WILLIAMARNOLD
788
An Electron-Hole Picture of Photosynthesis’”sb
by William Arnold Bwlogy Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee
(Received October 5 , 1964)
The present picture of the light reaction in photosynthesis consists of two (0.8-v.) electron transfers separated by an electron-transport chain. The arguments for this scheme make use of the information from spectral changes shown by plants upon illumination and by the oxidation or reduction of dyes added to illuminated chloroplasts. S o use is made of the information from the fluorescence or the delayed light emitted by the plants. If we emphasize the information given by the two light emissions and neglect the chemical information, we are led to a picture of the light reaction in photosynthesis in which free electrons and holes play a n essential part.
Introduction Photosynthesis is the process by which green plants reduce C02 to carbohydrates and oxidize water to 02. This act stores in the carbohydrate about 5.1 e.v. of free energy/atom of carbon. The energy comes from sunlight absorbed by chlorophyll. Since the process can go in red light, we know that the energy per quantum is about 1.8 e.v. Respiration of plants and animals and combustion of coal and oil reverse the process. The yearly turnover2 of some 2 X 1011 tons of carbon in this cycle furnishes the energy for living things. Research with radioactive carbon, largely by Calvin and associate^,^ has shown that COZ does not take part in any photochemical reaction. Carbon reduction is a series of enzyme reactions that can take place in the dark. This Calvin cycle is driven by electrons at -0.4 v. and by ATP. The problem in photosynthesis is to show how chlorophyll and light can lift a n electron from the level of water (+0.8 v.) to that of the reductant (-0.4 v.) and make ATP. The most popular scheme at present is shown in Figure 1. There are two light reactions, each of which lifts an electron 0.8 v. Between them there is a 0.4-v. electron-transport system making ATP. A number of the papers in the Warrenton Symposium‘ gives the evidence on which the idea stands. Essentially what is done is to emphasize the absorption changes seen in green plants on illumination and to make use of the information as to the oxidation and reduction of dyes by illuminated chloroplasts. KO use is made of the information furnished by the fluorescent and delayed light emitted by the plant. The Journal of Physical Chemistry
Emphasizing the information on light emission and neglecting that on the light absorption and dye reduction, we come to a picture of photosynthesis in which electrons and holes play an important, part. The idea that photosynthesis is an electronic process has been suggested several Experiments Considered We use four kinds of experiments. I . Quantum Yield. There is now general agreement that green plants absorb 8 quanta of light to reduce one C02. The measurement of this number has been the subject of a long and bitter controversy that we will not explore. If 8 quanta (1.8 e.v.) are used to store 5.1 e.v., then the efficiency of the whole process of photosynthesis is 35%. This high efficiency tells us that the point a t which reducing power is generated (1) (a) Research sponsored by the U. 5. Atomic Energy Commission under contract with the Union Carbide Corp.; (b) presented to the International Conference on Photosensitization in Solids, Chicago, Ill., June 22-24, 1964. (2) E. I. Rabinowitch, “Photosynthesis and Related Processes,” Interscience Publishers, Inc., New York, N. Y., 1945. (3) J. A. Bassham and M. Calvin, “Path of Carbon in Photosynthesis,” Prentice-Hall, Inc., Englewood Cliffs, N. J., 1952. (4) “Photosynthetic Mechanisms of Green Plants,” National Academy of Sciences, National Research Council, Washington, D. C., 1963. ( 5 ) A. Szent-Gyorgyi, Science, 93, 609 (1941). (6) E. Kats, “Photosynthesis in Plants,” Iowa State College Press, Ames, Iowa, 1949, Chapter XV, p. 291. (7) J. A. Bassham and M. Calvin, USAEC Unclassified Report UCRG2853, 1955. (8) W. Arnold and E. 9. Meek, Arch. Bwchem. B w p h y s . , 6 0 , 809 (1956).
AN ELECTRON-HOLE PICTURE OF PHOTOSYNTHESIS
---
-04-
------)
789
ELECTRONS TO THE C A L V I N CYCLE
0
-3
0-
-1
9
z
& +04a
C0.S-
Figure 1. Present scheme for the electron transfer in photosynthesis.
