Evaporation-induced self-assembly of liquid crystal biopolymers

Soon Mo Park ^ab and Dong Ki Yoon *^a
aDepartment of Chemistry, Korea Advanced Institute of Science and Technology (KAIST), Daejeon, 34141, Republic of Korea. E-mail: nandk@kaist.ac.kr
^bDepartment of Chemical and Biomolecular Engineering, Cornell University, Ithaca, NY 14853, USA

First published on 8th February 2024

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Wider impact Evaporation-induced self-assembly (EISA) has increasingly captured the spotlight owing to its foundational scientific principles and the vast potential it holds for application in materials science and nanotechnology. Notably, liquid crystal biopolymers have emerged as promising candidates for EISA, primarily due to their highly organized structures and the biocompatible nature they acquire post-deposition. The review at hand provides a comprehensive panorama of recent strides in EISA concerning liquid crystal biopolymers and the intrinsic mechanisms propelling self-assembly and explores the ramifications of diverse processing conditions. Looking ahead, the insights unveiled in this review are poised to play a pivotal role in steering the trajectory of materials science by informing strategic advancements and enabling tailored approaches within the burgeoning domain of evaporation-induced self-assembly.

1. Introduction

Evaporation of solutions is a natural phenomenon closely related to our life and fundamental science.^1,2 And it offers valuable insights for industrial applications, such as coating, printing, and patterning.^3–7 Thus, comprehending and effectively controlling the underlying principles of evaporation are essential. However, this proves to be challenging, given that diffusion and flow occur spontaneously during the drying and deposition processes.⁸ Moreover, a solution's characteristics continuously change, including concentration, density, viscosity, and interfacial area.⁹ To gain a comprehensive understanding of this spatiotemporal system, extensive research has been carried out on evaporation, delving into different aspects, encompassing initial concentrations,^10,11 solution components,^5,12 and boundary conditions.¹³ Beyond internal factors, manipulating external conditions, such as temperature, humidity,¹⁴ surface wettability,^10,15 and exposed interfacial area,⁷ has led to intriguing phenomena. These phenomena include the Marangoni flows,^5,12,16 stick-and-slip motion,^10,11 and various deposition patterns.⁶ Especially, in the deposition process, suspended particles exhibiting anisotropy develop condensed phases near the contact line, giving rise to unique morphologies that reflect the phase information.¹⁷

Anisotropic polymeric materials found in nature tend to undergo self-assembly once a specific concentration threshold is surpassed, displaying distinctive collective behavior owing to their unusual elasticity.^18,19 For instance, when a diluted deoxyribonucleic acid (DNA) aqueous solution is evaporated on a substrate, the DNA chains extend linearly along the moving direction of the contact line due to the receding force.^20,21 However, with an increase in the initial concentration, the DNA solution undergoes sequential transitions into chiral nematic and columnar phases during the drying process, and these structures in the phases are manifested in the resulting deposited film.²² Moreover, biopolymers exhibiting cholesteric phases, such as cellulose nanocrystals and collagen, create diverse hierarchical structures not observed in the building blocks which can form only uniaxial alignment.^23–25 While their condensed phases, featuring various structural morphologies, have been extensively studied in equilibrium systems, there are limited cases demonstrating collective behavior in dynamic systems, particularly regarding phase transition processes near the liquid–air interface. Hence, comprehensive insights can give protocols for the evaporation of various anisotropic biomaterials with inspiring related research.

Here, we present the evaporation-induced self-assembly (EISA) of representative biopolymers and colloids that reveal the liquid crystal (LC) phases (Fig. 1 and Table 1). First, we commence with an examination of the physical properties of aqueous biopolymer solutions such as hydrodynamics, rheology, and LC elasticity. This analysis explores molecular attributes such as the length scale, morphology, and surface chemistry, subsequently correlated with extensive research on lyotropic LC phases. We delineate anisotropic morphologies in the deposited film depending on the building blocks and highlight their potential for practical applications. Knowledge of evaporation holds significance not only for comprehending collective behavior within non-equilibrium systems but also for gaining fresh insights into leveraging biopolymers as fundamental building blocks in materials sciences.

