Reaction of carotenoids and ferric chloride: Equilibria, isomerization, and products

Article abstract of DOI:10.1021/jp034063q

In the oxidation of carotenoids, ethyl all-trans-8a?2-apo-?2-caroten-8a?2-oate and all-fraws-?2-carotene, with ferric chloride, several equilibria occur between Fe³⁺, Fe²⁺, Cl^-, the neutral carotenoid, and its radical cation and dication. The radical cation and dication were found to abstract an electron from Fe²⁺. Isomerization of carotenoids occurs during the oxidation. In the presence of air, a stable product is formed in high yield during the oxidation. ¹H NMR, LC-MS, and optical studies show that this product is the 5,8-peroxide of the starting material. A mechanism for the formation of this compound is proposed.

Full text of DOI:10.1021/jp034063q

J. Phys. Chem. B 2003, 107, 5333-5338
5333
Reaction of Carotenoids and Ferric Chloride: Equilibria, Isomerization, and Products
Yunlong Gao and Lowell D. Kispert*
Department of Chemistry, UniVersity of Alabama, Box 870336, Tuscaloosa, Alabama 35487-0336
ReceiVed: January 10, 2003; In Final Form: March 28, 2003
In the oxidation of carotenoids, ethyl all-trans-8′-apo-â-caroten-8′-oate and all-trans-â-carotene, with ferric
3
+
2+
-
chloride, several equilibria occur between Fe , Fe , Cl , the neutral carotenoid, and its radical cation and
2
+
dication. The radical cation and dication were found to abstract an electron from Fe . Isomerization of
carotenoids occurs during the oxidation. In the presence of air, a stable product is formed in high yield during
the oxidation. H NMR, LC-MS, and optical studies show that this product is the 5,8-peroxide of the starting
1
material. A mechanism for the formation of this compound is proposed.
Introduction
SCHEME 1
It is known that carotenoids serve as light harvesting agents
in photosystems,1,2 act as “triplet valves” to harmlessly dissipate
the energy of chlorophyll (Chl) triplets, and are scavengers of
3
singlet oxygen which can destroy Chl. In the absence of
antioxidants, the carotenoids are unstable to heat, light, and air/
oxygen, degrading to compounds with smaller molecular
4
weights. Oxidation of carotenoids under various conditions and
in different systems5 has been used to generate products. Most
of the products identified to date are carbonyl compounds of
the apo-â-carotenal or apo-â-carotenone types. In the oxidation
of all-trans carotenoids with ferric chloride (FeCl3) in anhydrous
-8
9
•+
dichloromethane, carotenoid radical cations (Car ) and cis
isomers are formed in the reaction mixture.
3+
2+
It was found that several equilibria exist among Fe , Fe ,
the neutral carotenoid, and its radical cation and dication. The
radical cation and dication can also abstract an electron from
Car is also formed in photosystem II reaction centers.10-12
The formation and accumulation of the radical cations were
found to be induced by the photoaccumulated primary electron
acceptor radical P680 (Car donates an electron to P680 ).
Car can be reduced by electron donation from a monomeric
•+
2+
Fe . A stable oxidation product was formed in the presence
of O2. LC-MS, H NMR, and optical studies show that this
product is the 5,8-peroxide of Car. A reaction mechanism for
the formation of this compound is proposed.
1
•
+
•+
•
+
13
Chl and also by cytochrome b559. To understand the roles of
•
+
Car in photosystem II reaction centers, the physiochemical
Experimental Section
•
+
14
properties of Car need to be studied. It has been shown that
•
+
the use of FeCl3 to form Car also allows for the convenient
optical study of the carotenoid dication (Car ) formed from
Ethyl all-trans-8′-apo-â-caroten-8′-oate (I) was a gift from
Hoffmann-LaRoche, Basel; all-trans-â-carotene (II) and ferric
chloride (FeCl3) were purchased from Sigma; and benzyltri-
ethylammonium chloride (BTAC), silver tetrafluoroborate (Ag-
BF4), and anhydrous dichloromethane (CH2Cl2) were purchased
from Aldrich. Acetonitrile of HPLC grade, obtained from Fisher,
was treated with potassium carbonate before use. All-trans-â-
carotene was purified by extraction with benzene and precipita-
tion with methanol. The carotenoids were stored in the dark at
-14 °C in a desiccator containing CaSO4 and were allowed to
warm to room-temperature just before use. Tetrabutylammonium
hexafluorophosphate (TBAHFP) was obtained from Fluka.
