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Photochemistry und Photobiology Vol. 53, No. 4. pp. 545-548, 1991 Ml31-8655/91 $03.00+0.

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THE MAXIMUM EFFICIENCY OF PHOTOSYNTHESIS*


JAMES R. BOLTON? and DAVID0. HALL^
Photochemistry Unit, Department of Chemistry, The University of Western Ontario, London,
Ontario, Canada N6A 5B7 and Division of Biosphere Sciences, Kings College London,
Campden Hill Road, London W8 7AH, UK
(Received 10 October 1989; received in revised form 22 October 1990; accepted 12 November 1990)

Abstract-Within the ideal assumptions: (1) two Photosystems for photosynthetic fixation of COz, (2)
all solar photons with A 700 nm are absorbed, (3) the photon requirement is 8 for each CO, molecule
fixed and O2 molecule evolved and (4) the principal stable product of photosynthesis is d-glucose. the
theoretical maximum efficiency of conversion of light to stored chemical energy in green-plant type
(oxygen-evolving)photosynthesis in bright sunlight is calculated to be 13.0%. Thermodynamic argu-
ments are presented which indicate that a photosynthetic system with one Photosystem would be
highly unlikely to be able to drive each electron from water to evolve 0, and reduce CO,. The
practical maximum efficiency of photosynthesis under optimum conditions is estimated to be 8-9%.

INTRODUCTION efficiency calculations on the total incident


Photosynthesis is the process whereby green plants, irradiance. For the solar distribution we have util-
algae and certain bacteria utilize a portion of the ized (vide infra), 43% of the irradiance lies in the
photon energy from the sun to drive endergonic PAR; thus efficiencies calculated on the basis of the
reactions that store chemical energy. This energy PAR will be 2.32 times higher than those calculated
conversion reaction annually results in the world- using the total incident irradiance as the base.
wide storage of -3 x lo2 J of energy, so it is of In the past few years there have been some
considerable interest to know what is the theoretical reports (Pirt et al., 1980; Pirt, 1983, 1986; Osborne
maximum efficiency of photosynthesis, if all but and Geider, 1987) of practical photosynthetic
unavoidable losses are reduced to zero. efficiencies, based on total incident solar irradiance,
In green plants, algae and cyanobacteria (we shall which exceed 17% for algal systems. We believe
not consider photosynthetic bacteria in our analysis, these claimed efficiencies to be greater than the
maximum possible for photosynthesis. There has
since they do not use water as a source of electrons
been some previous discussion of photosynthesis
or protons) the overall photosynthesis reaction is
efficiencies (Emerson, 1958; Duysens, 1959; Ross
light 1
and Calvin, 1967; Kok, 1969; Schneider, 1973;
C02(g) + H20([) + 6 C6Hl206(s) + 02(g) (1) Walker and Herold, 1976; Bassham, 1977; Bolton,
where the partial pressures of C 0 2 and 0 2 are 1978a,b; Bolton, 1979); however, none of these
0.000350 and 0.21 atm, respectively, in the normal clearly stated the complete rationale for the limiting
atmosphere. efficiency of photosynthesis. It is important to estab-
Photosynthetic efficiencies have often been calcu- lish this upper limit for both theoretical and practical
lated on the basis of the incident irradiance in the reasons (especially where it is proposed to use
photosynthetically active region (PARS: usually photosynthesis as an energy conversion and storage
taken to be 400-700 nm). This is not a proper basis process or to remove C 0 2 from the atmosphere).
for an efficiency calculation, since the radiation out-
side the PAR is not accounted for and also the THE IDEAL CONDITIONS FOR PHOTOSYNTHESIS
fraction of the incident irradiance lying in the PAR
varies markedly with different light sources. In com- Since we wish to calculate an ideal maximum
mon with almost all other areas of solar energy efficiency for photosynthesis, it is important to state
utilization (e.g. photovoltaic cells), we base our and justify a set of conditions and assumptions that
define the ideal conditions for photosynthesis.
*ContributionNo. 434, Photochemistry Unit, Department
of Chemistry, The University of Western Ontario. Photosynthesis operates with two photosystems
tTo whom correspondence should be addressed.
$Abbreviations: ATP, adenosine triphosphate; Chl, The proposal by Hill and Bendall (1960) that
chlorophyll; c,, incident solar irradiance; is. integrated green-plant photosynthesis proceeds via two photo-
photon flux; .Io,, molar oxygen flux; N,,, Avogadros systems is now almost universally accepted and but-
number; PAR, photosynthetically active region; X i , tressed by many biophysical, biochemical and
mole fraction of component i; q, efficiency; qa,fraction
of light absorbed; 4, quantum yield; A,, threshold wave- physiological observations, which include isolation
length; h, chemical potential of component i. of biochemically distinguishable reaction-center