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2. Driving forces in EISA of anisotropic biopolymers

2.1. Hydrodynamics and rheological properties of the aqueous solution

We will introduce a comprehensive overview of EISA processes concerning anisotropic biopolymers and colloids, along with the resultant anisotropic structures observed in the deposited films. The flow of the liquid towards the contact line, driven by a surface tension gradient at the liquid–gas interfaces, causes the suspended solutes to condense.^8,9 It leads to a phase transition near the contact line, and the distinctive morphological patterns emerge as a manifestation of the liquid crystalline structures of the solutes during the drying process. To comprehend the underlying driving forces for these structures, our focus shifts toward investigating the self-assembly process within a non-equilibrium system. This inquiry is approached through the views of hydrodynamics, rheological analysis, and LC elasticity.

When positioning the initial concentration of the aqueous biopolymer solution in proximity to the nematic phase to initiate the self-assembly of LCs during the drying process, the solution exhibits a relatively high viscosity owing to the substantial macromolecular weight of the solute. This elevated viscosity correlates with a lower Reynolds number (Re), a parameter delineating flow conditions in hydrodynamics,²⁶

where ρ is the mass density (kg m⁻³, ), v is the flow velocity (m s⁻¹, ), L is the length scale of the system (m, ) and η is the solution dynamic viscosity (Pa s, ).

This elucidates that solute transportation during evaporation is primarily governed by capillary flow, transpiring along laminar capillary streamline pathways devoid of turbulence.

The capillary flow profile of (i) the sessile droplet, as well as (ii) under the meniscus curve in the coating process, can be assessed through height averaging when the solution undergoes evaporation under conditions of partial wetting (where the contact angle θ lies between 0° and 90°, Fig. 2a and b).

2.2. Liquid crystal elasticity of anisotropic biopolymers and colloids

In the drying process, the LC phases of the anisotropic biopolymers are developed near the contact line due to the flow-induced condensation, and the morphologies are directly reflected in the deposited film. The foundational LC and molecular anisotropy model is rooted in Onsager's approach, specifically targeting monodisperse infinite hard rods.³⁴ Following the theorem, researchers have advanced this framework by introducing an extension that accommodates the finite length scales and flexibility of solutes, which is gauged by contour length (L), diameter (d), and persistence length (p).^35–39 Their study unveiled that this flexibility factor (α = l/p) contributed to the increased critical concentration and a corresponding decrease in the order parameter based on the Onsager criteria,

where ϕ is the volume fraction of the solutes, d is the diameter (m), l is the contour length of the biopolymer (m), and p is the persistence length (m).

The LC building blocks align themselves parallel to the direction of the capillary flow streamline in order to minimize rotational resistance.^40,41 Meanwhile, the solutes present in the LC phases undergo splay deformation due to the convergence of meniscus towards the solid–liquid–air triple point on the substrate (Fig. 3a). The collective behavior exhibited by liquid crystalline biopolymers throughout the drying process can be described through the integration of the Frank–Oseen elastic energy (F) coupled with condensation effects.⁴² Notably, the modified equation captures the phenomenon of solute condensation induced by capillary flow, which subsequently accelerates the elastic instability of the system beneath the meniscus curve,

where K₁, K₂ and K₃ are the elastic moduli for splay, twist and bend deformation, respectively, and ∂ρ is the variation in the local solute density, ρ⁰ is the mean solute density, and E is an elastic compressibility induced by external stress.

In this formula, the elastic constants of the liquid crystal are associated with factors such as the volume fraction and length scales.^43,44 Discrepancies persist between theoretical models and experimental measurements in the interpretation of ‘semi-flexible’ criteria (L ∼ Α*p), where Α is the constant.^36,37 Nevertheless, we choose to simplify matters by directly comparing the contour length (l) to the persistence length (p) (Fig. 3b).

(i) The elastic constants of rigid LC polymers (l < p)

(ii) The elastic constants of (semi-) flexible LC polymers (l > p)

where k_B is the Boltzmann constant, and T is the temperature (K).

