Chiral Amplification in Nature: Studying Cell-Extracted Chiral Carotenoid Microcrystals via the Resonance Raman Optical Activity of Model Systems

Article abstract of DOI:10.1002/anie.201901441

Carotenoid microcrystals, extracted from cells of carrot roots and consisting of 95 % of achiral β-carotene, exhibit a very intense chiroptical (ECD and ROA) signal. The preferential chirality of crystalline aggregates that consist mostly of achiral building blocks is a newly observed phenomenon in nature, and may be related to asymmetric information transfer from the chiral seeds (small amount of α-carotene or lutein) present in carrot cells. To confirm this hypothesis, we synthesized several model aggregates from various achiral and chiral carotenoids. Because of the sergeant-and-soldier behavior, a small number of chiral sergeants (α-carotene or astaxanthin) force the achiral soldier molecules (β- or 11,11′-[D₂]-β-carotene) to jointly form supramolecular assemblies of induced chirality. The chiral amplification observed in these model systems confirmed that chiral microcrystals appearing in nature might consist predominantly of achiral building blocks and their supramolecular chirality might result from the co-crystallization of chiral and achiral analogues.

Full text of DOI:10.1002/anie.201901441

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Accepted Article
Title: Chiral Amplification in Nature: Cell-extracted Chiral Carotenoid
Microcrystals Studied Via RROA of Model Systems
Authors: Monika Anna Dudek, Ewa Machalska, Tomasz Oleszkiewicz,
Ewa Grzebelus, Rafal Baranski, Piotr Szcześniak, Jacek
Mlynarski, Grzegorz Zajac, Agnieszka Kaczor, and
Malgorzata Baranska
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To be cited as: Angew. Chem. Int. Ed. 10.1002/anie.201901441
Angew. Chem. 10.1002/ange.201901441
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Chiral Amplification in Nature: Cell-extracted Chiral Carotenoid
Microcrystals Studied via RROA of Model Systems
Monika Dudek, Ewa Machalska, Tomasz Oleszkiewicz, Ewa Grzebelus, Rafal Baranski,
Piotr Szcześniak, Jacek Mlynarski, Grzegorz Zajac, Agnieszka Kaczor* and Malgorzata Baranska*
Abstract: Intriguingly, we have observed that carotenoid
microcrystals, extracted from cells of carrot roots and built from 95%
achiral β-carotene, exhibit a very intense chiroptical (ECD and ROA)
signal. This serendipitous discovery of preferential chirality of
crystalline aggregates, composed mostly from achiral building blocks
is a newly observed phenomenon in nature and with high probability
may be related to asymmetric information transfer from chiral seeds
(small amount of α-carotene or lutein) present in carrot cells. To
confirm this hypothesis, we have synthesized several model
aggregates built from various achiral and chiral carotenoids.
Because of the sergeant-and-soldier behaviour, a small number of
chiral sergeant (α-carotene or astaxanthin) forced achiral soldier
molecules (β- or 11,11’-d2-β-carotene) to form jointly supramolecular
assemblies of induced chirality. Chiral amplification observed in
these model systems proved that chiral microcrystals appearing in
nature might be composed predominantly from achiral building
blocks and their supramolecular chirality might be the result of co-
crystallization of chiral and achiral analogues, due to their proximity
in cell compartments.