The optical spectra were recorded with a double beam
Shimadzu UV-visible 1601 spectrophotometer (190-1100 nm)
using 1 cm quartz cells. A Vydac 201 TP54 polymeric C18
column (250 × 4.6 mm i.d.) packed with 5 µm particles
(Hesperia, CA) and a Shimadzu LC-600 pump with a SPD-
M10AVP PDA detector were used for the HPLC separation
and detection. LC-MS experiments were performed by directing
the column effluent to an APCI (atmospheric pressure chemical
ionization) MS. Acetonitrile was the mobile phase. A funnel
2+
•
+
2+
Car at room temperature. Formation of Car electrochemi-
cally requires low temperature (-70 °C) procedures and dealing
with the resulting difficulties with moisture. However, it has
been shown that high yields of cis isomers are obtained by the
electrochemical method due in part to the better control of the
reaction conditions. Nonetheless, degradation of the carotenoids
by electrochemical and FeCl3 oxidation methods is smaller than
by thermal methods. It has also been shown when dichlo-
romethane solutions of carotenoids are treated with small
amounts of FeCl3 that extensive photodegradation occurs upon
subsequent irradiation with near UV to visible light. Further
questions arise as to why there are differences between
9
15
•
+
electrochemical and FeCl3 preparation of Car as well as what
•+
products are formed upon reaction of O2 with Car . To address
these questions, we choose two natural carotenoids ethyl all-
trans-8′-apo-â-caroten-8′-oate (I) and all-trans-â-carotene (II)
(see Scheme 1).
*
To whom correspondence should be addressed.
1
0.1021/jp034063q CCC: $25.00 © 2003 American Chemical Society
Published on Web 05/13/2003

5334 J. Phys. Chem. B, Vol. 107, No. 22, 2003
Gao and Kispert
2 2
Figure 1. UV/vis/NIR spectra (a) of pure I in CH Cl , (b) after adding
1
equiv FeCl , (c) 5 min later, (d) 10 min later.
3
Figure 3. HPLC showing product formation in the reaction of I (a)
and II (b) with FeCl . The solid line is that of the product, and the
3
dashed line is that of the starting material.
product will be described later. Peak x which appears during
the oxidation could be due to the dication of the starting material.
Because, according to previous ZINDO/S calculations and
1
4
2+
optical studies, the absorption peak of Car should appear
•
+
between those of Car and Car . Peak x may also be due to the
radical cation of the product. Figures 1 and 2 exhibit two well-
defined isosbestic points, that is, wavelengths at which the
absorbance does not change with time during the reaction. It is
generally accepted that occurrence of an isosbestic point in a
closed system requires that the changes in the concentrations
of the various components be linearly related. Because the
dication was not produced during the initial oxidation (assume
peak x is due to the dication) and formation of Car from Car
is known to be fast, the possibility that the product is from the
dication can be ruled out. This was also demonstrated by the
fact that the yield of the product is very low when the
concentration of FeCl3 is high (the dication of the starting
material was produced at the initial oxidation). Whether the
neutral starting material is a direct precursor of the product is
unclear.
1
9
Figure 2. UV/vis/NIR spectra (a) pure II in CH
2
Cl
2
, (b) after adding
0
.2 equiv FeCl , (c) 5 min later, (d) 10 min later.
3
2+
•+
containing silica gel was used for rapid filtration of the solution
to remove inorganic species and ions before injection.
9
Osteryoung square-wave voltammetry (OSWV) was per-
formed with a BAS-100 B/W electrochemical analyzer in a
conventional three-electrode system at room temperature.
TBAHFP was the supporting electrolyte. A platinum disk
electrode was selected as working electrode, a platinum wire
was selected as the counter electrode, and a saturated calomel
electrode (SCE) was selected as the reference electrode.
