Donator Acceptor Map for Carotenoids, Melatonin and Vitamins
Ana Martı ´nez,*,†Miguel A. Rodrı ´guez-Girone ´s,‡Andre ´s Barbosa,‡and Miguel Costas§,|
Instituto de InVestigaciones en Materiales, UniVersidad Nacional Auto ´noma de Me ´xico, Circuito Interior, S N,
Ciudad UniVersitaria, P. O. Box 70-360, Coyoaca ´n, 04510, Mexico, Department of Functional and
EVolutionary Ecology, Estacio ´n Experimental de Zonas A´ridas, CSIC, c/General Segura 1, 04001 Almerı ´a,
Spain, and Laboratorio de Biofisicoquı ´mica, Departamento de Fisicoquı ´mica Facultad de Quı ´mica,
UniVersidad Nacional Auto ´noma de Me ´xico, Ciudad UniVersitaria, Coyoaca ´n, 04510, Mexico
ReceiVed: April 14, 2008; ReVised Manuscript ReceiVed: July 7, 2008
Bright yellow and red colors in animals and plants are assumed to be caused by carotenoids (CAR). In animals,
these pigments are deposited in scales, skin and feathers. Together with other naturally occurring and colorless
substances such as melatonin and vitamins, they are considered antioxidants due to their free-radical-scavenging
properties. However, it would be better to refer to them as “antiradicals”, an action that can take place either
donating or accepting electrons. In this work we present quantum chemical calculations for several CAR and
some colorless antioxidants, such as melatonin and vitamins A, C and E. The antiradical capacity of these
substances is determined using vertical ionization energy (I), electron affinity (A), the electrodonating power
(ω-) and the electroaccepting power (ω+). Using fluor and sodium as references, electron acceptance (Ra)
and electron donation (Rd) indexes are defined. A plot of Rdvs Raprovides a donator acceptor map (DAM)
useful to classify any substance regarding its electron donating-accepting capability. Using this DAM, a
qualitative comparison among all the studied compounds is presented. According to Rdvalues, vitamin E is
the most effective antiradical in terms of its electron donor capacity, while the most effective antiradical in
terms of its electron acceptor capacity, Ra, is astaxanthin, the reddest CAR. These results may be helpful for
understanding the role played by naturally occurring pigments, acting as radical scavengers either donating
or accepting electrons.
Bright yellow and red colors in animals are thought to be
caused by a number of carotenoids (CAR) deposited in scales,
skin and feathers.1-6It has been claimed that CAR are
responsible for much of the yellow, orange and red pigmentation
manifested in the animal kingdom, and many articles have been
written (reviewed in refs 3 and 4), affirming the idea that CAR
consist of pigments and antioxidants. For many years, the idea
has existed that the pigmentation in animals may indicate
antioxidant status, given that these substances have antioxidant
properties.7,8Animals may face a tradeoff when allocating CAR
(acquired from the diet) either for physiological or for coloration
purposes. It is assumed that higher-quality individuals (those
who acquire more carotenoids or are in better state of health)
are able to devote more of the acquired CAR to coloration,
which in turn appears to be important for sexual advertisement
and ultimately reproduction and species survival. Coloration thus
reveals individual quality and becomes the target of sexual
selection. Of course, colorless antioxidant substances, such as
vitamins and melatonin, are also present in animals and plants.
Antioxidants are important since these molecules scavenge free
radicals, thus limiting cellular damage.
Several studies exist which discuss CAR and vitamins7-35
as antioxidants. There are three mechanisms that are discussed
in the literature7-20for the reaction of free radicals with CAR,
namely, electron transfer reaction, hydrogen atom transfer from
the CAR, and radical addition to the CAR. Concerning the first
mechanism, it was reported that, in order to scavenge free
radicals, CAR can either donate or accept unpaired electrons.7-17
Antioxidant molecules become oxidized by transferring electrons
to the free radical, a reaction that prevents other molecules
undergoing oxidation reactions with this free radical. As this
reaction halts oxidation, these molecules are labeled as anti-
oxidants. On the other hand, when CAR accepts an unpaired
electron from the free radical, the free radical loses electrons
and therefore becomes oxidized and CAR molecules are
reduced. This charge transfer does not prevent the oxidation of
other molecules; it prevents the reduction of other molecules.