545
546 and DAVID
JAMESR. BOLTON 0. HALL

complexes associated with each of the two photo- energy of Chl* is internal energy and not Gibbs
systems, the Emerson "red-drop" effect, and wave- energy. The chemical potential of Chl* (or the avail-
length dependent oxidation and reduction of the able energy for chemical energy storage) is obtained
cytochrome b-f complex (Emerson, 1958; Duysens, from the expression
1962; Barber, 1987; Andreasson and Vanngard, pchi* = u
g -k (kT/e)en (XChI.) (2)
1988). Furthermore Bolton (1978a, 1979) has pre-
sented arguments which indicate that if photo- = 1.80 + 0.0259 en (2.4 x = 1.35 eV
synthesis were to operate with only one photo- [Eq. (2) is the same as Eq. (6) of Parson (1978);
system, it would have to function almost at the see also Ross et al. (1976)].
thermodynamic limit. Since the reported efficiences Reaction (l), under the photosynthesis operating
of 17-18% are not compatible with the assumption conditions, requires a Gibbs energy output of at least
of two photosystems in photosynthesis, we expand 1.29 eV. Thus if photosynthesis were to operate with
on Bolton's arguments here. one photosystem, it would have to do so with very
Under the conditions in which reaction (1) occurs, small losses other than the unavoidable theoretical
the following are the values of the important ther- losses. This is equivalent to attempting to design an
modynamic functions for reaction (1) (Bolton, almost frictionless Carnot heat engine. The result of
1978a): this thermodynamic analysis is that we can reject the
AH = 467 kJ mol-' hypothesis of one photosystem, which, although not
AG = 496 kJ mol-' impossible, is highly implausible.
E = 1.29eV In our subsequent analysis we shall assume a
two-photosystem mechanism, a scheme which was
As Parson (1978) and Bolton (1978a, 1979) have evolved more than 3 billion years ago by cyanobac-
pointed out, it is very important to use thermody- teria and has remained virtually unchanged since
namic functions calculated for the actual conditions then (Rao et al., 1985).
under which photosynthetic C 0 2 fixation is occur-
ring. However, for comparison, we also give the
values of these functions calculated under standard All solar photons incident on the system with wave-
conditions (gases at 1 atm pressure) lengths A less than the threshold wavelength
A, = 700 nm are absorbed
AHv = 467 kJ mol-'
This is clearly an overstatement, as in a leaf some
AGO = 479 kJ mol-'
incident photons are reflected and others trans-
E" = 1.24eV
mitted; however, this assumption is necessary for
The difference between AG and AGO arises from purposes of calculating the maximum efficiency.
the work necessary to compress the gases to the The characteristic wavelengths for Photosystems I
standard state. and I1 are 700 and 680 nm, respectively. However,
Light absorbed by a chloroplast eventually in broadband sunlight photons up to 700 nm are
appears as excited-state energy (I, of reaction center utilized effectively, so we shall use 700 nm as the
chlorophyll entities. As there are two photosystems, threshold wavelength A,.
one operating at 690 nm (Photosystem 11) and the We use the analysis procedure of Bolton et al.
other operating at 700 nm (Photosystem I), four (1985) and the standard global Air Mass 1.5 sunlight
photons are observed by each photosystem for every spectral irradiance distribution Ei (W m-2 nm-I)
oxygen molecule evolved. Thus for every C 0 2 mole- tabulated by Hulstrom et al. (1985) vs wavelength
cule fixed and O2 evolved, there are four photons (A) in approx. 10 nm intervals. We require the inte-
absorbed at 680 nm and four at 700 nm. The aver- grated photon flux j, (photons m-* s-') up to the
age photon energy is thus 1.80 eV corresponding to long wavelength threshold A, = 700 nm
the average wavelength of 690 nm.
If we assume that the only route of decay for the
(3)
chlorophyll excited states (Chl*) is radiative decay
(fluorescence), the excited state lifetime of chloro- from which we obtain jg = 1.223 x lo2' photons
phyll a would be 19.0 ns (Connolly et al., 1982). m-2 s-I
Under these conditions and the photon flux incident
from a standard solar irradiance (vide infra), a
steady-state kinetic analysis (Archer and Bolton, The photon requirement per C 0 2 fixed and 0 2