By directly comparing the relaxation time of splay deformations with the duration leading to the kinetically quenched state during the drying process, it would yield the most precise insight into the formation of an anisotropic structure within the deposited film.⁴⁵ Unfortunately, due to the current lack of analytical methods for such assessments, our approach is to focus on comprehending the system through the Ericksen number (Fig. 3c).^46,47 This dimensionless number effectively characterizes the interplay between LC elasticity and capillary-induced viscous forces that emerge during evaporation. The LC elasticity could be estimated through the elastic constants of the deformations, and although the numbers are around the unity, we could discern which force slightly dominates this system depending on the coating speed,

where K is the LC elasticity (N).

Our focus has been on discerning Ericksen numbers by employing carefully chosen papers, enabling us to estimate and correlate these values with the orientation of biopolymers within deposited films (Table 2). Examples in the table about the ambient drying of biopolymer solutions reveal Ericksen numbers spanning 0.1 to 10. The numerical values exhibit higher magnitudes when the orientation of building blocks aligns parallel to the coating direction. Conversely, in instances where the material orients perpendicular to the coating direction, the numbers generally range from 0.2 to 4. Additionally, an undulated structure in the cases of bacteriophage and collagen emerges under transient conditions between parallel and perpendicular alignments.

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Our investigation affirms that the orientation of the biopolymers within the deposited film can be manipulated by the dominance of capillary flow and LC elasticity, irrespective of the atomic composition or molecular structure of the building blocks. Throughout the evaporation process, the orientation of the blocks aligns parallel to the capillary flow when viscous force dominates, whereas the dominance of elastic force results in alignment perpendicular to the flow direction (parallel to the contact line). Notably, the alignment is absent in cases of diluted concentration because it could be driven by the characteristics of collective behavior exhibited in the LC phases. Furthermore, in instances where the biopolymers form a helical structure, an undulated pattern reflective of the helicity manifests in a range in which viscous force and elasticity are balanced. Our findings elucidate the role of capillary flow and LC elasticity in governing chain orientation during the evaporation process and highlight the impact of chirality on the resultant film structure. In addition, the transient Ericksen number at cross-over velocities during the coating process suggests that theoretical estimations hold promise for interpreting biopolymer alignment in thin films.

3. Liquid crystal phases and anisotropic structure formation in EISA

3.1. Deoxyribonucleic acid (DNA)

Organisms have evolved various strategies to compress their genetic material, DNA, to the smallest possible cellular level: LC ordering,^48–53 supercoiling by entanglement,^54,55 hierarchical structure by DNA-histone interactions,^56,57etc. Indeed, LC forms, one of the strategies for molecular compaction, have been found in sperm heads, chromosomes, and viruses (Fig. 4), where the compression efficiency of LC has allowed tens of thousands of base pairs with an overall contour length of a few microns to be packed into the capsids or heads of 50–100 nm. This ingenious packing not only efficiently stores genetic information but also protects the DNA from potential harm, including irradiation, oxidative agents, and degrading enzymes, because it reduces the accessibility of DNA molecules through structural sequestration.⁵⁸ In particular, the DNA LC expression has not only served important functions in living organisms, but has also helped to analyze the structure of DNA. When measuring X-ray diffraction patterns to analyze the structure of DNA chains, the chains could be aligned without interchain entanglement, which allowed for the formation of clear X-ray diffraction patterns.^59,60