amplification. To explore this phenomenon, we prepared model
aggregates built from the combination of chiral and achiral
carotenoids, following a sergeant-and-soldiers rule.[7,8] According
to the effect, a small number of chiral units (sergeants) forces a
large number of achiral ones (soldiers) to adopt
a
supramolecular structure and to display an intense chiral
signal.[9,10] This kind of chirality amplification was observed for
other supramolecular systems[11–13] like foldamers,[14] helical
nanotubes and columns,[15,16] as well as for polymers and
copolymers.[17–19] The chiral sense of studied here model
aggregates comes from the chirality transfer between: chiral αC
or astaxanthin (AXT) molecules and achiral βC components,
which together form a mixed supramolecular chiral systems
exhibiting the resonance enhancement of ROA (RROA). On the
other hand, aggregates composed of only chiral carotenoids
were studied by us before.[20–23] Those assemblies also show a
strong optical activity, generated by a non-symmetric layout of
molecules through the non-covalent interactions (π–π stacking,
hydrogen bonding, hydrophobic effects). In detail, the chiral
information from a carotenoid chiral centre is imposed to the
whole system containing a chromophore (polyene chain) in the
chiral conjugated arrangement. The process of carotenoid
aggregation enables observation of a significant enhancement in
the ROA scattering, called by us the Aggregation-Induced
Carotenoid microcrystals are formed in crystalline chromoplasts
of carrot root,[1,2] where a needle-like, rhomboidal, and helical
types can be found.[3,4] The size of those crystalline aggregates
is usually of a few μm up to 20 μm, what was determined by
means of the AFM technique.[3] The predominant component of
natural microcrystals is achiral β-carotene (βC) accompanied by
a small contribution of chiral α-carotene (αC) and lutein.[3–5]
Moreover βC molecules constitute ca. 95% of total carotenoids
content of measured specious.[6] Despite the achiral composition,
microcrystals reveal natural chirality at the supramolecular level.
Here, we present the study of carotenoid microcrystals, as well
as several model systems using Electronic Circular Dichroism
(ECD) and Raman Optical Activity (ROA). We want to prove the
hypothesis that microcrystals’ optical activity might be driven by
the process of chirality induction, leading to a chiral signal
Resonance
Raman
Optical
Activity
(AIRROA).[20–23]
Nevertheless, ROA spectroscopy is hampered by its low
sensitivity, because only one photon in a billion gives rise to the
ROA effect.[24] The AIRROA phenomenon causes a substantial
increase in the ROA intensity due to the aggregation of
supramolecular chiral structures, of a resonantly enhanced
chiroptical signal. The high vibrational specificity and the
enhanced sensitivity of AIRROA make it a unique tool to explore
chirality of supramolecular model aggregates and natural
carotenoid microcrystals. Amplification of chirality in momentary
asymmetric systems is considered a key phenomenon in
understanding the origin of homochirality of biological
macromolecules.[25] This model study on chiral amplification in
dynamic supramolecular systems proves that chiral
microcrystals may appear in nature purely in the
physicochemical process of chiral induction due to the proximity
of achiral and chiral analogues in the cell environment.
[*]
M. Dudek, E. Machalska
Faculty of Chemistry, Jagiellonian University, Gronostajowa 2,
30-387 Cracow (Poland)
T. Oleszkiewicz, E. Grzebelus, R. Baranski
Institute of Plant Biology and Biotechnology, Faculty of
Biotechnology and Horticulture, University of Agriculture in Krakow,
AL. 29 Listopada 54, 31-425 Cracow (Poland)
Here we focus on crystalline aggregates released from
carrot cells using an extraction procedure described in the
Supporting Information. Microscopic images of helical,
rhomboidal, and needle-like microcrystals are presented in
Figure 1. The ECD spectrum reveals quite strong negative–
positive bands (going from longer to shorter wavelengths),
known as bisignate Cotton effects, with a clearly accentuated
vibrational structure, also seen in the UV-Vis spectrum and
typical for carotenoids without conjugated carbonyl groups (like
βC).[26–28] Because of the coincidence of the ROA excitation
laser line (532 nm) with an absorption of the main chromophore,
carotenoid microcrystals show an enhanced and monosignate
RROA spectrum (Figure 1), opposite in sign to the ECD
P. Szcześniak, J. Mlynarski
Institute of Organic Chemistry, Polish Academy of Sciences,
Kasprzaka 44/52, 01-224 Warsaw (Poland)
G. Zajac, A. Kaczor, M. Baranska
Faculty of Chemistry, Jagiellonian University, Gronostajowa 2,
30-387 Cracow (Poland)
Jagiellonian Centre for Experimental Therapeutics (JCET),
Jagiellonian University, Bobrzynskiego 14, 30-348 Cracow (Poland)
E-mail: kaczor@chemia.uj.edu.pl, baranska@chemia.uj.edu.pl
Supporting information for this article is given via a link at the end of
the document.