The bulk electrolysis experiment was performed by using a
platinum gauze as the working electrode, a platinum wire as
the counter electrode, and a silver wire as the pseudo reference
electrode. The applied electrolysis potential was 1 V.
Parts a and b of Figure 3 show the HPLC of the products for
I and II after 10 min reaction with 1 equiv of FeCl3, respectively.
The small peaks close to the product are probably due to isomers
of the product because the UV/vis absorption spectra of these
peaks, which are obtained by the PDA detector, are similar to
that of the product. The starting material disappears after 10
min reaction.
Separation of products was performed on a silica gel column;
1
the eluent was CH2Cl2. H NMR spectra of the products in
To ascertain whether the product is due to the reaction of
1
CDCl3 were determined with a Bruker AM 360 ( H, 360.13
•+
-
-
Car with Cl , the concentration of Cl was increased by
adding BTAC to the reaction mixture of I and FeCl3 to observe
whether the formation of the product increases. Surprisingly,
MHz) spectrometer.
AM1 and ZINDO/S17,18 semiempirical molecular orbital
calculations were carried out using Hyperchem 6.03 software
on a Dell computer (Pentium III).
16
•
+
the peak of Car disappeared at once, and the intensity of the
starting material increased significantly (see Figure 4), indicating
that Car is reduced to Car. Where does the electron come
from? It is known
FeCl4 in H2O. Does this reaction also occur in CH2Cl2? Figure
•
+
Results and Discussion
20-22
3+
-
that Fe can react with Cl to form
-
Figures 1 and 2 show the UV/vis spectra of the oxidation of
I and II with one equiv of FeCl3 in CH2Cl2 in the presence of
air. The absorption near 440 nm is due to the neutral starting
material. The absorption peak in the near infrared region is due
to the D0fD2 transition of the carotenoid radical cation
5
shows the UV/vis spectrum of the reaction of FeCl3 with 2
equiv of BTAC in CH2Cl2. The two peaks with absorption at
-
21
3
14 and 360 nm are typical for FeCl4 . The two peaks
+
disappear after addition of Ag to the solution due to the reaction
•
+ 14
(
Car ). The intensity of this peak decreases with time and a
FeCl4- + Ag f FeCl + AgCl
+
new absorption peak about 30 nm blue-shifted compared to the
3
•+
starting material increases with time, indicating that Car reacts
with other species to form the product. Identification of the
The reduction of Car•+ is due to the decrease of Fe3+

Reaction of Carotenoids and Ferric Chloride
J. Phys. Chem. B, Vol. 107, No. 22, 2003 5335
Figure 4. UV/vis/NIR spectra showing the effect of increasing the
-
concentration of Cl in the reaction of I and FeCl
3
. (a) Pure I in CH
2
-
Cl
2
, (b) 1 min after adding 1 equiv FeCl
Cl solution.
3
to I, (c) after adding 1 drop
of saturated BTAC CH
2
2
Figure 6. UV/vis/NIR spectra showing the effect of adding AgBF
the reaction solution of I and FeCl . (a) Pure I in CH Cl , (b) 5 min
after adding 1 equiv FeCl , (c) after adding 1 drop of saturated AgBF
CH Cl solution to (b).
4
to
3
2
2
3
4
2
2
Figure 5. UV/vis/NIR spectra showing the formation of FeCl -
0 µM FeCl reacts with 100 µM BTAC (solid line) and the dissociation
after addition of 200 µM AgBF (dashed line).
after
4
2
3
-
of FeCl
4
4
concentration when FeCl4- forms. The equilibrium is
Car + Fe h Car•+ + Fe
3
+
2+
According to the initial concentrations of Car and Fe3+ and
Figures 1a,b and 2a,b, the calculated equilibrium constants are
about 1 and 2.5 for the redox reactions of I and II, respectively.
•+
The difference is probably due to the fact that Car (I) contains
an electron-withdrawing group and favors the back reaction.