In the literature, these substances are often referred to as
antioxidants. However, as the relevant event in biological
systems is the trapping of free radicals, it would be more precise
to refer to these substances as “antiradicals”. Antioxidation and
antireduction represent two sides of the same coin: antiradical
activity through electron transfer. Antiradical action prevents
radical damage, either by the oxidation or by the reduction of
free radicals. Hence, antiradical substances can be classified in
terms of their oxidation and reduction potential.
In order to evaluate oxidation potential, it has been
demonstrated9that relative antioxidant efficiency is determined
by vertical ionization energy (I). Compounds that have low I
values are the most easily oxidized substances, and as a result,
* Author to whom correspondence should be addressed. On sabbatical
leave at Department of Functional and Evolutionary Ecology, Estacio ´n
Experimental de Zonas A´ridas, CSIC, Almerı ´a, Spain. E-mail: martina@
†Instituto de Investigaciones en Materiales, Universidad Nacional
Auto ´noma de Me ´xico, Circuito Interior, S N, Ciudad Universitaria.
‡Department of Functional and Evolutionary Ecology, Estacio ´n Experi-
mental de Zones A´ridas, CSIC.
§Laboratorio de Biofisicoquı ´mica, Departamento de Fisicoquı ´mica
Facultad de Quı ´mica, Universidad Nacional Auto ´noma de Me ´xico, Ciudad
|On sabbatical leave at Facultad de Ciencias, Departamento de Quı ´mica
Fı ´sica, Universidad de Granada, Granada, Spain.
J. Phys. Chem. A 2008, 112, 9037–9042
10.1021/jp803218e CCC: $40.75
2008 American Chemical Society
Published on Web 08/21/2008
they represent the most efficient antiradicals, in terms of their
electron donating capability. In order to evaluate reduction
potential, it is necessary to estimate the potential for electron
acceptance. This can be achieved by assessing vertical electron
affinity (A), which is a good indicator of the electron attraction
force. Substances with high and positive A values have a greater
capacity for accepting electrons. Compounds that have large
positive A values are the most easily reduced substances, and
thus they represent the most efficient antiradicals, expressed in
terms of their electron accepting capability. Another useful
measure of electrodonating and electroaccepting power has been
reported recently by Ga ´zquez et al.36They established a simple
charge-transfer model and analyzed the global response of a
molecule immersed in an idealized environment that may either
withdraw or donate charge. A quadratic interpolation for the
energy as a function of the number of electrons was proposed
to evaluate the response of a molecule to charge acceptance or
withdrawal in terms of the electron affinity and the ionization
potential. Within this approximation, these authors conclude that
the propensity to donate charge, or electrodonating power, may
be defined as
whereas the propensity to accept charge, or electroaccepting
power, may be defined as
In the case of electrodonating power, lower values imply a
greater capacity for donating charge. In the case of electroac-
cepting power, higher values imply a greater capacity for
accepting charge. It is important to note that I and A refer to
donating or accepting one electron, while ω-and ω+refer to
fractional charges. In this way, the electrodonating and elec-
troaccepting powers are based on a simple charge transfer model
expressed in terms of the chemical potential and the hardness.
The chemical potential measures the charge flow direction
together with the capacity to donate or accept charge, providing
for the charge donation process more emphasis to the ionization
potential than to the electron affinity. Contrary, the electroac-
cepting power gives more significance to the electron affinity
than to the ionization potential and hardness measures the
resistance to the flow of the electrons.
As it is necessary for substances to donate or accept unpaired
electrons in order to trap free radicals, it is possible to use ω-
and ω+to analyze the antiradical capacity of pigments and other
well-known antioxidant substances. In this article, we report
quantum chemical calculations for several CAR and certain
colorless antioxidants such as melatonin, vitamins A, C and E
for this purpose. The antiradical capacity of CAR, melatonin,
vitamin A, C and E is analyzed using I, A, ω-and ω+. Using
fluor and sodium as references, electron acceptance (Ra) and
electron donation (Rd) indexes are defined, producing a donator
acceptor map (DAM) useful to classify any substance regarding
its electron donating-accepting capability.
Density functional theory37-39as implemented in Gaussian
0340was used for all the calculations. Becke’s 1988 functional,
which includes the Slater exchange along with corrections
involving the gradient of the density41and Perdew and Wang’s
1991 gradient-corrected correlation functional42were employed
in the calculations for complete optimizations, without symmetry
constraints. D5DV basis sets were also employed.43-45Harmonic
frequency analyses permitted us to verify optimized minima.
