Cooperative Self-Assembly of Helical Exciton-Coupled Biosurfactant

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Cooperative self-assembly of helical exciton-coupled biosurfactant-functionalized porphyrin chromophores Kyle C Peters, Shekar Mekala, Richard A Gross, and Kenneth Singer ACS Appl. Bio Mater., Just Accepted Manuscript • DOI: 10.1021/acsabm.9b00086 • Publication Date (Web): 28 Feb 2019 Downloaded from http://pubs.acs.org on March 5, 2019

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ACS Applied Bio Materials

Cooperative self-assembly of helical exciton-coupled biosurfactant-functionalized porphyrin chromophores

Kyle C. Peters, *† Shekar Mekala, ‡ Richard A. Gross,‡ and Kenneth D. Singer*†

†

Department of Physics, Case Western Reserve University, Cleveland, OH, United States.

‡

Center for Biotechnology and Interdisciplinary Studies (CBIS) and New York State Center for Polymer Synthesis,

Rensselaer Polytechnic Institute, Troy, NY, United States.

*Corresponding authors: [email protected], [email protected]

KEYWORDS: cooperative self-assembly, supramolecular polymerization, sophorolipid, porphyrin, carbohydrate hydrogen-bonding

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ABSTRACT Bio-based, self-organizing molecules are of considerable interest as functional materials due to their structural versatility, sophisticated nano-architectures, and sustainable biosynthesis. Here, we study the self-assembly of a systematic series of bioconjugate sophorolipid-functionalized zinc porphyrin complexes with potential applications in optoelectronic devices. Our results provide insight into the molecular features that control the polymerization pathway, in particular the influence of carbohydrate chirality and non-covalent hydrogen-bonding on biosurfactantdriven self-organization of sophisticated light-absorbing supramolecular polymers. The selfassembly process is driven by a combination of hydrogen-bond, steric, and π-π interactions. Compounds under investigation were synthesized to examine the influence of peripheral chiral carbohydrate hydrogen bonding on chromophore aggregation and physicochemical properties through selective acetylation of the sophorose moiety. In dilute methanol/water solution, we found that excitonically-coupled helical structures form by strong carbohydrate hydrogenbonding interactions, in contrast to weakly coupled J-type aggregate formation with acetyl-group substitution of sugar hydroxyl moieties. Temperature-dependent UV/vis absorption and circular dichroism revealed that supramolecular polymerization proceeds through a cooperative mechanism of self-assembly for compounds bearing free OH groups capable of forming hydrogen-bond interactions. In contrast, per-acetylation of the sophorolipid’s sugar group leads to micellar aggregation that is governed by a sterically-driven isodesmic (non-cooperative) assembly mechanism.


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INTODUCTION Molecular self-assembly provides an attractive approach to construct nano-architectures for highperformance functional materials by exploiting the self-organizing abilities of Nature.1 Bioinspired assembly of molecules are of considerable interest as technological materials due to their functionality that facilitates structural modifications, introduction of sophisticated structures that bring chirality and the potential use of natural structures derived from sustainable biocatalysts.2 Research has focused on two main aspects, 1) fabrication of sophisticated selfassembled nano-structures from bottom-up methodologies for multi-functional material applications,3 and 2) molecular design schemes to better understand the biological mechanisms that facilitate self-assembly of these sophisticated nano-arrangements.4 These two aspects involve the interplay of non-covalent interactions that facilitate selfassembly through hydrogen-bonding, π-π stacking, metal-ligand coordination, dipole-dipole, van der Walls, and hydrophobic interactions.5 However, controlling this delicate interplay of assembly mechanisms is not straightforward nor well understood. Looking towards Nature for insight we see many vital, and extremely precise biological systems that are governed by this balance between non-covalent interactions.6 Self-assembled structures are often a result of these intermolecular interactions and lead to the formation of complex supramolecular systems7 and vesicles,8 DNA-structured systems 9,10 and helically-organized electronic materials.11 Therein lies the challenge – understanding Nature’s particular processes, and further harnessing and exploiting these abilities for modern nano-technological advances.12 Among potential bio-functional candidates, photosynthetic pigments show promise for multi-functional materials due to their efficient charge transfer properties and highly tunable chemical structures.13,14 As natural-occurring organic chromophores, porphyrins play the role of energy-harvesting antennae in photosynthetic and electron transport systems.15 3 ACS Paragon Plus Environment