•+
The above experiment implies that Car can abstract an electron
2+
from Fe . Another experiment shows that decreasing the
-
concentration of Cl by adding AgBF4 to the reaction mixture,
which results in the formation of AgCl, can increase the
concentration of the radical cation (see Figure 6).
2+
Figure 7. UV/vis/NIR spectra showing that the dication of I (a) and
II (b) can also abstract an electron from Fe2 . (1) Starting material;
To examine whether Car can also abstract an electron from
+
2+
Fe , excess FeCl3 (about 4 equiv) was added to I and II CH2-
Cl2 solutions. Parts a and b of Figure 7 show the UV/vis spectra
for the reaction mixtures of I and II, respectively. The absorption
peak in the near infrared region is much broader than those in
(
2) after the starting material was treated with 4 equiv FeCl
subsequent addition of a drop of saturated AgBF (about 2 equiv of
FeCl ).
3
, (3) after
4
3
2
+
used to determine the reduction potentials of Car2+ and Car•+:
Figures 1 and 2. Because the absorption peak of Car should
•
+
2+
appear between the maxima of Car and Car , the broad peak
oxidation of I for 1 min at 1100 mV (vs SCE) to produce Car
•
+
2+
could be due to overlap of Car and Car . These peaks
disappear at once after addition of excess of BTAC and the
peaks of neutral starting material reappear (the intensity of the
neutral starting material is lower than that before addition of
FeCl3 because of the dilution of the solution after addition of
was then followed by scanning the voltage from +1100 to -100
2
+
•+
mV. The reduction potentials for Car and Car are 928 and
800 mV (vs SCE), respectively (solid line in Figure 8). When
I was treated with 4 equiv of FeCl and then scanned from
3
+1100 to -100 mV, the same reduction potential peaks for
•
+
2+
2+
•+
FeCl3 and BTAC solution), indicating that both Car and Car
Car and Car appeared (dashed line in Figure 8), indicating
2+
2+
can abstract an electron from Fe .
that Car is produced when I is treated with 4 equiv of FeCl3.
2
+
OSWV was also used to examine the formation of Car (I)
when I was treated with 4 equiv of FeCl3. OSWV was first
The reduction potential peaks appear at 288 and 56 mV are
attributed to those of iron ions. For II, the reduction potentials

5336 J. Phys. Chem. B, Vol. 107, No. 22, 2003
Gao and Kispert
SCHEME 2
Figure 8. OSWV of Car2+ and Car•+ of I. Solid line: Oxidation of I
2
+
for 1 min at 1100 mV (vs SCE) to produce Car was then followed
by scanning the voltage from +1100 to -100 mV. Dashed line: I was
treated with 4 equiv of FeCl
mV.
3
and then scanned from +1100 to -100
SCHEME 3: Structure of the 5,8-Peroxide of Car
To determine whether the products are produced by participa-
tion of O2 present in air, the reactions were carried out in a
cuvette in a N2 drybox. After 10 min, the cuvette was sealed
and taken out of the drybox, and the spectra were then measured.
The absorption peak of the product and peak x were absent,
but they appeared after the reaction mixture was exposed to
O2. From Figure 1, we can see that if the reaction is carried out
in the presence of air, a strong peak of a product appears 10
min later, indicating that O2 was involved in the formation of
the product.
Figure 9. HPLC showing equilibria exist in the reaction of I with
FeCl . (a) Pure I, (b) 30 s after I was treated with excess FeCl , (c)
solution b treated with 1 drop of saturated BTAC CH Cl solution
wavelength: 441 nm, the strongest absorbance of I, intensity normal-
ized to strongest peak).
3
3
Based on the above results, the mechanism shown in Scheme
2
2
2
is proposed for the reaction of Car with FeCl3 in CH2Cl2 in
(
the presence of oxygen. According to this scheme, the concen-
tration of the dication of the starting material should decrease
as the concentrations of neutral and radical cation species
decrease. Because, however, the intensity of peak x in Figures
1 and 2 increases with the decrease in concentration of these
two species, peak x is not due to the dication of the starting
material. Oxidation of the isolated product with FeCl3 in
CH2Cl2 shows that a peak with the same absorption as peak x
appears, implying that it is due to the radical cation of the
product.
for Car•+ and Car2+ are almost the same and cannot be
distinguished by OSWV.