is separated from the point at which oxidizing power is generated. We will refer to these points as A and B. The separation can be by distance or by a membrane, but, in either case, there must be an electronic conductor between points X and B. I I . Photosynthetic C'nit. Experinientsg niade long ago with Robert Enierson showed that in green plant photosynthesis 2000-2500 chlorophyll molecules are involved in the reduction of one COZ molecule. Since this reduction needs four electrons, we see that 500600 chlorophyll iliolecules cooperate in the transfer of an electron front water to the Calvin cycle. I I I . Fluorescence. Although it has been known since the time of Stokes that green plants fluoresce, it is only recently that we have had good measurements. Latimer, et al.," showed that fluorescence amounts to 2 4 % of the light absorbed in the region where the rate of photosynthesis is a linear function of light intensity. We will use 2.5ycin our argument. A number of people have studied fluorescence as a function of the exciting light intensity. Figure 2 is a schematic representation of the results of Franck and collaborators. At low light intensities the rate of photosynthesis is proportional to the intensity of the exciting light. At higher light intmsities, the rate becomes independent of the exciting light, and we say that it is saturated. From the curve it can be seen that, as the rate of photosynthesis beconies saturated, the slope of the curve for fluorescence doubles. I V . Delayed Light. I n addition, we know that green plants enlit a delayed light. This emission, which has the same spectral composition as fluorescence, has been studied from 5 X 10-5 to 6 X lo3sec. Figure 3 shows the intensity of the delayed light as a function of time in the dark. The data are for Chlorella at three different temperatures. The points for - 165' were taken from a paper by Tollin, et aZ.'* As can be seen, the decay is not exponential; it is very roughly proportional to 1 he reciprocal of the time.
Figure 2 . Photosynthesis and fluorescence as a function of exciting light intensity.
I
, 10-~
,
,
to-2' ' 0 1
I IO TIME (sec)
100
Figure 3. Decay of delayed light a t three temperatures for Chlorella.
I
10-
\
.. 8
Figure 4. Decay of delayed light a t short times. line is an exponential with a time constant of 1 . 7
The solid 10-9 sec
x
The long times involved, as well as the small temperature effect, argue that the delayed light conies from the (9) R . Emerson and
W.Arnold, J . Gen. P h y s i o l . , 16, 191 (1932). (10) P. Latimer, T. T. Bannister, and E. Rabinowitch. Science, 124, 585 (1956). (11) J. Franck, "Photosynthesis in Plants,'' Iowa State College Press, Ames, Iowa, 1949, Chapter X V I , p. 293. (12) G. Tollin, E. Fujimori, and 11. Calvin. Proc. \-atZ. Acad. Sei.
L' S . , 44, 1035 (1958).
Volume 69, S u m b e r 3
March 1965
WILLIAMARXOLD
790
PHOTOSYNTHETIC UNIT 500 -600 CHLOROPHYLLS
CYCLE
Figure 5. The electron-hole scheme for the electron transfer in photosynthesis.
recombination of electrons and holes as was suggested by Tollin. Figure 4, taken from the Warrenton Symposium (Arnold and D a ~ i d s o n ) is , ~ a decay curve for the delayed light from Chlorella. The delayed light signals are plotted as a fraction of the steady-state fluorescence (taken to be unity). The solid curve is an exponential sec., which is the having a time constant of 1.7 X lifetime of fluorescence from Chlorella given by Tomita, et aZ.13 It must be remembered that, in determining the lifetime, the assumption was made that the decay was exponential. Extrapolation of the decay to shorter times suggests that a large fraction of the in vivo fluorescence of green plants is delayed light. I n the electron-hole picture of photosynthesis that we now present we make that assumption.
The Electron-Hole Picture I n Figure 5, the rectangle represents a photosynthetic unit made from 500-600 chlorophyll molecules. A and B are the two reaction centers. The absorption of a light quantum by any one of the 500 chlorophyll molecules f o r m an exciton that can run over the whole unit. An exciton that hits the reaction center A is broken up to form a free hole in the chlorophyll and an electron bound to A. This electron, a t -0.4 v., can go to the Calvin cycle or to an electron-transport chain that makes ATP. A second exciton cannot react with A until the electron has moved out of A. Similarly, an exciton can react a t B to form a bound hole and a free electron in the chlorophyll. Again, a second exciton cannot react with B until the hole has been used in the oxidation of water. The free electron and hole can move about in the chlorophyll until they recombine and form an exciton. This movement constitutes the electronic conductor that we need between A and B and determines the nonexponential decay of the delayed light. The Journal of Physical Chemistry
An approximate estimation of the lifetimes involved can be made from the fluorescence experiments. At high light intensities an exciton mill generally find the two reaction centers filled. If the quantuin yield of fluorescence is to be 5% a t high intensities, then the lifetime of the exciton must be one-twentieth sec.I4 that is believed to be as large as the 1.5 X the natural lifetinie of chlorophyll. Thus, the lifetime of an exciton, when the traps are filled, is 7 X sec. At low intensities of exciting light, the traps A and B will be empty. Since we know that the process of photosynthesis is very efficient a t low intensities, the lifetime of the exciton iriust be about one-tenth as large as, say, 7 X 10-l1 sec. This agrees with the calculations of Bay and Pearlstein'j for the time for an exciton to react with the reaction center in a photosynthetic unit. The lifetimes and yields are shown in Table I.