To understand the spontaneous phase transition to the ordered LC phases, numerous studies have revealed several distinct characteristics of these LCs in vitro (Fig. 5).^61–63 The emergence of the phases can be theoretically explained by modelling the chain as the repulsive rigid or semi-flexible rod-like particle. The length scales of DNA chains with diameter (d ∼ 2 nm), contour length (l ∼ 0.34 * the number of base pairs (bp)), and persistence length (p ∼ 50 m)⁶⁴ satisfied the condition for LC ordering as stated by the Onsager criteria (Fig. 5a). The critical volume fraction (φ_I–N) marking the transition from the isotropic to nematic phase was found to be influenced by the number of base pairs below the persistence length.⁶⁵ In practical terms, this implies that exceeding 147 bp in a single DNA chain does not significantly vary the volume fraction compared to cases below 147. Depending on the concentration, different phases were identified, including nematic, cholesteric, and columnar, through polarizing optical and electron microscopy to obtain structural information based on the molecular structure (Fig. 5b–d).^61–63,65 Moreover, given the polyelectrolyte nature of DNA, its distinct traits were influenced by surrounding ionic contents that change the persistence length and the effective diameter of the DNA molecule.^66,67 Significant insights have emerged by investigating the rigid DNA fragments within differing ionic environments, such as interparticle spacing and phase boundary transition in the LC phases.^65,68 This behavior becomes more evident in various additives such as polyvalent cations (including polyamines), polymers, and organic solvents.⁶⁹ Those investigations also help to estimate the collective behavior of DNA in cholesteric and hexagonal columnar phases and semiflexible DNA chains with long contour lengths (L/P > 1). The flexibility does not fundamentally change the intrinsic properties of the LC phases (including the nematic and columnar hexagonal arrays), but it does affect the defect composition and rheological properties of the solution.

Based on the collective behavior of DNA LC in stable (metastable) states, people have tried to understand the interplay between their self-assembling behavior and evaporation-induced condensation. As mentioned in the introduction, the DNA chains were just stretched by the receding force of the contact line and deposited on the substrate in the drying process of the diluted DNA solution (Fig. 6a and b).^20,21,70 However, the evaporation of the concentrated solution is quite different from the diluted case because the initial concentration is high enough to induce the LC phase transition, in which the chains show collective behavior before thoroughly dehydrating.

Indeed, Morii et al. discovered, for the first time to my knowledge, the annular alignment of salmon sperm DNA chains in a drop-casting process (Fig. 6c).²² They analyzed the DNA alignment in the deposited film as a function of the distance from the center of the circular film. They found different structures depending on the initial concentration and temperature, one of which is orthogonal, with most molecular alignments being concentric but a small region near the center of the droplet being radially aligned. Based on the real-time observation, they proposed a possible mechanism for the chain orientation driven by a transitive balance of physical effects between the hydrodynamic forces and the Brownian motion of the chain segments. They found that an appropriate concentration to ensure mass diffusion and phase transition is essential and that highly dilute DNA solutions are unsuitable for forming oriented membranes.

Aligning to the above, Smalyukh et al. found a periodic zigzag structure in a ring-shaped deposit from DNA dry droplets (Fig. 6d).⁴² In this study, Lambda-DNA, with 48502 bp, shows a lyotropic liquid crystal around the contact line and aligns parallel to the boundary to minimize elastic energy. However, upon depinning, the radial dilative stress induces undulations at the rim, propagating inward through the columnar liquid crystal. They describe the structure formation through a model based on Frank–Oseen elastic energy with experimental results. The chain flexibility (l/p > 300) higher than the precedents might affect the formation of the micron-scale structure under the contact line receding force, not aligned parallel to the contact line.

Inspired by the pioneering works above, we have developed to fabricate periodic DNA microstructures in a long-range order (Fig. 7).^71–74 The brushing method allows reproducing the phenomenon by grooving the solution interface, which induces competitive interaction between compressive stress and DNA liquid crystal elasticity (Fig. 7a).⁷¹ The line defects were induced by buckling instability of the columnar liquid crystal, and systematically studied the dimensional tunability along the width and depth of the micro-sized template. A solution coating process has been introduced to induce from uniaxial alignment to orthogonal orientation by controlling the moving velocity of the coating plate.⁷² The combination with topographic templates could give a spatial confinement effect to the liquid crystal and deform the interfacial curvature of the solution (Fig. 7b and c).^73,74 The structural anisotropy can then be transferred, internally and externally, e.g., to an alignment layer, facilitating the alignment of nanomaterials on a surface or to a directional matrix, enabling their orientation within a mixture.