1990) indicates that under full sunlight irradiance,


evolved is a minimum of eight
the steady-state mole fraction of Chl* (&,I*) would If we assume that two absorbed photons result in
be 1.2 x lo-". However, the fluorescence quantum the transfer of one electron from water through the
yield is known to be 0.02 or less (Clayton, 1965). two photosystems ultimately to reduce C 0 2 , the
Hence, under the operating conditions prevalent in stoichiometry of reaction (1) requires that a mini-
a chloroplast, &,I* will be 2.4 x or less. mum of eight photons is required to produce one
It is important to note that the excited state molecule of O2 and absorb one molecule of C02.
Efficiency of photosynthesis 547

However, an extra photon may be required to prod- determining the efficiencies to be expected under
uce the additional (third) AT for the complete C02 operating conditions:
fixation cycle in order to produce the phosphorylated
sugars necessary for starch and sucrose synthesis Incomplete absorption
(Halliwell, 1984; Lawler, 1987). Although the quan-
tum requirement of photosynthesis is known to vary Bjorkman and Demmig (1987) measured the frac-
somewhat with wavelength (Baleigh and Biddulph, tion q,,of light absorbed by leaves of 37 species of
1957; Evans, 1987), we assume that the quantum C3-type vascular plants. They found that q. varied
requirement for the fixation of one C 0 2 and evolution from 0.75 for a thin shade leaf of cotton to 0.90
of one O2molecule is the minimum possible value of for a thick Eucalyptus leaf. We shall assume their
8 for all absorbed wavelengths. average value of 0.84.

Less than ideal quantum yield


The principal stable product of photosynthesis is
d-glucose Baleigh and Biddulph (1957) have determined the
quantum yield 4 for C02 absorption vs wavelength
Although triosephosphate is the first product of for red kidney bean leaves (Phaseolus vulgaris L.)
COz fixation, it is immediately converted to C6 up to 680 nm. They found a maximum 4 of 0.109 at
sugars (i.e. d-glucose) after export from the chloro-
plast for sucrose synthesis in the cytoplasm or used
+
690 nm but vaned considerably with wavelength.
Emerson et al. (1958) found an average quantum
directly for storage as starch in the chloroplast itself. yield for oxygen evolution of 0.104 from 660 to
Photosynthetic organisms do contain other elements 680 nm for Chlorella pyrenoidoisa. More recently
such as N, S and P; however, the incorporation of Evans (1987) found a maximum quantum yield of
these elements into the biological system from organic 0.111 at 600 nm (and a mean value of 0.089 in white
and inorganic components in the nutrient medium light for a number of C3 plant leaves). Most studies
requires the expenditure of chemical and/or photon find a marked drop in t$ below -420 nm. This is
energy. Since reaction (1) is the only known source probably due to absorption by non-active chromo-
of energy for plant growth, other than the deliberate phores, e.g. pigments in the epidermis. We shall use
addition of energy-rich substrates such as N H 3 , we
base our efficiency calculations on reaction (1). Con-
+
a value of = 0.106 (white light) in our calculations
based on the extensive investigation by Bjorkman
sideration of more complex processes must necessarily and Demmig (1987).
yield lower efficiencies and, since our purpose is to
establish a maximum efficiency for photosynthesis,
Photorespiration
we restrict our analysis to reaction (1).
Losses of up to 50% of prefixed C 0 2 can occur
as a consequence of the C 0 2 fixing enzyme inter-
THE EFFICIENCY CALCULATION acting with O2 during the light-induced C 0 2 fixing
The maximum molar flux of O2 is obtained by process, the consequence of which is the formation
dividing the absorbed photon flux by the oxygen of gycollate and not phosphorylated sugars. Plants
quantum requirement have developed biological and morphological mech-
anisms to reduce photorespiration losses, but they
Jo, = = 2.54 x mol m-2 s- (4) are imperfect depending on environmental con-
8N.4 ditions; in fact, the process may provide protection
where N A is Avogadros number. against excessive light, especially under stress con-
The maximum photosynthetic efficiency qFtX is ditions such as high or low temperatures and water
obtained by calculating the flux of stored chemical deficiency. Actual losses due to photorespiration
energy and dividing by the incident solar irradiance may vary considerably depending on the physical
Ei (total irradiance of the global AM 1.5 sunlight) and physiological conditions.