Figure 1. Carotenoid pigments. Schematic representation of the molecular structure of thirteen carotenoid pigments found in the feathers of the
male house finch.4
J. Phys. Chem. A, Vol. 112, No. 38, 2008
Martı ´nez et al.
In order to compute I and A, further single-point calculations
were necessary. I is calculated as the difference between the
energy of the cation and the neutral molecule, assuming that
both of these have the ground-state nuclear configuration of the
neutral molecule. A is also calculated as vertical, and represents
the energy difference between the neutral and the anion,
calculated with the ground-state nuclear configuration of the
neutral molecule. Solvent effects were included by using the
polarizable continuum model (PCM),46,47with water and
benzene as the solvents for polar and nonpolar environments,
The methodology used in this work was validated comparing
the results with those obtained using B3LYP and 6-311G(d,p),
as well as those reported previously by Galano.9The relative
values for I and A do not depend on the functional and/or on
the basis set.
Results and Discussion
In Figures 1 and 2 we schematically present the chemical
structure of CAR, melatonin and vitamins A, C and E. CAR in
Figure 1 identified in the house finch (Carpodacus mexicanus),
a species which provides an apt model because male house
finches have carotenoid-based plumage coloration in various
parts of the body (head, underside and rump).4Coloration may
vary from pale yellow to bright red, and this trait is crucial in
the choice of mate, as females prefer to mate with males
displaying the reddest and most saturated plumage coloration.4
There are at least 13 different types of CAR (see Figure 1) found
in the feathers of house finches, some of which typically confer
a red hue and others which are yellow in color.4The pigments
are classified48as “yellow” when they present multipeaked
spectral absorbance curves with λmax< 460 nm. They are “red”
when the shape of spectral absorbance represents a smooth curve
as in λmax> 460 nm. Previously Galano9reported I values for
six of these CAR. She used a similar methodology, including
solvent effects (water and benzene). A comparison between the
results of Galano and those obtained in this work is presented
in Figure 3. It is evident that our results are consistent with
those presented in ref 9. Moreover, we performed single point
energy calculations for the optimized structures of certain CAR
and vitamins, considering solvent effects. As indicated in Figure
3, the results are largely consistent, so we may conclude that
the effect of the solvent is not important when we want to obtain
relative values for I. Also in Figure 3 we present A values,
obtained for the gas phase as well as with benzene and water.
The results are in agreement, and we can also conclude that the
effect of the solvent is not important for the relative values
Vertical Ionization Energy and Electron Affinity. Table 1
reports I and A, for CAR, vitamins and melatonin. The lowest
I value is for BC and BRYP, and the highest corresponds to
vitamin C. The low I values represent the most easily oxidized
substances and indicate the most efficient antiradicals, expressed
as their electron donating capability. Generally, I values from
Table 1 indicate that yellow CAR act as better antioxidant
molecules than red ones, while melatonin and vitamins are the
poorest antioxidant molecules. According to these results,
melatonin and vitamins are not as good antioxidants as CAR.
As shown in Table 1, A is both large and positive in the case of
all animal pigments (CAR) and is negative in the case of
melatonin and vitamins C and E. For vitamin A, the value is
positive but lower than the values are for pigments. One
important conclusion that we can derive from these results is
that naturally occurring pigments are able to accept an electron.
A is positive, which means that the anion is more stable than
the neutral molecule, i.e. they are more capable of accepting
Figure 2. Melatonin and vitamins A, C and E. Schematic representa-
tion of the molecular structure of melatonin and vitamins A, C and E.
Figure 3. I and A values (in eV) for six selected CAR. (A) To calculate
I, in a previous work,9full geometry optimizations were done using
B3LYP/6-31G(d,p). Polar (water (wt)) and nonpolar (benzene (bz))
solvent effects were included by using the polarizable continuum model.
In this work, full geometry optimizations using BPW91/D95V basis
set were carried out. We also considered solvent effects for the same
six CAR. Our results for the gas phase and those using benzene and
water are largely consistent. The relative order is the same using various
solvents and in the gas phase. (B) A values (in eV) for selected CAR,
obtained in the gas phase, and using water (wt) and benzene (bz).