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Figure 1. Optical images of microcrystal isolated from carrot cells. The size of aggregates is of a few μm up to 20 µm. The ECD spectrum shows strong,
negative/positive chiral signal (from -30 to 15 mdeg) in the range of the UV-Vis spectrum. The ROA laser (green dashed line, 532 nm) coincides with the
microcrystal absorption, thus the resonance Raman (dotted line) and ROA (solid line) spectra were recorded. A, B, C symbols represent inserts of Raman and
RROA bands in the appropriate spectrum range.
transition in the excitation range, in agreement with Nafie’s
theory of the Single Electronic State (SES) limit.[29] We observe
characteristic RROA bands due to typical carotenoid vibrations,
i.e.: 1 at 1519 cm–1, 2 at 1159 cm-1, 3 at 1009 cm–1, and 4 at
956 cm–1, which are assigned to the C=C stretching, C–C
stretching, the in-plane CH3 rocking, and the C−H out-of-plane
wagging motions coupled with the C=C out-of-plane torsion
modes, respectively.[30,31] In addition, the RROA shoulder
localized at 967 cm–1 is associated with the symmetric C–H and
C out-of-plane wagging[32] with a small contribution due to β
rings’ deformations[31] and the C–C stretching vibrations.[33] The
Raman imaging study reported that the position of the 1 band at
1519 cm–1, as well as the 1/2 ratio of integral intensities (1.005)
is specific for the helical crystalline aggregates and the presence
of βC in crystal content.[3,4] We claim, that the presence of those
features in the RROA spectrum is related with the induced chiral
information from βC. In addition, the band at 956 cm–1 is
characteristic for both the needle-like and rhomboidal
microcrystals. (A detailed spectral analysis is given in the
Supporting Information).
βC molecules aggregate in the hydrated organic
environment, which is seen by the shift of the UV-Vis band, as
well as by the frequency decrease of the 1 Raman band, in
comparison to the monomer spectrum (Figure 2, left). Moreover,
βC has a tendency to form J-type aggregates[34] (a red-shift of an
absorption band) due to the methylated and twisted cyclohexene
rings, as well as the lack of OH groups. For flatter carotenoids
(for example lutein), the H-type aggregates are favourable, in
which π,π-stacking and hydrogen bonds are stronger.[2,35,36] βC
assemblies do not give chiroptical signals, as seen in the ECD
and RROA spectra (Figure 2, left). Thus, the chirality of a
monomer plays an important role in the chirality of the
supramolecular system, and its lack results in the formation of
racemic aggregates from a macroscopic perspective.[9] In
contrast to βC, a model system built from the combination of
achiral βC (80%) and chiral αC (20%) shows a chiral signal in
the ECD and RROA spectra (Figure 2, right). To prove the
induction of βC chirality at the supramolecular level a few strong
spectral features can be pointed out: 1/ the outlined vibrational
[26–28]
ECD/UV-Vis structure;
2/ the value of Raman and RROA
1/2 ratio close to 1 (0.95);[3] 3/ the position of 1 Raman and
RROA band at 1520 cm–1, i.e. shifted. Similar to carotenoid
microcrystals, we observe the RROA band at 965 cm–1 due to
the hydrogen-out-of-plane (HOOP) motions. The HOOP mode is
recognized as a sensitive marker of distortion of the polyene
chain.[37,38] Therefore, its occurrence is most likely related to the
bending of the carotenoid chain in the βC/αC model, which
probably comes from αC, whose structure is more bent (Figure
S2). Overall, it is important to note that the non-chiral (UV-Vis
and Raman) spectra of the achiral (βC) and chiral (βC/αC)
systems are strikingly similar, confirming that both aggregates
are structurally similar. In addition, the Raman spectra of both
aggregates resemble closely the ROA spectrum of the βC/αC
system, showing that the chiral signal is predominantly related to
βC.
To exclude further the possibility that the chiral signal
recorded for the βC/αC model results solely from αC molecules,
we investigated the concentration-dependent behavior of αC in a
water–acetone solution. Figure 3 (left) shows clearly that αC
aggregates at such small concentrations do not give
a
noticeable chiroptical signal. In particular, the αC assemblies
obtained at the concentration used for the βC/αC system also do
not give any ECD spectrum (cyan line). On the other hand, the
ECD signal is already observed for the βC/αC 95:5% system,
where a chiral αC constitutes only 5% of the total carotenoid
content, i.e. at the concentration of ca. 4·10–7 M (Figure 3, right,
violet line).