Structurally


appealing for functional material applications,16 porphyrins are a group of hetero-aromatic macrocyclic compounds composed of highly conjugated pyrrole subunits that facilitate efficient electron transfer and allow for intense photo-absorption in the visible region.17,18 Due to their attractive light-harvesting capabilities and ease of chemical modification, these chromophores have been the focus of extensive study for light-harvesting photovoltaic systems,19–22 nanosensors23 and material science applications24 including nonlinear optics25 and potential biomedical applications,26 among others. However, understanding these chromophore-based systems and their molecular assembly and interactions are important to advance our ability to construct advanced functional electronic devices and biomimetic light-harvesting nanostructures.27–29 A number of synthetically modified porphyrin schemes have been specifically functionalized with peripheral-motifs designed to exploit particular intermolecular self-organizing characteristics for bottom-up construction of functional materials30 and artificial photosynthetic systems.31 Of particular focus in the advancement of supramolecular chemistry, carbohydrates (sugars) have gained interest as building blocks to produce structurally stable, complex nanoarchitectures through non-covalent hydrogen-bonding interactions whilst introducing chirality.32 Considering these promising attributes to facilitate complex self-assembled systems, there is relatively little research reporting physicochemical properties of porphyrin-carbohydrate conjugates,33–36 and, to the best of our knowledge, no report of porphyrin-surfactant conjugates. This work introduces the molecular design of porphyrin-microbial derived biosurfactant conjugates. Some microbial surfactants are well known for their ability to self-assembly into hierarchically ordered structures through control of non-covalent interactions with precise amphiphilic self-balance.37 Among notable biosurfactants, a distinct class of glycolipids, known as sophorolipids (SL), have gained considerable attention due to their large-scale environmental-friendly production,38 ease of


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structural modification39 and intriguing amphiphilic self-assembly properties.40–47 In addition, their biodegradability and sustainable production has been an attractive feature leading to their incorporation in consumer products such as dish washing detergents, cosmetics, and pharmaceuticals.48 SLs consist of a unique disaccharide (sophorose, 2-glucose units linked β-1-2) that is β-glycosidically linked to a sub-terminal hydroxylated fatty acid. Important to this work, SLs are amenable to selective chemical acylation (e.g. acetylation) at sophorose 6′- and/or 6′′positions49,50 and at lipid moieties (e.g. metathesis, hydrogenation).51 The sugar moiety possesses several inherent chiral centers and contains seven OH sites that are able to participate in intermolecular hydrogen-bonding or easily substituted chemically. Herein, we investigate the delicate interplay among non-covalent self-organizing interactions of SL-conjugated zinc porphyrins by precisely controlling the hydrogen bonding interaction via acetylation of the peripheral sophorose OH groups. In our previous work,52 we reported the synthesis of novel, bioconjugated SL-(Zn)porphyrin compounds prepared through an efficient chemo-enzymatic route. A library of compounds was designed to exploit hydrogenbonding group availability, the number of SL-arms conjugated to the porphyrin core and hydrocarbon chain rigidity through double bond saturation. These molecular designs feature an interplay among self-assembly interactions where steric, π-π, and carbohydrate hydrogenbonding interactions compete in multi-chromophoric aggregation. Preliminary solution-based UV/vis absorption studies in different organic solvents (chloroform, toluene, 1,4-dioxane, dimethyl sulfoxide, methanol, etc.) and solvent:water mixtures were previously explored, including water-content-dependent measurements in methanol (MeOH) for 0%, 25%, 50%, 75% and 90% MeOH:water ratios.52 Our results revealed that at a particular 1:1 volume ratio of MeOH:water—the reason for which is still under study, di-conjugate SL-porphyrin compounds



(two SL-arms conjugated to the porphyrin core) with SL-arms bearing hydrogen-bond groups (Figure 1, compound 1C) exhibited a diminished optical density and a prominent bathochromically-split Soret region with the emergence of a narrowed, red-shifted band. Diconjugated SL-porphyrin compounds with di-acetylated (at the 6′- and 6′′- positions) sophorose moieties (Figure 1, compound 1B) showed similar spectroscopic features as 1C. Additionally, di-conjugated SL-porphyrin with per-acetylated sophorose moieties (Figure 1, compound 1A) also showed a diminished optical density and red-shift, however, the broadened spectral band suggests weakly interacting molecules.53 The spectral changes for hydrogen-bonding-eligible compounds (1B and 1C) were attributed to excitonically-coupled J-type aggregation facilitated by a solvent-sensitive mixture of MeOH:water (1:1 by vol.). However, these assemblies were not fully characterized. In the present study, we expand investigations of aggregate species and broaden studies to elucidate influences of chiral sophorose hydrogen-bonding on solution-induced ordering as well as the mechanism of self-assembly. Here, we focus on the di-conjugated family of SL(Zn)porphyrin derivatives (Figure 1) and use selective acetylation as the structural variable to control the available hydrogen-bonding interactions. UV/vis absorption and circular dichroism (CD) spectroscopic studies reveal the formation of excitonically-coupled helical J-aggregates in dilute solution, which is evidenced by distinct Soret band splitting (UV/vis) accompanied with an intense CD Cotton effect (CE). Fixed wavelength temperature-dependent spectroscopic studies reveal the presence of cooperative self-assembly and comparative studies indicate that carbohydrate acetyl-group substituents play a significant role in the self-association process, suggesting that chiral carbohydrate hydrogen-bonding interactions determines the polymerization pathway and drives self-assembly.


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Figure 1. Molecular structure of di-conjugated sophorolipid-(Zn)porphyrin compounds.