3.2. Nanocellulose

Cellulose, the most abundant biopolymer on our planet, is present in plants, marine environments, and products of bacteria.^75,76 The fibres of cellulose can be broken into controllable nanoscale building blocks called cellulose nanocrystals (CNCs) (Fig. 8a). These cellulose components, originating from renewable materials, possess not only eco-friendly benefits but also distinctive practical interest due to their various functional properties such as mechanical strength, optical and thermal properties.^77–80

It is well-known that CNCs have the ability to self-assemble into a helical structure, which is referred to as chiral nematic or cholesteric phases (Fig. 8b) based on the twisting morphology of a single nanocrystal (Fig. 8c and d).^75,76,81,82 Such a hierarchical structure in the CNC matrix contributes to an iridescent color based on the periodicity of the refractive index (Bragg reflection), and researchers have tried to tune the pitch and tactoid formation to enhance their chiral optical activities.^83–86 Although much progress has been made with much effort, in this section, we will only discuss the unwind nematic order of CNCs induced by hydrodynamic flow and refer interested readers to the above available literature describing these cholesteric systems.

When drying sessile CNC dispersion droplets on the flat substrate, in-plane multiaxial alignment was found in the deposited film where the local director of CNCs is uniaxially aligned (Fig. 9a).⁸⁷ Pritchard et al. monitored the drying process in real-time through polarized optical microscopy (POM) and analyzed the drying dynamics using computational fluid dynamics. They utilized the Peclet number, a parameter comparing solute Brownian motion to capillary flow, to validate the dominant factor behind the sequential alignment of CNCs. They found that contact line behavior dominates the orthogonal alignment of CNCs in the deposition and studied various morphologies changing the initial concentration, surface wettability, and droplet volume. Also, there is another suggestion for the CNC alignment based on surface tension gradient-induced torque near the substrate–liquid–air interfaces.⁸⁸ The torque due to the surface tension getting higher close to the contact line rotates the CNCs perpendicular to the direction of the receding lines and parallels them to the solution boundary layer that matches with the behavior of splay relaxation.

To induce uniform alignment in the circular deposited film, researchers controlled the experimental systems via (i) the introduction of additives ref. 88–91 and (ii) surface modification using chemical treatment (acid hydrolysis) (Fig. 9b and c).^92,93

3.3. Protein amyloid

Amyloid fibrils are anisotropic colloids formed by self-assembly of peptide β-sheet aggregates into twisted and helical ribbons,^94,95 which have been intensely investigated in biology and medicine due to their relationship with pathological conditions such as age-related dementia (Fig. 10a).^96–98 The fibrillated proteins based on the amyloid core structure have recently been discovered at the origin of biological functionality in a remarkably diverse set of roles based on the unique properties and rich chemistry of peptides.^99,100

The rod-like shape with the one-sided handedness induces isotropic to liquid crystal phase transition that can be well described by the Onsager theory extended to the charged and semiflexible polymers, where modifying the system makes rich behavior in the concentrated solution (Fig. 10b).^26,101–103 In particular, Mezzenga et al. discovered the formation of tactoids along a concentration gradient, such as homogeneous, bipolar, and cholesteric ones, and analyzed the order and orientation transition in a confinement effect and hydrodynamic system with a support of theoretical estimation.^104–107

For example, Almohammadi et al. investigated the liquid–liquid crystalline phase separation of aqueous filamentous colloids (here, beta-lactoglobulin amyloid fibrils) during droplet evaporation (Fig. 11a).¹⁰⁸ They demonstrated that two phase transitions occur with increasing concentration: nucleation and growth and spinodal decomposition where they also discovered the structural changes and dynamics of the tactoids in a hydrodynamic system. The amyloid alignment in the deposited films lacked macroscopic uniformity but retained hierarchical structures such as microscopic fingerprint textures and parabolic focal conic domains. It is similar to the CNCs’ collective behavior in the drying process, including tactoid fusion close to the contact line with sliding instability or parabolic multi-domains in slow evaporation.