Table I : Lifetime and Fate of Excitation 70of excitations resulting
-
--in-
Natural lifetime of chlorophyll14 Exciton when traps are filled (high intensity) Exciton when traps are empty (low intensity) Exciton when traps are empty (celcd.l5)
Electron trans-
Lifetime, 8ec.
Fluorescence
Heat
fer
1 . 5 X lo-*
100.0
0
0
7
x
10-10
7 x 10-11 3 . 6 X lo-" 8 . 6 x lo-"
5 , O 95.0
0
0.5
9 . 5 90.0
... ...
... , , .
.. ...
,
The main points in favor of the electron-hole model are now given. (1) At low light intensities, where we know that the process of photosynthesis is very efficient, the model gives a probability of 0.9 that an absorbed quantum will be used. (2) At high light intensities, above the saturation of photosynthesis, the model gives a mechanism for the plant to dispose of the excess energy absorbed. When both traps are filled, the probability that an exciton will be converted to heat is 0.95. (3) At low light intensities the experimentally observed fluorescence yield consists of 0.5% true fluorescence and somewhat less than 2.5% delayed light. This agrees with the measurements of Latimer, et ~ 1 . (4) At high light intensities the differential yield of (13) G. Tomita and E. Rabinowitch, B w p h y s . J . , 2, 483 (1962). (14) S. Brody and E. Rabinowitch, Science, 125, 555 (1957). (15) Z. Bay and R. Pearlstein, Proc. Natl. Acad. Sci. C'. S., 5 0 , 1071 (1963).
~ 0
EXCHANGE OF SUBSTITUENTS ON NITROGEN IN MOLTEN SALTSAND AMINES
fluorescence will be 5%. This agrees with the findings of Franck." ( 5 ) The model provides the electronic conductor that is needed to prevent back-reactions between the reducing and the oxidizing power. (6) The model provides a mechanism for the production of delayed light.
791
Two problems in solid state physics must be solved before the electron-hole picture of photosynthesis has to be taken seriously. (1) Can an exciton break up to give a bound electron and a free hole? (2) How do free electrons and holes move in an aggregate of a few hundred pigment molecules?
Exchange of Substituents on Nitrogen in Molten Ammonium Salts and Amines
by Heinz K. Hofmeister and John R. Van Wazer Monsanto Company, Central Research Department, St. Louis, Missouri
(Received February 19, 1964)
At 200-300° in sealed tubes, methyl groups and hydrogen atoms exchange places on the nitrogen atoms of ammonium ions in melts of tetramethylammonium chloride with ammonium chloride. Likewise, the three pure mixed methylammonium cations-CH3?;H3+, (CH&SH2+, and (CHS)&H+-undergo such rearrangements. I n all cases, there is an equilibrium between the various ammonium ions which is not much different from that expected for random sorting of the hydrogens and methyl groups. The kinetics of the thermal equilibration of methyl-, dimethyl-, and trimethylammonium ions a t 300" are presented. Mixtures of aniline and dimethylaniline in the same temperature range p , ! ~ , exchange hydrogens and methyl groups to give a near-random equilibrium in the presence of appreciable amounts of HCl. Shifting of phenyl groups between nitrogen atoms is immeasurably slow under the conditions studied.
As pointed out by Skinner,l the enthalpy of redistribution reactions gives a direct measure of the departure of bond-energy-term values from constancy. This information may alSo be obtained indirectly2 by measuring the deviations from statistically random sorting in the scrambling of substituents in such reactions. As part of a broad quantitative study of new families of inorganic compounds, ranging from small molecules .to macromolecular species, it has been deemed desirable to establish certain generalities concerning deviations from the statistically random sorting of substituents in scrambling reactions. The information presented below represents a specific experimental example studied for this purpose, since we could find no quantitative chemical data or any thermochemical information concerning the scrambling of substituents on quadruply connected nitrogen. Simultaneously,
data were also obtained for another general treatment we are attempting which deals with the kinetics of scrambling reactions.
Experimental Details The N,N-dimethylaniline, aniline, methylamine hydrogen chloride, and ammonium chloride were reagent ~~
-
(1) H. A. Skinner, Rec. trav. chim., 73, 991 (1954). (2) The values of AH may be estimated, rather closely in many cases, by calculating (in terms of free energy) the deviations from randomness of the measured equilibrium constants of the appropriate scrambling reactions. This assumes cancellation of the partition functions for translation, rotation, and vibration. See A. G. Evans and E. Wnrhurut, Trans. Faraday SOC.,44, 1S9 (1948); J. R. Van Wazer and L. Maier, J. Am. Chem. SOC.,86,811 (1964); K. Moedritzer and J. R. Van Wazer, Inorg. Chem., 3 , 139 (1964). (3) Manuscripts concerned with (a) regularities in the deviations of scrambling reactions from randomness and (b) a theory of the variations to be found in the kinetics of such reactions are now in preparation.
Volume 69,Number 9 March 1965
