by plants to perform this conversion is both complex and highly efficient. Two initial steps of photosynthesis—energy transfer and electron transfer—are essential to its efficiency: Molecules of the light‐harvesting system transfer electronic excitation energy to special chlorophyll molecules, whose role is to initiate the directional transfer of electrons across a biological membrane; the electron transfer, which takes place in a pigment‐protein complex called the reaction center, then creates a potential difference that drives the subsequent biochemical reactions that store the energy. (Higher plants use two different reaction centers, called photosystems I and II, while purple bacteria make do with a single reaction center. The difference is that the bacteria do not generate oxygen in the photosynthetic process.) Both the elementary energy transfer and the primary electron transfer are ultrafast (occurring between ${10−}^{13}$ and ${10−}^{12}$ seconds), leading to the trapping of excitation energy at the reaction center (on a 100‐picosecond timescale) and subsequent electron transfer in about 3 picoseconds with almost 100% quantum yield.

This article is only available in PDF format

References

1. J. Deisenhofer, H. Michel, EMBO Journal 8, 2149 (1989).
2. E. C. Kellogg, S. Kolaczkowski, M. R. Waseliewski, D. Tiede, Photosynth. Res. 72, 47 (1989).
3. T. Middendorf, L. Mazzola, D. Gaul, C. Schenck, S. Boxer, J. Phys. Chem. 95, 10142 (1991). https://doi.org/JPCHAX
N. Raja, S. Reddy, S. V. Kolaczkowski, G. J. Small, J. Phys. Chem. 97, 6934 (1993).https://doi.org/JPCHAX
4. A. P. Schreve, N. J. Cherepy, S. Franzen, S. G. Boxer, R. A. Mathies, Proc. Natl. Acad. Sci. U.S.A. 88, 11207 (1991).https://doi.org/PNASA6
5. Y. Won, R. A. Friesner, J. Phys. Chem. 92, 2208 (1988).https://doi.org/JPCHAX
6. R. A. Marcus, R. Almeida, J. Phys. Chem. 91, 2973; 2978 (1990).
Y. Hu, S. Mukamel, J. Chem. Phys. 94, 6973 (1989). https://doi.org/JCPSA6
J. S. Joseph, W. A. Bialek, J. Phys. Chem. 97, 3245 (1993).https://doi.org/JPCHAX
7. M. Bixon, J. Jortner, M. E. Michel‐Byerle, Biochim. Biophys. Acta 1056, 301 (1991).https://doi.org/BBACAQ
8. K. Schulten, M. Tesch, Chem. Phys. 158, 421 (1991). https://doi.org/CMPHC2
A. Warshel, W. W. Parson, Annu. Rev. Phys. Chem. 42, 279 (1991).
N. Marchi, J. N. Gehlen, D. Chandler, M. Newton, J. Amer. Chem. Soc. 115, 4178 (1993).https://doi.org/JACSAT
9. W. Holzapfel, U. Finkele, W. Kaiser, D. Oesterheldt, H. Scheer, H. U. Stilz, W. Zinth, Chem. Phys. Lett. 160, 1 (1989); https://doi.org/CHPLBC
W. Holzapfel, U. Finkele, W. Kaiser, D. Oesterheldt, H. Scheer, H. U. Stilz, W. Zinth, Proc. Natl. Acad. Sci. 87, 5168 (1990).
10. C. Kirmaier, D. Holten, Biochem. 30, 609 (1991).
11. J. Breton, J.‐L. Martin, J. C. Lambry, S. J. Robles, D. C. Youvan, in Reaction Centers of Photosynthetic Bacteria, M. E. Michel‐Byerle, ed., Springer‐Verlag, New York (1990), p. 293.
12. C. K. Chan, T. J. DiMagno, L. X. Q. Chen, J. R. Norris, G. R. Fleming, Proc. Natl. Acad. Sci. U.S.A. 88, 11202 (1991).https://doi.org/PNASA6
Y. Jia, T. J. DiMagno, C. K. Chan, Z. Wang, M. Du, D. K. Hanson, M. Schiffer, J. R. Norris, G. R. Fleming, M. S. Popov, J. Phys. Chem. 97, 13180 (1993).
13. M. H. Vos, F. Rappaport, J.‐C. Lambry, J. Breton, J.‐L. Martin, Nature 363, 320 (1993).https://doi.org/NATUAS
14. S. S. Skourtis, A. J. da Silva, W. Bialek, J. N. Onuchic, J. Phys. Chem. 96, 8034 (1992).https://doi.org/JPCHAX
J. M. Jean, R. A. Friesner, G. R. Fleming, J. Chem. Phys. 96, 5827 (1992).https://doi.org/JCPSA6
15. S. G. Johnson, G. J. Small, J. Phys. Chem. 95, 471 (1991).https://doi.org/JPCHAX
16. A. Y. Borisov, A. Freiberg, V. Godik, K. K. Rebane, K. E. Timpmann, Biochim. Biophys. Acta 807, 221 (1985).https://doi.org/BBACAQ
17. V. Sundström, R. van Grondelle, H. Bergström, E. Akesson, T. Gillbro, Biochim. Biophys. Acta 851, 431 (1986).https://doi.org/BBACAQ
18. T. G. Owens, S. P. Webb, L. Mets, R. S. Alberte, G. R. Fleming, Proc. Natl. Acad. Sci. U.S.A. 84, 1532 (1987). https://doi.org/PNASA6
G. H. Schatz, H. Brock, A. R. Holzwarth, Proc. Natl. Acad. Sci. USA 84, 8414 (1987).
19. J. G. C. Bakker, R. van Grondelle, W. T. F. den Hollander, Biochim. Biophys. Acta 725, 508 (1983). https://doi.org/BBACAQ
L. Valkunas, S. Kudzmauskas, V. Liuolia, Sov. Phys. Coll. 26, 1 (1986).https://doi.org/SPCODK
20. R. E. Fenna, B. W. Matthews, Nature 258, 573 (1975).https://doi.org/NATUAS
21. F. van Mourik, R. R. Verwijst, J. M. Mulder, R. van Grondelle, J. Lumin. 53, 499 (1992).
22. N. Krauss, W. Hinrichs, I. Witt, P. Fromme, W. Pritzkow, Z. Dauter, C. Betzel, K. S. Wilson, H. T. Witt, W. Saenger, Nature 361, 326 (1993).
23. W. Köhlbrandt, D. N. Wang, Nature 350, 326 (1991).https://doi.org/NATUAS
24. M. Du, X. Xie, Y. Jia, L. Mets, G. R. Fleming, Chem. Phvs. Lett. 201, 535 (1993).

More about the authors

Graham R. Fleming, University of Chicago.

Rienk van Grondelle, Free University of Amsterdam, Netherlands.