Our group reported, in collaboration with Mezzenga's group, the fabrication of a hierarchical structure of protein amyloids with the property of minimizing liquid crystal elastic energy in the vicinity of contact lines and a template capable of inducing stick-and-slip motion (Fig. 11b).¹⁰⁹ The filamentous protein amyloids self-assembled, while the contact line was pinned to form a macroscopic fibre structure, aligned parallel to the contact line, with micrometre-scale gaps along the edges that could be next pinned. A series of time-lapse POM images characterised the self-assembly process to elucidate the formation mechanism, and the structures' dimensions could also be controlled by adjusting the spacing of the templates.

3.4. Filamentous virus

The basic principles governing the isotropic-to-nematic phase transition in hard rods were established in the 1940s, focusing on the interplay of the aspect ratio and concentration.³⁵ In general, the properties of biopolymers are more complex than those of theoretical models, for example, due to flexibility and surface charge. However, Ff phages, a group of filamentous bacteriophage, have filled the gap with their molecular properties. For example, M13 phages have a contour length of 880 nm and a diameter of 6.6 nm, and their aspect ratio aligns with the Onsager criteria (L/D > 100) (Fig. 12a).¹¹⁰ And the phages maintain the uniform conformation of length, topography, and chemical composition, yielding remarkably consistent suspensions. The capacity for tunability via chemical and biological methods enables systematic manipulation of interaction potentials,¹¹¹ rendering these models exceptionally effective for comprehending and designing liquid crystals. Consequently, these models facilitate direct quantitative comparisons with theoretical predictions, thereby facilitating investigations into intricate LC phases.^112–117 Noteworthy is the profound influence of molecular-level chirality on the self-assembly process within concentrated solutions. Leveraging insights, such as the formation of a helicoidal structure involving approximately 2700 copies of a single peptide and a fivefold rotation axis, researchers strive to comprehensively explore the origin and behavior of chiral mesophases, including cholesteric and chiral smectic C phases (Fig. 12b and c). The intricate relationship between microscopic and macroscopic chirality, encompassing factors like handedness and pitch, remains an ongoing focus of research, crucial for achieving a comprehensive understanding of colloidal liquid crystals.

Professor Belcher and Lee are pioneering researchers who have significantly contributed to fabricating functional materials using evaporation-induced self-assembly involving viral films.¹¹⁸ Among their key findings, they have observed the formation of liquid crystal structures ranging from nematic to chiral smectic C, dependent on concentration and thickness variations.¹¹⁹ At higher initial concentrations, the mono-dispersity of the bacteriophage led to the formation of helical bundles with a smectic-based long-range order, which is directly reflected in the film as a periodic zigzag structure. The authors attributed this phenomenon to the dominant effect of expressing chiral liquid crystal structures over the interfacial effect. AFM and laser diffraction pattern results with POM supported their assertion.

Furthermore, the investigation by Lee and colleagues delved into the intricate interplay between environmental parameters and the kinetics governing the conversion of helical macromolecules into higher-ordered structures via a dip-coating process.^120,121 They explored the applicability of these factors for regulating assembly under controlled experimental conditions. Their study revealed that the formation of sub-micrometre-scale structures originated from the spontaneous transitions within liquid crystal dynamics, coupled with distinctive chiral characteristics, including nematic orthogonal twist, cholesteric helical ribbon, and smectic helicoidal nanofilament (Fig. 13). Examining at the microscale, the establishment of ordered configurations were closely tied to the geometric constraints such as curved menisci, along with the periodic modulation of material flow. By manipulating meniscus motion, they materialized the large-scale ordered film as a functional material. Moreover, by fine-tuning coating parameters within the self-assembly process, they successfully produced a diverse array of nanostructures on a large scale.¹²² This achievement was facilitated by manipulating interparticle interactions contingent upon the concentration of additive ions. Adjustments to thermodynamic parameters resulted in distinctive undulations in the transient meniscus curve, leading to a hierarchical dotted pattern. Notably, the periodic alteration of coating speed, a pivot of kinetic factor, governed the formation of periodic dots within this pattern. Building on the groundwork, our group explored collective behaviors in non-equilibrium systems.¹²³ We focused on understanding the interplay between liquid crystal phase transition near the solution contact line and the resulting M13 film morphologies. Through multiple viewpoints of microscopic analysis, we directly visualized the presence of liquid crystal three-dimensional structures in the deposited films. We also involved the rheological and hydrodynamic analysis, revealing the competition between the liquid crystal elasticity and the capillary flows in forming hierarchical structures. Our work holds significance in optimizing experimental conditions for precise ordering and orientation of chiral filamentous colloids. By delving into the dynamics of non-equilibrium systems, we contribute to understanding intricate processes in this field.