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Figure 2. Comparison of βC aggregate (orange) and βC/αC system (pink). The UV-Vis spectrum of βC aggregate is red shifted, but the ECD does not show
a chiral signal. Contrarily, the ECD of βC/αC system presents intense positive/negative bands (from 20 to -20 mdeg), stable after 24 hours (pink, dashed line).
In like manner, βC aggregate does not give the RROA spectrum, but βC/αC model does (the negative profile of RROA). The Raman spectra of both systems
(dotted line) and monomer (black, dotted line) are also presented. A, B show inserts of the Raman and RROA profiles in the appropriate spectrum range.
* represents Raman acetone bands.
Figure 3. Left panel: The concentration dependent ECD and UV-Vis spectra of αC in the aggregated form. Violet colour means the lowest concentration
of αC used in the preparation of βC:αC95:5% mixed aggregate (panel right). Cyan colour represents the αC concentration used in the formation of βC/αC
model system (Figure 2). Right panel: ECD and UV-Vis spectra of mixed aggregate consisting of 95% βC and 5% αC.
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To verify the induced chirality of βC in aggregated mixed
systems, we built another model using (3S,3S)-astaxanthin
(AXT) as a chiral sergeant and compared it with a system
containing solely AXT. As presented in Figure 4 (left), the
βC/AXT model system also shows a strong optical activity. The
outlined ECD vibrational structure (maxima located at 518, 485,
454 nm), the position of the RROA 1 band (1519 cm–1) and the
ratio between integral intensities of 1/2 (1.12), may be
recognized as typical for βC in the aggregated form and may be
considered as a chiral response of βC at the supramolecular
level. Moreover, these spectral features are significantly different
compared with single aggregated AXT molecules (Figure 4,
right). The red-shift of the UV-Vis band, and the frequency
decrease of the Raman C=C mode (1525  1521 cm–1) are
typical for the J-type arrangement, which has been studied in
detail before.[22,23] To confirm that the chiral signal of the βC/AXT
model is not a result of the chirality of AXT itself, we highlight
some spectral differences between these two aggregates. For
the AXT J aggregate the 1/2 intensity ratio equals 1.72, as well
as the 1217 cm–1 RROA band, assigned to the C–C stretching
combined with the ring methylene twist vibration,[31–33] is
significantly weaker compared with this band (at 1211 cm–1) in
the βC/AXT model spectrum. Neither the RROA profile exhibits
the HOOP band (4), which implies the distortion of the polyene
chain. Its absence may be connected with the lower deformation
of the carotenoid chain in the ‘looser’ J aggregate, which
consists of several layers of monomers, twisted with respect to
those above and below.[2,36,39]
To confirm ultimately the presence of βC inside the
supramolecular structures of mixed aggregates, we considered
another βC/AXT model, formed using synthesized de novo
11,11’-d2-β-carotene derivative (βC-d, for synthesis refer to the
Supporting Information), and keeping the same AXT sergeant
and the procedure of aggregate preparation. As a result of
deuteration, in the βC-d/AXT system we can observe (Figure 5):
1/ the opposite ECD profile that corresponds to the opposite
chirality and the twisting direction (handedness) of
supramolecular structure; 2/ the RROA/Raman frequency shifts
of 1 (1519  1514 cm–1) and 2 (1159  1162 cm–1) bands; 3/
the presence of the HOOP band at 970 cm-1 in the RROA
spectrum (Figure 5C).
Figure 4. Comparison of the βC/AXT model (green) and the AXT J aggregate (blue). The UV-Vis spectra of both systems are red shifted. The ECD spectra
show strong optical activity, however different profiles confirm the formation of different aggregates’ types. Both systems give enhanced and negative RROA
spectra, although some different features can be pointed: the position of C=C stretching band (1519, 1515 cm-1) or the integral intensity ratio of two main
bands (1519/1159 cm-1 and 1515/1161 cm-1). Raman spectra of both systems, as well as monomer (black) are also presented. * represents Raman acetone
bands.