Results in the gas phase are consistent with those using benzene and
DAM for Carotenoids, Melatonin and Vitamins
J. Phys. Chem. A, Vol. 112, No. 38, 2008 9039
electrons and thus they represent the most efficient antiradicals
(expressed as their electron accepting capability). Melatonin and
vitamins C and E have negative A values. This implies that these
molecules will not accept an electron, i.e. it is necessary to give
some energy in order to form the anion. These molecules are
the most inefficient antiradicals (expressed as their electron
accepting capability). As in order to trap free radicals, substances
must either donate or accept electrons, animal pigments (CAR)
are better antiradicals than melatonin and vitamins. They have
lower I values than colorless substances (meaning that they are
better antioxidants), and also they are able to act as antireduc-
tants without losing energy.
Electrodonating and Electroaccepting Power. The propen-
sity to accept or donate charge can be analyzed using ω-and
ω+expressed in eqs 1 and 2. Results are presented in Table 1.
In the case of electrodonating power (ω-) low values imply
strong capability to donate electrons. In the case of electroac-
cepting power (ω+) high values imply strong capability to accept
electrons. For CAR, high values for I also imply high values
for ω-. However, this is not the case for melatonin and vitamins
because the ω-value is lower for these substances than it is in
the case of animal pigments, in contrast to I values. Apparently
ω-is a better indicator of antioxidant power than I, as it has
been claimed that vitamins represent effective antioxidant
substances. For example, there are reports that point to vitamin
E as representing the most important lipid-soluble antioxidant
present in cell membranes.49The electrodonating power of
melatonin and vitamins is higher than that of animal pigments.
According to these results, the order of reactivity expressed in
terms of facility for oxidation, referring to the ω-value, is as
i.e. colorless antioxidants represent better electron donors than
colored ones, with vitamin E representing the best antioxidant.
Similarly, yellow pigments represent better antioxidants than
red ones and the reddest pigment (ASTA) represents the worst
antioxidant. Thus, these results might indicate that in animals,
pigmentation is not a sign of antioxidant status. However, it is
important to analyze the other side of the coin, in order to
determine whether the color in animals may be an indication
of their antiradical status. For this purpose, it is necessary to
analyze A and ω+. In Table 1 it is possible to appreciate that
ω+correlates well with A. CAR are good “antireductants”, and
the reactivity order, in terms of facility for reduction considering
A and ω+values, is as follows:
i.e. red pigments are better electron acceptors than yellow or
colorless substances. ASTA is the best antireductant while
melatonin is the worst. Moreover, red pigments are better
antireductants than yellow ones, and the reddest pigment
(ASTA) is the best antiradical (considering electron capture).
Thus, both ω-and ω+results appear to indicate that, among
animals, pigmentation is not an indication of antioxidant status
but rather an indication of antiradical status. These results
suggest that it is important to analyze the charge flow direction
together with the capacity to donate or accept charge. In order
to have a complete description of the charge transfer process it
is critical to consider I and A together, as Ga ´zquez et al.43
suggested for the electrodonating and electroaccepting power
In order to analyze solvent effects, I, A, ω-and ω+were
obtained in water and benzene for the six CAR shown in Figure
3 and also for vitamins E and C. Solvent effects increase the
values with respect to those in the gas phase, but the general
pattern is preserved. Hence, the above reached conclusions are
qualitatively the same when a solvent is taken into account.
Donator Acceptor Map (DAM). In order to make a
comparison with other well-known antioxidant and antireductant
substances, experimental values of I and A for F and Na atoms
were applied to obtain the corresponding ω+and ω-values. F
represents a good electron acceptor while Na represents a good
electron donor. For any substance L, we define an electron
acceptance index as
If Ra) 1, then ωL
as F. If Ra> 1, then ωL
than F. If Ra< 1, then ωL
acceptor than F. In the same way, the electron donation index
is defined as
+and L is as good an electron acceptor
+and L is a better electron acceptor
+and L is a worse electron
If Rd) 1, then ωL
as Na. If Rd> 1, then ωL
donor than Na. If Rd< 1, then ωL
electron donor than Na.
Figure 4 shows schematically a plot of Rdvs Raproviding a
donator acceptor map (DAM). There are four regions in the
DAM, namely: (1) the best antiradical zone where L is a good
electron donor (Rd small) and a good electron acceptor (Ra
-and L is as good an electron donor
-and L is a worse electron
-and L is a better
TABLE 1: Vertical Ionization Energies (I), Vertical
Electron Affinities (A)a, Electron Donation and Acceptance
Powers (ω-and ω+) and Indexes (Rdand Ra), Obtained with
I (eV) A (eV)
1.17 0.20 0.54
aI and A values were obtained according to CAR f CAR++ 1e
[I ) E(CAR+) - E(CAR)]; CAR-f CAR + 1e [A ) E(CAR) -
E(CAR-)]. For F and Na, experimental values of I and A are used.
bComplete optimizations without symmetry constrains were done at
the BPW91/D95V level. Reference values for well known oxidant
(fluor) and reductant (sodium) are also shown.