RESULTS AND DISCUSSION Synthesis and molecular design. The series of compounds used in this study were synthesized as summarized in Figure 1, which includes di-conjugated SL-(Zn)porphyrin compounds where the SL arms are per-acetylated (1A), di-acetylated (1B), and non-acetylated (1C). Synthesis was performed by chemo-enzymatic modification of SLs with selective acetylation of the sophorose hydroxyl-group. SLs were conjugated to zinc porphyrin dye through a Cu (I) catalyzed azidealkyne cycloaddition (CuAC) click reaction.54,55 Full characterization of all compounds, including nuclear magnetic resonance (1H NMR, 13C NMR), and high-resolution mass spectrometry (HR-MS) were carried out to insure product quality, these results are reported in our previous work.52 This unique biosurfactant-functionalized chromophore features an intriguing geometry consisting of a central photo-absorbing hydrophobic core capable of π-π



stacking, peripheral SL-arm steric interactions accompanied by hydrophilic carbohydrate hydrogen-bonding moieties that also introduce chirality.

Water-induced aggregation. Room temperature UV/vis measurements were collected in MeOH (a good solvent, 3.0  10-6 M) for compounds 1A, 1B, 1C, and neat zinc porphyrin 1 (Figure S1). The porphyrin precursor 1 showed prominent spectroscopic peak locations at 421 nm, 553 nm, and 593 nm corresponding to the Soret and Q-band absorption region commonly observed for monomeric (non-interacting) metallo-porphyrins surrounded by solvent.18 Functionalized compounds in MeOH all exhibited identical spectral features including a common 1 nm red-shift of the Soret peak (422 nm) relative to the neat precursor 1 (Figure S1). Subsequently, UV/vis absorption measurements were recorded for all functionalized compounds in MeOH:water (1:1 by vol.) and the results revealed a significant difference between 1A and hydrogen-bond-capable 1B and 1C compounds (Figure 2a), consistent with our previous findings.52 Upon additional of water, the solution spectral response of 1A showed a diminished optical density and bathochromically-broadened lineshape indicating monomer aggregation.53 More interestingly, hydrogen-bond-capable compounds 1B and 1C exhibited a split Soret absorption band with prominent peak locations near 424 nm and 439 nm, amounting to an energy separation of about 800 cm-1. Spectral absorbance shifts can arise from intermolecular mixing of excited-state interactions, and, according to the exciton interaction theory developed by Kasha,56 a red-shifted and narrowed main absorption band is indicative of J-type, head-to-tail aggregates.57 For both 1B and 1C, the emergence of a clearly resolvable split-Soret (Davydov splitting) suggest highly-interacting J-aggregates through strong multi-chromophore excitoncoupling, as opposed to mildly-interacting J-aggregates exhibited by 1A leading to lineshape


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broadening. An extended spectral range UV/vis absorption plot (700-350 nm) is given in the Supporting Information (Figure S2). Additional photoluminescence measurements in MeOH and MeOH:water were collected for 1A and 1C, which further confirms the presence of porphyrin-porphyrin J-type aggregates (see Supporting Information Figure S3).

Figure 2. Soret region a) UV/vis and b) CD of SL-porphyrin compounds 1A, 1B and 1C in MeOH:water (1:1 by vol.) at room temperature and fixed molar concentration (3.0  10-6 M) compared to monomeric precursor 1 in MeOH, as indicated. Insert displays color change upon addition of water.

Self-organization. To further our investigation, exciton-coupled circular dichroism (ECCD) was employed to examine the multi-chromophoric spatial arrangement of SL-porphyrin compounds within the split-Soret absorption region. The method of CD spectroscopy is a valuable technique often used to study chiral systems, in particular, chiral oriented ensembles of 9 ACS Paragon Plus Environment


achiral excitonically-coupled chromophores.58 Experimentally, CD is a measurement of the differential molar extinction of left- and right-handed circular polarized light (Δε = εL - εL) and, hence, is sensitive to chiral-oriented optically-absorbing entities. When two (or more) adjacent porphyrins form a chiral system, their degenerate (or quasidegenerate) electric transition dipole moments (Bx and By) interact spatially causing the energy level of the excited state to split. As a result, two Cotton effects (CE) with opposite polarity are observed in the CD spectrum (bisignate couplet) for which the sign sequence is determined by the absolute sense of twist between the two interacting transition moments. If the chirality of the transition moments is clockwise, then the CD displays a positive couplet, that is, positive-first/negative-second (+/-) bisignate CE when viewed from longer to shorter wavelengths. On the other hand, a -/+ signature classifies counterclockwise chirality (negative couplet). The corresponding CD spectra for both 1B and 1C (Figure 2b) display intense split CD features providing direct evidence of excitonic coupling between porphyrin chromophores. Comparatively, fully acetylated 1A (Figure 2b) is CD-silent indicating the absence of excitonic coupling. The CD spectrum of 1C exhibits a strong trisignate signal (-/+/-) with two large CEs at 447 nm (-) and 433 nm (+) accompanied with a smaller CE at 424 nm (-). Compound 1B showed a similar, but less intense trisignate signal (-/+/-) with CEs located at 439 nm (-), 435 nm (+) and 423 nm (-). Both compounds 1B and 1C displayed zero crossings located near 428 nm and 440 nm. The appearance of multisignate CD bands have previously been attributed to strong π-π stacking interactions between two porphyrins within close proximity and is characteristic of a two-dimensional oscillator where the mutually orthogonal components of the electric transition dipole moments (Bx and By) contribute significantly,59 reflecting 2-dimensional coupling. In