HPLC was used to further corroborate the equilibria. Figure
9
shows that a stable product was produced 30 s after I was
treated with excess FeCl3 (about 4 equiv of I) and all of the
starting material was consumed. The peaks of I and its cis
isomers appeared after adding a drop of saturated BTAC CH2-
Cl2 solution to the reaction solution, indicating that one or more
equilibria exist. Because the stable product was produced after
all starting material was consumed, the neutral starting material
is not a direact precursor of the product. Similar results were
found for II. The identification of the cis isomers is according
APCI LC-MS can provide rapid identification and quantifica-
2
6
+
tion of carotenoid oxidation products. The [M + H] ion is
26
usually detected by this method. APCI LC-MS shows that the
base peak has the molecular mass of the starting material plus
33 (493 and 569 for the two cases, respectively. The mass of I
and that of II are 460 and 536, respectively), indicating that O2
9
,23,24 1
to previous results.
H NMR spectroscopy and values of
2
5
the Q ratio (absorbance of the “cis peak”/absorbance of the
most intense maximum) were used to identify these isomers.
The mechanism proposed below can account for the formation
of cis isomers
2
7-30
has added to Car. According to other studies,
the product
was tentatively assigned to the 5,8-peroxide of Car (CarO2) (see
Scheme 3).
1H NMR data for the 5,8-peroxides of Car have been reported
only for short chain carotenoids such as the 5,8-peroxide of
trans-Car•+ h cis-Car•+
trans-Car + h cis-Car2+
3
1
ethyl 15-apo-â-caroten-15-oate. To establish the structure of
peroxides of Car with long chains such as I and II, NMR studies
2
1
are needed. The H NMR spectra (Figure 10) of I and its
cis-Car + + Fe h cis-Car•+ + Fe
2
2+
3+
reaction product show that the chemical shifts of the protons
of the product are almost the same as those of I, with the
exception of H-7 and H-8. Similar results were found for II.
The chemical shifts of H-7 and H-8 of the products are the same
as those of the 5,8-peroxide of ethyl 15-apo-â-caroten-15-oate
cis-Car•+ + Fe h cis-Car + Fe3+
2+
23
According to a previous study, isomerization of Car is
•
+
2+
31
mediated by Car and Car .
reported by Pfoertner (5.56 and 4.65, respectively).

Reaction of Carotenoids and Ferric Chloride
J. Phys. Chem. B, Vol. 107, No. 22, 2003 5337
The formation of the 5,8-peroxide should be due to other
3
7
mechanisms. It is known that radical cations of organic
•
-
compounds may react with O2 to form peroxides. A possible
reaction mechanism for the formation of CarO2 in the oxidation
of Car with FeCl3 in the presence of O2 is shown below:
Car + Fe h Car•+ + Fe
3
+
2+
O + Fe h O2•- + Fe
2
+
3+
2
Car•+ + O2 h CarO2
•-
CarO + Fe h CarO2•+ + Fe
3
+
2+
2
However, according to this mechanism, the concentrations of
•
+
•+
Car and the radical cation of the product (CarO2 ) cannot be
linearly related, and there should be no isosbestic point between
•
+
•+
the peaks of Car and CarO2 in Figures 1 and 2. The same
product was formed in the electrolysis of the neutral starting
material in the presence of O2, indicating that the product is
•
+
•-
probably due to the reaction of Car and O2 because O2
cannot be produced under our electrolysis conditions. We
propose the following mechanism for the formation of CarO2
in the oxidation of Car with FeCl3 in the presence of O2:
Car + Fe h Car•+ + Fe
3
+
2+
Car•+ + O f CarO
•+
2
2
CarO2•+ + Fe h CarO + Fe
2+
3+
2
Figure 10. 1H NMR spectra in CDCl
c).
of I (a) and the product (b) and
3
(
CarO2•+ + Car h CarO + Car
•+
2
TABLE 1: λmax (nm) Calculated by ZINDO/Sa
0 2
fS D fD
This mechanism is consistent with the facts that the concentra-
tions of Car , CarO2 , and CarO2 are linearly related and that
the concentrations of both CarO2 and CarO2 increase with
S
0
2
•
+
•+
Car•+
•+
CarO
2
Car
CarO
2
•
+
I
II
415 (446)
434 (460)
400 (420)
398 (432)
814 (848)
872 (973)
720 (658)
843 (790)
•+
the decrease of Car and Car.
a
The λmax (nm) in CH
2
Cl
2
determined by experiment is in paren-
Conclusions
theses.