3.5. Collagen fibril

In biological tissues, collagen fibrils are found in a highly concentrated state within the organic matrix of skeletal structures (Fig. 14a).^124–126 These fibrils endow specific properties, such as mechanical resistance in bones and tendons and transparency in the cornea.^127,128 The challenges in investigating these distinct properties within our tissues are rooted not only in the inherent attributes of the fibrils themselves but also in the hierarchical structure, spanning from the nanoscale to the microstructural level.¹²⁹ This spontaneous organization of well-ordered structures in diverse collagen matrices exhibits notable analogies to the liquid crystal ordering in the concentrated collagen solutions (Fig. 14b).^54,130–133

The synthesis of collagen fibrils occurs within the cells, yielding three polypeptide chains that intertwin into an elongated,¹³⁴ semi-flexible triple helix with a diameter of 1.5 nm and a length of 300 nm. Due to the high aspect ratio, they presented lyotropic liquid crystal characteristics manifesting birefringent textures known as fingerprints above certain concentrations.^125,128,131 Early observations of these mesoscopic phases have been systematically clarified through joint endeavors by biologists and physicists aiming to quantitatively characterize collagen phase diagrams changing factors such as contour length, pH, ionic strength, solvent composition, and additives.¹³¹ This foundational understanding has paved the way to modulate the long-range organization of collagen, enabling the establishment of uniaxial fibril orientations in tendons and layered orthogonal alignment in bone and the cornea and bridging the gap between in vitro findings and living tissues.

Trials to fabricate a biomimetic structure have been initiated since the 1980s through evaporating droplets containing collagen solutions (Fig. 15).^25,135–138 The surface morphologies of the resulting films are also quite similar in nature, and the researchers have analysed several key factors, including the initial concentration of the solution, as well as the dimensions (diameter and length) of the fibrils and the rate of evaporation. For instance, Maeda conducted investigations utilizing techniques such as atomic force microscopy and polarized light microscopy (Fig. 15a).¹³⁵ This study highlighted the presence of a critical concentration threshold for nanoscale self-assembly. At concentrations below 0.005 mg mL⁻¹, collagen fibrils exhibited a random configuration on the mica substrate due to their inherent flexibility. However, as the initial concentration exceeded 0.05 mg ml⁻¹, these fibrils adopted a distinctive wavy crimp morphology characterized by periodic blue and yellow bands in polarized light microscopy. Within each band, the fibrils are uniaxially aligned and, at certain points, present interlocking and translational dislocation of these bands in the formation of concentric ring patterns.

Moreover, the diameter of the fibrils emerged as another crucial determinant of morphologies that varied based on solution pH (controlled by acetic acid) and the specific collagen types formed through natural fibrillogenesis.¹³⁷ These phenomena indirectly support the notion that the established collagen structures originated from liquid crystal-mediated self-assembly.¹³¹ The application of a solution coating technique greatly enhanced the uniformity of the aligned collagen fibril network (Fig. 15b and c).^25,138 By precisely manipulating external variables, researchers successfully achieved a structure analogous to human connective tissue. The resultant structures, driven by liquid crystals, featured diverse hierarchical levels, such as the periodicity of the twisted plywood structure, upon the specific conditions applied.