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recent literature, similar trisignate CD bands have been associated with super-helical arrays of porphyrin-based systems with multi-chromophoric interactions.60–62 The CEs observed for 1B and 1C are an indication of multi-chromophoric coupling among Soret band transitions, suggesting left-handed helical aggregation in MeOH:water is enabled by hydrogen-bonding between appropriately conformed disaccharide units, thus engaging the carbohydrate stereogenic influence on the aggregated entity. Additionally, it is well-known that the intensity of split CEs is inversely proportional to squared interchromophoric distance, and the results here suggest that the added OH groups and corresponding hydrogen bonds provide structural stability that facilitates ample π-π stacking. In contrast, the structural design of 1A forbids hydrogen-bonding interactions through hydroxyl acetylation, disengaging the carbohydrate chiral influence during aggregation and consequently a CD-silent response. To elucidate the presence of hydrogen-bonding in 1B and 1C and the possible amide linker contributions to the self-assembling aggregates, Fourier-transform IR (FTIR) spectroscopy was employed. The attenuated total reflectance (ATR) FTIR spectrum for 1A, 1B, and 1C in the assembled solid state was recorded, full spectra are displayed in Figure 3 and selected peak center data of the spectra is given in the Supporting Information (Table S1). 1A 1B 1C

Normalized Reflectance [-]

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


4000

1744 cm-1

3500

3000

2500

2000

1500

1000

Wavenumber [cm-1]


500


Figure 3: Normalized ATR spectra of 1A (bottom), 1B (middle), and 1C (top) in the selfassembled powder form. Spectra was normalized to the peak near 2950 cm-1 and shifted vertically for clarity.

It is well established that, within the O-H stretching region (3200–3550 cm-1), larger band intensity and lower wavenumber shifts indicate increases in the degree and strength of hydrogen-bonding, respectively.63 Observations of Figure 3 show sizable spectral broadening and noticeable intensity increase at around 3320 cm-1 for 1B and 1C relative to the band of 1A with a peak near 3380 cm-1. This demonstrates that extensive hydrogen bonding is occurring for 1C and 1B, but not 1A. This is consistent with that 1A is peracetylated which eliminates O-H hydrogen bonding. The relative intensity of amide I and amide II bands as well as details in band shoulders for 1A, 1B and 1C show no apparent changes. Therefore, it’s likely that amide bond confirmations of these compounds are highly ordered. In addition, the presence of acetyl group (C=O) esters is confirmed by the observed absorption band near 1744 cm-1 for 1A and 1B, but not 1C that is non-acetylated. A further look into the physical structure of the macromolecular species was carried out by electron microscopy (EM) with solution-casted samples. Scanning electron microscope (SEM) images of 1A and 1C were taken from a 45˚ tilt angle to bring to light the 3D nature of the aggregates (Figure 4). Images of 1A (Figure 4a) show collections of sub-micron spheres that gather together to form a larger secondary network of spheres. SEM images of 1C (Figure 4b) reveal flat, circular structures with relatively uniform size, ranging from 3-4 µm, that are displaced from each other in the x-y plane. Furthermore, it seems that each circular structure is composed of several disk-like structures that are axially stacked out-of-the-substrate plane (z-


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direction). Illustration of the mesoscopic structures is highlighted in Figure 4 and lower magnification EM images are provided in the Supporting Information (Figure S4). Transmission electron microscopy (TEM) images were recorded for solution-cast samples to further examine aggregate species (Figure 4). TEM images of 1A (Figure 4c) show spherical aggregates, much like the SEM, and higher magnification images reveal a high-density core based on the darkened central region. TEM images of 1C (Figure 4d) show elongated oblong aggregates that exhibit a denser central core. Higher magnification reveals that the 1C aggregates are composed of elongated fibrillar structures that are stacked laterally in a hierarchical fashion.

Figure 4. Electron microscopy images. SEM images of a) 1A and b) 1C taken from a 45˚ tilt angle, and TEM images taken of c) 1A and d) 1C.