In the oxidation of carotenoids with FeCl3, there exist
equilibria among the carotenoid, the radical cation, dication,
and various inorganic species. In addition, the radical cation
The optical absorption of CarO2 is blue-shifted compared to
that of Car because the conjugated chain of CarO2 is shorter
than that of Car. The maximum absorption wavelengths (λmax)
2
+
and dication can abstract an electron from Fe . This phenom-
enon is more pronounced for Car containing an electron-
•
+
•+
of Car, CarO2, Car , and CarO2 by gas-phase ZINDO/S
calculations are listed in Table 1. The maxima of these species
in CH2Cl2 determined by UV/vis are also included. The
geometries of these species were optimized using the AM1
method. The restricted Hartree-Fock (RHF) formalism was
used to optimize the geometries of the neutral species, and
unrestricted Hartree-Fock (UHF) was used to optimize those
of radical cations. The single-excitation configuration interaction
was used to calculate the optical absorption spectrum. The
weighting factors for σ-σ and π-π overlap are 1.267 and
•
+
2+
withdrawing group. Isomerization via Car and Car occurs
during the oxidation. The 5,8-peroxide of Car is formed when
the reaction mixture is exposed to O2. The formation of this
•+
compound is attributed to the reaction of Car with O2. Whether
such a reaction exists in the reaction center of photosystem II,
•+
and thus protects it, needs further study. Because Car is also
28-30,32-34
formed by photoillumination, the previous studies
need
to be reexamined: Is the formation of the 5,8-peroxide of Car
due to the oxidation of Car by singlet oxygen, or is it due to
•
+
0
.585, respectively. The calculation shows that, although the
the reaction of Car with O2, or both? This study gives both
NMR and MS evidence for the formation of the 5,8-peroxide
absolute values of the calculated absorption wavelengths do not
match the experimental value, the relative absorption wave-
lengths for the different species are in agreement with the
experimental values.
28-30,32-36
of carotenoids with long chains. Previous studies
gave
only LC-MS evidence for the formation of the 5,8-peroxide of
II because of difficulties in the purifications.
2
8-30,32-34
The 5,8-peroxide of long-chain Car is a specific marker for
Oxidation of Car by singlet oxygen
oxidation
or by thermal
3
0,32-34
28,35,36
singlet oxygen quenching by Car,
but it was also found
in other systems affords many products, and
in the thermal oxidation.2
8,35,36
Formation of singlet O2 is usually
the yield of 5,8-peroxide is very low so that separation of this
compound on a preparative scale is impossible. The strong
selectivity and high yield (more than 90%) of this compound
produced by the method described in this study should facilitate
due to energy transfer from the excited state of a sensitizer to
the triplet ground state of O2. In the present study, the reaction
mixture was kept in the dark and singlet O2 cannot be formed.

5338 J. Phys. Chem. B, Vol. 107, No. 22, 2003
Gao and Kispert
the synthesis and purification of this group of carotenoids so
that physiochemical properties of these compounds can be
studied in the future. These compounds may be precursors of
other degradation products, when carotenoids are oxidized in
the presence of O2. Study of these compounds may contribute
to understanding the degradation pathway of carotenoids in
biological systems.
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7
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(
Acknowledgment. We thank Dr. E. Hand for helpful
discussions. This work was supported by the Division of
Chemical Sciences, Office of Basic Energy Sciences, Office of
Energy Research of the U.S. Department of Energy under Grant
No. DE-FG02-86ER13465.
(
1
(
3
(
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