Fluctuating light conditions


These conditions (e.g. clouds, shading, etc.) may
-
-
~ m-* s-lx496 OOO J mol-I
2 . 5 4 ~ 1 0 -mol lead to rapid changes in irradiance which may not
967 W m-2 be compensated for in the optimal distribution of
light photons between the two photosystems. Such
= 0.130 or 13.0% (5) loss factors are difficult to calculate and thus we use
clear sunlight for our efficiency estimates.
EFFICIENCIES UNDER OPERATING CONDITIONS If we take only the first two factors into account
the efficiency of photosynthesis drops to
Of course the above ideal conditions are never
achieved in a real photosynthetic organism. A num- 0.130 x (0.106/0.125) x 0.84 = 0.093
ber of other loss factors must be considered in or 9.3%
548 JAMESR. BOLTONand DAVID0. HALL

CONCLUSIONS Bolton, J. R. (1979) Solar energy conversion in photo-


synthesis-features relevant to artificial systems for the
We have shown that the maximum efficiency of photochemical conversion of solar energy. In The
Chemical Conversion and Storage of Solar Energy
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This value is calculated assuming the operation of pp. 31-50. Humana Press, Clifton, NJ.
two photosystems and that the primary stored prod- Bolton, J. R., S. J. Strickler and J . S. Connolly (1985)
uct of photosynthetic C 0 2 fixation is d-glucose. This Limiting and realizable efficiencies of the solar photo-
lysis of water. Nature (London) 316, 495-500.
ideal value also assumes that the quantum require- Clayton, R. K. (1965) Molecular Physics in Photosynthesis,
ment is eight photons per C 0 2 fixed and 02 mole- p. 169. Blaisdell, New York.
cule evolved at all wavelengths and that all photons Connolly, J. S., S. B. Samuel and A. F. Janzen (1982)
with wavelengths less than 700 nm are absorbed Fluorescence lifetimes of chlorophyll a: solvent, concen-
and utilized in driving the photosynthesis reaction. tration and oxygen dependence. Photochem. Phorobiol.
36, 565.
When these last two assumptions are modified to Duysens, L. N. M. (1959) The path of light energy in
incorporate actual measured quantum yields and photosynthesis. In The Photochemical Apparatus, its
absorption factors, the efficiency estimate drops to Structure and Function, Brookhaven Symposia in
9.3%. There are some arguments, such as the ques- Biology, Vol. 11, pp. 1CL25.
tion of an extra ATP requirement (vide supra), Duysens, L. N. M. (1962) A note on efficiency for conver-
sion of light energy. Plant Physiol. 37, 407-408.
which would indicate that a minimum of nine pho- Emerson, R. (1958) The quantum yield of photosynthesis.
tons may be required to fix C 0 2 to the level of Ann. Rev. Plant Physiol. 9, 1-24.
sucrose and starch. If this is the case the calculated Emerson, E., R. Chalmers and C. Cederstrand (1958)
efficiencies of 13.0 and 9.3% would be reduced to Some factors influencing the long-wave limit of photo-
synthesis. Proc. Nail. Acad. Sci. USA 43, 133-143.
11.6 and 8.3%, respectively. Evans, 1. R. (1987) The dependence of quantum yield on
The assumption that photosynthesis operates with wavelength and growth irradiance. Ausr. J . Physiol. 14,
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Acknowledgements-This work was supported by an ditions. Solar Cells 15, 365-391.
operating grant to JRB from the Natural Sciences and Kok, B. (1969) In Physiology of Plant Growth and Devel-
Engineering Research Council of Canada and by a opment (Edited by M. B. Wilkins), pp. 335-379.
Research Grant to DOH from the Commission of the McGraw-Hill, London.
European Communities. We also thank Drs. M. D. Lawler, D. W. (1987) Photosynfhesis:Metabolism, Control
Archer, R. K. Clayton, M. C. W. Evans, Govindjee, P. and Physiology. Wiley, New York.
Nobel, J. W. Otvos, M. Seibert, A. Trebst and D. A. Osborne, B. A. and R. J. Geider (1987) The minimum
Walker for critical readings of the manuscript. photon requirement for photosynthesis. New Phytol.
106, 631-644.
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