Self-assembly. The concentration-dependent absorption was investigated in the range 1.2 - 20  10-6 M for compound 1B in MeOH:water (1:1 by vol.) at room temperature (Figure S5). Upon dilution, the low energy exciton band located at 439 nm subsides and the high energy band at 424 nm increases, indicating the portion of aggregated species depends on the total concentration. Inspection of the area-normalized Soret region reveals the emergence of a clear 13 ACS Paragon Plus Environment


isosbestic point at 432 nm indicating a reversible, linear process between the monomers and aggregate species.64 These results suggest the aggregation proceeds through a 1D polymerization route, inspiring more sensitive temperature-dependent measurements to further characterize the self-assembly. Temperature-interval spectral measurements were carried out in dilute MeOH:water solution to examine the temperature-dependent aggregation of functionalized compounds (Figure 5). When a 3.0  10-6 M solution is heated above 55 ˚C, the Soret region for compounds 1B and 1C form a single absorption band with peak location at 424 nm; a 2 nm red-shift from their monomeric peak at 422 nm in MeOH (Figure S1). At elevated temperatures, the CD spectrum of all three compounds display a CD-silent response signifying the absence of exciton coupling and suggesting a molecularly dissolved state. For 1A (Figure 5a), the UV/vis low-energy shoulder near 435 nm remained present at elevated temperatures signifying a partially aggregated state. Exploration of higher temperatures that approach the boiling point (~70 ˚C) was not performed. Upon cooling from the fully solvated state, a temperature-sensitive split Soret and temperature-insensitive isosbestic point is once again observed for 1B and 1C indicating the presence of excitonic coupling and thermal equilibrium, respectively.65 Correspondingly, the CD spectra displays a bisignate CE growth within both UV/vis Soret bands with zero crossings as previously observed. Comparing the spectral scans of 1B and 1C in Figure 5, at low temperature the UV/vis absorption peak near 439 nm for 1C is noticeably larger, and the corresponding CD amplitude is over twice that of 1B. This higher degree of optical activity observed for 1C indicates a larger rotational strength, or rather higher probability of a CD transition, which may be attributed to the stronger hydrogen-bonding interactions leading to conformational differences between 1B and 1C.58


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Notably, the temperature-dependent (Figure 5) and concentration-dependent (Figure S5) spectra yield the same absorbance invariant isosbestic point located at 432 nm, implying both experimental methods result in analogous assembly processes.66

Figure 5. Temperature-interval UV/vis absorption (top row) and CD (bottom row) spectral scans of compounds 1A (a, d), 1B (b, e), and 1C (c, f) cooled slowly from 55 ˚C at fixed concentration 3.0  10-6 M).

Mechanism of self-assembly. To gain insight into the self-assembly mechanism, analytical methods were employed by monitoring the temperature-sensitive excitonic-band evolution.67 At fixed wavelength, the UV/vis and CD spectral change is collected and normalized (unity) to represent the temperature-dependent fraction of aggregated molecules, n(T), referred as cooling curves. Upon slow cooling from the monomeric state, curve profiles are used to distinguish between an isodesmic and cooperative (nucleation-elongation) self-assembly process.66 Comparatively, the nucleation-elongation process exhibits a rapid increase in assembly that is realized by a 2-step, non-sigmoidal profile. In accordance, two dimensionless equilibrium 15 ACS Paragon Plus Environment


constants contribute to the total associative assembly process. The first nucleation step consists of activation development governed by the equilibrium constant Ka, where monomers initially form a pre-aggregate, which eventually associate into nucleated aggregates composed of tens to hundreds of pre-aggregate entities. In the subsequent elongation step, these polymerizationeligible nuclei associate into elongated stacks, creating polymer-like structures. This process is governed by the stack size-dependent elongation equilibrium constant, Ke. To identify the selfassembly mechanism of compounds 1A, 1B and 1C, the temperature-dependent UV/vis absorption and CD were monitored near the exciton absorption band at fixed wavelength and concentration (3.0  10-6 M). For compounds 1B and 1C, the low-energy side of the exciton band at λprobe = 442 nm, was selected to monitor UV/vis absorption and CD while ensuring adequate signal intensities. Since 1A is CD-silent (Figure 5d), the monitoring wavelength was chosen on the low-energy shoulder of the UV/vis absorption at λprobe = 439 nm. Cooling curves displaying the fraction of aggregated molecules was plotted as a function of temperature (Figure 6) by normalizing the acquired spectroscopic signal (Figure S6, and S7) between 0 and 1 (see Supporting Information).


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Figure 6. Cooling curves for compounds 1A, 1B, and 1C monitored by a) UV/vis and b) CD at fixed wavelength 439 nm for 1A, and 442 nm for 1B and 1C. The solid lines represent fits to either the isodesmic or cooperative self-assembly models.

The cooling curve profile of both 1B and 1C (Figure 6) clearly exhibit non-sigmoidal behavior evidenced by a sharp transition at a specific temperature, implying a cooperative selfassembly process that cannot be modeled by isodesmic assembly. In contrast, the UV/vis curve profile of 1A follows a smooth trend representative of isodesmic (non-cooperative) assembly. To analyze the cooperative assembly behavior, the nucleation-elongation model for 1D supramolecular polymer growth was adapted.67,68 In this simplified model,69 two distinct regimes are adjoined by an elongation onset temperature (Te) and, together, represent the temperature-dependent normalized fraction of aggregated molecules n(T). Accordingly, the model in the elongation regime (T < Te) is described as; 17 ACS Paragon Plus Environment