J. Phys. Chem. A, Vol. 112, No. 38, 2008
Martı ´nez et al.
large); (2) the worst antiradical region where L is a bad electron
donor (Rdlarge) and a bad electron acceptor (Rasmall); (3) the
good antireductant sector (Raand Rdlarge) where L is a good
electron acceptor and hence a good antiradical; and (4) the good
antioxidant region (Raand Rdsmall) where L is a good electron
donor and hence also a good antiradical. Note that three of the
four zones in the DAM correspond to good antiradical sub-
stances. Using the DAM, any substance L can be classified in
terms of its electron donating-accepting capability (respect to
F and Na). As such, the DAM is a useful tool for a qualitative
comparison among substances.
In Table 1, Raand Rdfor CAR, vitamins and melatonin are
presented. Figure 5 shows the DAM for CAR, melatonin and
vitamins. Results indicate that there are no better electron
acceptors than F, but Ravalues for ASTA and ADO are very
close to 1. Only two substances, vitamin E and melatonin, are
better electron donors than Na (Rd < 1). The DAM for the
studied substances (see Figure 5) shows that CAR are in the
good antireductant zone while the colorless compounds belong
to the good antioxidant sector. ASTA is the best electron
acceptor among all studied substances. In living organisms, red
CAR pigments might act as antireductants and, as such, as
antiradicals. Yellow CAR are closer to the worst antiradical
section than the red CAR. As antiradicals, they are certainly
less effective. Vitamin E is the best antioxidant and as such a
good antiradical, while vitamin C is the worst. CAR are good
antiradicals because they are good antireductants, i.e. yellow
and red CAR are able to neutralize free radicals by accepting
electrons. Melatonin and vitamins E and A are able to scavenge
free radicals more efficiently than CAR, mainly by donating
electrons, but the capacity of these substances for accepting
electrons is very low.
It is possible to determine the antiradical capacity of CAR,
melatonin, and vitamins C and E using I, A, ω-, ω+, Raand
Rd. I, ω-and Rdrefer to the electron donor capacity. Apparently
ω-is a better indicator of antioxidant power than I. A, ω+and
Rarefer to the electron acceptor capacity. According to these
results, vitamin E is the best antiradical substance acting as an
antioxidant, while the best antiradical acting as an antireductant
is ASTA, the reddest CAR. Vitamin C is classified as not as
good an antiradical substance as either CAR or vitamin E. Using
the DAM, any substance L can be classified in terms of its
electron donating-accepting capability (with respect to F and
Na). As such, the DAM permits a straightforward qualitative
comparison among substances. Overall, our results show that
it is misleading to equate the radical scavenging function of
substances with their oxidation potential. We must consider also
their antireductant potential. The possibility of either accepting
or donating electrons must be important for the charge transfer
process, which is highly relevant for the metabolism of living
organisms. These results may be useful for interpreting the role
played by animal pigments as radical scavengers, either donating
or accepting electrons.
Acknowledgment. This study was made possible due to
funding from the Consejo Nacional de Ciencia y Tecnologı ´a
(CONACyT), as well as resources provided by the Instituto de
Investigaciones en Materiales IIM, UNAM. The work was
carried out, using KanBalam supercomputer, provided by
DGSCA, UNAM. We would like to thank The Direccio ´n
General de Servicios de Computo Acade ´mico (DGSCA) of the
Universidad Nacional Auto ´noma de Me ´xico for their excellent
and free supercomputing services. We would also like to thank
Caroline Karslake (Masters, Social Anthropology, Cambridge
University, England) for reviewing the grammar and style of
the text in English. The authors would like to acknowledge both
Sara Jime ´nez Corte ´s and Marı ´a Teresa Va ´zquez for their
technical support. A.M. and M.C. are grateful for financial
support from the Ministerio de Educacio ´n y Ciencia de Espan ˜a
and DGAPA-UNAM-Me ´xico. A.B. was supported by the
projects CGL2004-02348 and POL2006-05175 funded by the
Spanish Ministry of Education and the European Regional
Development Fund. M.A.R.-G. was supported by the project
CGL2007-63223, funded by the Spanish Ministry of Education
and the European Regional Development Fund.
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