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Being structurally sensitive, the HOOP band[37,38] can be
considered as evidence of the presence of deuterated (more
bent) βC molecules in the supramolecular mixed arrangement,
which gives a chiral response. Moreover, an increase of the
HOOP band intensity can also be seen in the Raman spectra of
the βC monomer and its aggregate before, as well as after
deuteration (Supporting Information, Figure S5). However,
based on the vibrational analysis of 11,12-dideuterio retinal,[40] it
can be seen that the HOOP band is enhanced for deuterated
derivatives, which confirms a substantial deuterium-induced
change in the molecular structure of βC-d compared with βC.
Strikingly, this change is reflected not only in the βC-d Raman
spectrum, but also in the ROA spectrum of βC-d/AXT aggregate.
Independently of its origin, the band at 970 cm–1 can be treated
as an internal marker of βC-d, and therefore, its presence in the
ROA βC-d/AXT spectrum confirms that βC-d becomes optically
active in the mixed system.
model equals 0.97. Finally, the presence of the RROA
combination band at 2487 cm–1 originating from the fundamental
of vibrations located at 1514 and 970 cm–1.
Observation of a strong chiroptical signal from carotenoid
microcrystals extracted from the cells of carrot roots and built
mostly (95%) from achiral βC fits into the bigger picture of
amplification of chirality in carotenoid supramolecular
assemblies. Because of the unique capabilities of the AIRROA
we were able to demonstrate in several model systems that
chiral amplification in a sergeant-and-soldier fashion is a
universal phenomenon occurring for various carotenoid pairs of
sergeants and soldiers. Above all, the study demonstrates that
carrot microcrystals in carrot cells gain chirality in a purely
physicochemical process of chiral amplification occurring most
likely due to the proximity of sergeants and soldiers (in this case
αC and βC, respectively) in crystalline chromoplasts. This work
shows the potential of chiroptical methods in studying natural
biological systems of amplified chirality that brings hope for a
better understanding of the origin of chirality in biological
macromolecules.
On the other hand, the RROA spectrum of the βC-d/AXT
model reveals three other spectral features, which are shared
with the former systems. First, the value of the RROA ratio
between 1/2 is 1.32. Second, the integral intensity ratio
between RROA bands at 1214 and 1195 cm–1 of the βC-d/AXT
Figure 5. Comparison of the βC-d/AXT model (violet solid line) and the βC/AXT aggregate (dotted green line) in order to show the effect of deuteration. The
ECD spectra of both systems have similar, but opposite profiles. The UV-Vis spectra of both models are red shifted, what confirms the aggregation process.
Subsequently, both aggregates give the enhanced and opposite RROA spectra. Main changes due to deuteration: the frequency shift of main bands (1519
→ 1514 cm-1, 1159 → 1162 cm-1), the presence of the HOOP RROA band at 970 cm-1 (insert C) and the combination band at 2487 cm-1 (insert A). Raman
spectra of both systems, as well as monomer (black) are also presented. * represents Raman acetone bands.
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Acknowledgements
This work was supported by National Science Centre (grant no.
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Keywords: carotenoid microcrystals • chirality induction •
resonance Raman Optical Activity • supramolecular chirality •
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10.1002/anie.201901441
Angewandte Chemie International Edition
COMMUNICATION
COMMUNICATION
Into the chirality induction: Natural
microcrystals and model aggregates
are consist mainly of achiral β-
carotene accompanied by a small
contribution of chiral carotenoids.
According to the sergeant-and-
soldiers effect, a small number of
chiral units imposes a large number of
achiral ones leadning to the
amplification of a chiral signal, which
can be observed by means Electronic
Monika Dudek, Ewa Machalska, Tomasz
Oleszkiewicz, Ewa Grzebelus, Rafal
Baranski, Piotr Szcześniak, Jacek
Mlynarski, Grzegorz Zajac, Agnieszka
Kaczor* and Malgorzata Baranska*
1 – 5
Chiral Amplification in Nature: Cell-
extracted Chiral Carotenoid
Microcrystals Studied via RROA of
Model Systems
Circular
Dichroism
(ECD)
and
resonance Raman Optical Activity
(RROA).
.
This article is protected by copyright. All rights reserved.