ℎ

𝜙𝑛 (𝑇) = 𝜙𝑠𝑎𝑡 (1 − exp [− 𝑅𝑇𝑒2 (𝑇 − 𝑇𝑒 )]) ,

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(1)

𝑒

where T is the absolute temperature, he is the molecular enthalpy of elongation due to non-covalent interactions, sat is a normalization constant representing the measured saturation value, and 𝑅 is the gas constant. Within the nucleation regime (T > Te) the model takes the form; 1/3

𝜙𝑛 (𝑇) = 𝜙𝑠𝑎𝑡 𝐾𝑎 𝑒𝑥𝑝 [(

2

ℎ

1/3

3𝐾𝑎

− 1) 𝑅𝑇𝑒2 (𝑇 − 𝑇𝑒 )] ,

(2)

𝑒

where Ka is the dimensionless activation constant. Fits of Equation 1 and 2 to the experimental data were in good agreement, further supporting a cooperative mechanism of self-assembly for 1B and 1C (Figure 6). From the fits, the mean aggregation number averaged over all nucleated species at the elongation temperature was calculated; Nn(Te) = Ka-1/3. This quantity represents an estimate of the number of molecules that collectively compose the nucleated aggregate, which acts as the building blocks for polymerization. To model the sigmoidal UV/vis curve profile of 1A, the isodesmic model (iso) was adapted;66,68 𝜙 (𝑖𝑠𝑜) (𝑇) =

1 Δ𝐻 (𝑇−𝑇𝑚 )] 𝑅𝑇2 𝑚

1+𝑒𝑥𝑝[−0.908

,

(3)

where ∆H is the molar enthalpy release due to non-covalent interactions, Tm is the melting temperature that represents the crossover temperature from the monomer-dominated to the aggregate-dominated regime, defined as (iso)(Tm) = 0.5. Table 1 lists values corresponding to all relevant thermodynamic fitting parameters that characterize both isodesmic (Table 1a) and cooperative (Table 1b) self-assembly.

Table 1. Thermodynamic fitting parameters for a) isodesmic and b) cooperative model. Table 1a: Isodesmic model Compound

Method

Tm [K]

ΔH [kJ mol-1]


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1A

UV/vis

303

-107  2

Table 1b: Cooperative model Compound 1B 1C

Method

sat [-]

Te [K]

he [kJ mol-1]

Ka [-]

UV/vis

1.01

307

-127  1

8.89  1.46  10-5

22  1

306

-50.0  1

7.22  0.54  10

-6

52  1 27  1 129  6

CD

1.19

Nn(Te) [-]

UV/vis

1.00

311

-140  1

4.80  0.50  10

-5

CD

1.33

310

-30.0  1

4.58  0.68  10

-7

The fit of Equation 3 to the normalized UV/vis of 1A are in good agreement, yielding a melting temperature of Tm = 303 K and enthalpy of ΔH = -107 ± 2 kJ mol-1 (Table 1a). Upon review of the cooperative thermodynamic fitting parameters for 1B and 1C (Table 1b), an unexpected discrepancy between the UV/vis and CD values is evident, which will be addressed in the subsequent discussion. By first considering the UV/vis it is possible to compare the aggregation process between 1B and 1C. The polymerization onset temperature (Te) for 1B and 1C are 307 K and 311 K, respectively, indicating 1C aggregates at higher temperature compared to 1B. Although subtle, the 4 K difference suggests 1C forms more stable aggregates, which may be related to a greater amount of intermolecular hydrogen-bonding. Moreover, the enthalpy of non-covalent interactions at the elongation temperature (he) for 1B and 1C are -127 ± 1 kJ mol-1 and -140 ± 1 kJ mol-1, respectively. Negative values reveal the assembly process is enthalpy driven and the larger enthalpy value for 1C suggests it has a higher degree of noncovalent interactions that contribute to its assembly relative to 1B. The activation constant (Ka)—and hence Nn(Te)—is intimately related to the degree of cooperativity which, in part, governs the subsequent elongation and characterizes the degree of supramolecular polymerization.67 A small Ka value reflects a highly unfavorable nucleating aggregate, which is realized by a sharp transition from monomers to aggregates and, correspondingly, a high degree



of cooperativity. In the present case, the calculated Ka (UV/vis) value for 1C is almost 2-fold smaller than the value calculated for 1B, which is also reflected by about a 20% nucleating aggregate size (Nn(Te)) increase for 1C (27 ± 1) compared to 1B (22 ± 1) at the elongation temperature. From this data, 1C has a higher degree of cooperativity associated with the degree of aggregation as monitored by UV/vis, which suggests that the amount of free hydroxyl groups available in the sugar moiety contributes significantly to the aggregation process. As mentioned previously, there is a noticeable disagreement between the UV/vis cooling curves and fitting parameters compared to the collected CD for both 1B and 1C, in particular the inconsistent enthalpy values, which are proportional to the cooling curve slope near Te.68 However, collecting both UV/vis and CD measurements simultaneously allows for a comparison between the UV/vis and CD cooling curves, which are related to the degree of aggregation and net helicity, respectively. Moreover, it is worth noting that non-superimposable UV/vis and CD cooling curve profiles imply the aggregation development and preferential formation of one helical sense do not occur simultaneously.69 In this regard, inspection of the CD (net helicity) cooling curves for both 1B and 1C (Figure 6b) display a nearly linear temperature dependence, in contrast to an exponential trend exhibited by its respective UV/vis (degree of aggregation) curve profiles (Figure 6a) that agree nicely with the exponential temperature dependence predicted by Equation 1. A direct comparison plot for the normalized UV/vis and CD of 1B is displayed in the Supporting Information (Figure S8). Similar results were reported in the literature and attributed to a competition between monomers and the formation of left- (M) and right- (P) handed helical aggregates.70 Consequently, the presence of both left- and right-handed helical aggregates can indeed be expected to alter the observed CD cooling curve (net helicity), and hence can give rise to an almost linear CD response compared to the exponential response


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observed for the UV/vis degree of aggregation. It is also noticed that the CD cooling curves for 1B and 1C (Figure 6b) do not plateau as do the UV/vis curves at low temperatures. This observation presumably arises from the net helicity being less than 1, which also suggests the presence of both left- and right-handed helical aggregates with a preference for left-handed. Moreover, for 1C (Figure 6b) at lower temperatures a sudden increase in the CD intensity occurs which may be due to a second transition to the preferred handedness or higher order. Further inspection of Table 1b reveals the CD elongation temperature (Te) values for both 1B and 1C consistently lag its UV/vis counterpart by one-degree Kelvin. In accordance with the above discussion, this lag could be due to the existence of equal amounts of left- and righthanded helical aggregates, which would result in no net CD effect. Upon further cooling, formation from monomers to left-handed helical aggregates is slightly more favorable resulting in a net CD growth (at 442 nm) indicative of left-handed helical arrangement of excitonicallycoupled porphyrin chromophores. Further experiments are being considered to exploit this CD temperature laps to induce chiral amplification and/or accelerate the assembly process. From the cumulative results and analyses for 1B and 1C described above, we postulate that a solution-based self-assembly pathway occurs during slow cooling from the fully solvated state through growth polymerization, as animated in Figure 7. First, J-type pre-nuclei oligomers are developed and further aggregation to form ~ 20 – 30 disordered pre-nuclei. Shortly thereafter, both left- and right-handed helical nuclei are formed where the left-handed isomer is preferred. We believe aggregate ordering is facilitated by a combination of non-covalent interactions (π-π, hydrophobic, and hydrogen-bonding). Upon further cooling, the ordered aggregates continue to elongate into fibril aggregates composed of helical arrangements of excitonically-coupled porphyrin chromophores. For per-acetylated compound 1A we postulate



that the self-assembly pathway occurs by sterically-driven micelle aggregation through an isodesmic self-assembly.

Figure 7. Cartoon depiction of a possible self-assembly pathway that occurs from the molecularly dissolved (high T) to the fully assembled state (low T).

CONCLUSION In summary, self-aggregation of di-conjugated (two-armed) SL-functionalized zinc porphyrin compounds with different degrees of hydroxyl group acetylation (0, 2 at the 6′- and 6′′ positions and peracetylation (7)) of the sophorose disaccharide carbohydrate moiety were examined in solution by VU/vis and CD absorption spectroscopy. It was shown that, in dilute solutions of MeOH:water, hydrogen-bond-bearing compounds exhibit prominent J-type exciton coupling recognized by a split Soret and bisignate CD response, while fully acetylated SL-appended compounds exhibit weakly coupled J-type aggregates. Spectroscopic analysis indicates that fully acetylated SL-(Zn)porphyrin compound (1A) assemble into non-chiral oriented aggregates via an isodesmic assembly pathway, and electron microscopy images confirm micelle formation. Hydrogen-bond-bearing SL-(Zn)porphyrin compounds (1B, 1C) form helical oriented multi-


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chromophoric aggregates and further self-assembly through a cooperative (nucleationelongation) growth pathway. Additionally, an increase in hydrogen-bonding interaction sites aid in the cooperative nature of association, which may be manifested by larger polymerizationeligible nucleated aggregates upon growth for compound 1C. This research provides valuable insights into how carbohydrate chirality and variable acetylation of sophorolipid arms appended to a porphyrin core controls the self-assembly and corresponding polymerization pathway of SLporphyrin light-absorbing supramolecular structures. This work paves the way for further investigation into glycolipid-functionalized chromophore structures that can be manipulated to control self-assembly and formation of supramolecular structures that provide valuable optoelectronic materials.

EXPERIMENTAL SECTION Solution preparation. Dilute solutions used for spectroscopic studies of self-assembly for compounds 1A, 1B, and 1C were first prepared by dissolving the given compound in MeOH (a good solvent) to a concentration of 6.0  10-6 M and sonicating at room temperature for about ten minutes to ensure full solvation. With a syringe/needle, deionized water was injected into the vial, further diluting to the target concentration of MeOH:water (1:1 by vol.) at 3.0  10-6 M. Upon addition of water, the solution color turned from red-tented in MeOH to greenish-yellow in MeOH:water. Each solution was placed in a room temperature sonication bath for ten minutes to ensure adequate mixing. Vials were removed from the sonicating bath and 3 mL was placed in clean quartz cuvettes (10 mm path length) with a stir bar, capped and sealed with plastic paraffin film and tape. The final concentration was chosen such that the concentration-dependent elongation onset temperature for polymerization (Te(c)) fell within a physically accessible



temperature range to characterize the assembly process while maintaining an adequate detection signal. UV/vis and CD measurements. UV/vis absorption and circular dichroism (CD) spectral and fixed wavelength scans were collected using a JASCO 815 CD spectrophotometer equipped with a Peltier (PFD-425s) temperature controller. Variable-temperature spectral scans presented in Figure 4 of prepared compounds 1A, 1B and 1C were first heated to 55 ˚C and held at this temperature for 15 minutes to allow molecular dissolution and solution thermal equilibration. Each sample solution was cooled and spectral scans (500-350 nm) were collected every 5 ˚C. Temperature-dependent cooling curves monitored at fixed wavelength were collected with the same samples by reheating to the monomeric state and slow cooling to 5 ˚C (Figure S6, S7). A cooling rate of 1 ˚C min-1 was chosen to ensure thermal equilibrium and suppress kinetic effects while the UV/vis absorption and CD response were recorded every 0.2 ˚C at fixed wavelength of 442 nm for 1B and 1C, and 439 nm for 1A. A baseline measurement of MeOH:water (1:1 by vol.) was also recorded between the same temperature range, which was later used to baselinecorrect the data (see Supporting Information).

Fourier-transform IR measurements. A 5 mg ml-1 solution of 1A, 1B and 1C in MeOH:water (1:1 by vol.) were mixed in vials and heated on hotplate to 60 °C then cool to room temperature. 10-15 drops were placed on clean glass microscope slides, covered, allowed to dry then placed under vacuum overnight to fully evaporate the solvent. The deposited film/aggregates were scrapped off the glass substrate making a powder and infrared spectroscopic measurements were collected in powder form using an Agilent Cary 630 FTIR spectrometer operating in attenuated total reflectance (ATR) mode in the range 650–4000 cm-1.


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Photoluminescence measurements. Emission spectra was acquired for compounds 1A and 1C in MeOH and MeOH:water (3 × 10-6 M) at room temperature using a Horiba Fluorolog®3 Spectrofluorometer. The excitation wavelength was 365 nm and emission spectra were collected over the spectral range 380–850 nm. The corresponding emission spectra is shown in the Supporting Information (Figure S3).

Electron microscopy images. Electron microscopy images were taken at Swagelok Center for Surface Analysis of Materials (SCSAM) at Case Western Reserve University. Scanning electron microscopy (SEM) images were taken of compounds 1A and 1C with a FEI Helios Nanolab 650. Samples were prepared on a clean, standardized aluminum SEM holder by drop-casting from a 3.0  10-6 M solution in MeOH:water (1:1 by vol.), covered and allowed to air dried overnight at room temperature. Prior to drop-casting, the solution was heated on a hotplate set at 60 ˚C for one hour to insure a monomeric state, then allowed to slow cool to room temperature. Additional SEM images can be found in the Supporting Information, Figure S5. High-resolution analytical transmission electron microscopy (TEM) images were taken with a FEI Tecnai F30. Samples were prepared on a clean 400 mesh Cu (UC-A on Lacey) TEM grid by floating the grid atop bead of pre-made 1A and 1C solution in MeOH:water (1:1 by vol.) for 60 seconds. The grid was removed, excess solution was wicked with filter paper and allowed to dry then stained by the same procedure with uranyl acetate. Sample solution used were mixed to a 0.5 mg mL-1 concentration in MeOH:water, heated in vials to 60 ˚C and slow cooled to about 10 ˚C, for which the grid preparation took place.



ASSOCIATED CONTENT Supporting Information. Additional spectroscopic measurements including concentrationdependent UV/vis absorption, Fourier-transform IR, photoluminescence, temperature-dependent UV/vis and circular dichroism cooling curve data, baseline and normalization methods, fitting methods with plots and scanning electron microscopy images.

ACKNOWLEDGEMENTS The authors would like to thank Professor Adam Braunschweig at the CUNY Advanced Science Research Center for insightful discussions. Financial support from NSF Program for International Research and Education (PIRE), grant: OISE-1243313 is gratefully acknowledged. The authors acknowledge the use of the Materials for Opto/electronics Research and Education (MORE) Center (Ohio Third Frontier grant TECH 09-021), the Swagelok Center for Surface Analysis of Materials (SCSAM) at Case Western Reserve University for SEM and TEM imaging, and the Molecular Biotechnology Core at the Cleveland Clinic Foundation - Lerner Research Institute for use of the JASCO CD spectrophotometer.

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Cooperative Self-Assembly of Helical Exciton-Coupled Biosurfactant

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