Furthermore, professor Rey's group embarked on a theoretical exploration of the chiral self-assembly mechanism inherent to collagen I within a non-equilibrium system grounded in relaxation and transport principles.^139,140 The investigation demonstrated the pivotal role played by the simultaneous integration of isotropic-cholesteric phase ordering and anisotropic solvent transport in forming the helicoidal plywood structure. By simulating a biomimetic deposition process followed by controlled drying, it will be possible to finely regulate the hierarchical dimensions of the collagen structure.

4. Potential for practical applications

The alignment of building blocks in the deposited film can impart anisotropic characteristics to other materials, influenced by the surface morphology and the excluded volume effect of additives. We will now present two illustrative applications of biopolymeric films: (i) as an alignment layer (Fig. 16) and (ii) as an anisotropic matrix (Fig. 17 and 18).

4.1. On the film: alignment layer

An alignment layer serves the purpose of inducing uniform and planar alignment of anisotropic entities such as molecules, polymer chains, inorganic rod-like particles, and even living matter near the surface. Its role is to exert control over the orientation and arrangement of these entities, enabling users to tailor their properties on the substrate. Various mechanisms drive alignment layers, including surface roughness, geometrical confinement, and chemical heterogeneity.^141,142 In this context, films produced using anisotropic biopolymers find application as alignment layers based on the anisotropy of those factors.

Similar to other alignment layers, these biopolymeric films not only align materials following the director on the deposited film but also induce tilted alignment based on molecular characteristics. For instance, DNA, with its ability to induce tilted alignment relative to the long axis of its chains,¹⁴³ can serve as an alignment layer for thermotropic liquid crystals (Fig. 16a).^144,145 The DNA LC solution is coatable and can be applied as the alignment layer without a rubbing process due to the grooves in the chains. Sandwiched cells composed of a DNA alignment layer and thermotropic LCs could be employed in twisted-nematic and in-plane switching displays.

Furthermore, biomolecular alignment layers extend beyond nanomaterials, finding utility in cell alignment and tissue engineering due to their inherent biocompatibility (Fig. 17b). The layers immobilized by chemical treatment can be applied to an extracellular matrix that can align cellular structures on the surface.^120,138 These templates introduce anisotropic mechanical stresses during cellular differentiation and migration processes, and precise control over surface grooves via coating processes enables diverse cell alignments on dried films. The controllability based on LC elastic behavior would provide various topographic bio-templates for tissue scaffolding.

4.2. In the film: anisotropic matrix

The fluidity of liquid crystals enables them to function as solvents when mixed with additives, while their crystalline nature imparts directional alignment to these additives. This alignment in the liquid crystal medium is primarily driven by entropic steric interactions, which seek to maximize translational entropy at the expense of rotational entropy, a phenomenon initially described by Onsager.^35,146 The excluded volume effect, which tends to increase the effective volume of building blocks, not only facilitates the development of liquid crystal phases in concentrated solutions but also induces uniaxial alignment of the solutes along the local director of liquid crystals. The orientational ordering of solutes becomes arrested in the film after drying.

These findings demonstrate that co-dispersions allow for the alignment of nanorods with relatively small aspect ratios, which cannot spontaneously form ordered liquid crystal structures independently.^147–150 These nanorods are of particular interest due to their high surface-to-volume ratio and their responsiveness to optical, chemical, and electrical stimuli in an anisotropic manner.^151,152 Gold nanorods (GNRs), one of the examples, dispersed in a DNA solution exhibit various nematic-like ordering along with the local director of DNA chains (Fig. 17a).^73,74 The resulting DNA-GNR composite film displays polarization-dependent extinction colors based on localized surface plasmon resonance (LSPR). Additionally, the absorption spectrum of the films reveals that the longitudinal SPR peak is pronounced when the linearly polarized light aligns with the long axis of GNRs, whereas it becomes minimal when the polarizer is perpendicular. If the absorbance, including both longitudinal and transverse, is in the visible light range, the transmissive/reflective color can vary depending on the polarizer's angle.

Moreover, the GNRs formed a concentric pattern along the orientation of the CNCs in the deposited film. The GNRs dispersed in the CNCs are drop-cast on the flat substrate and the circular CNC-GNR film exhibited quadrant pattern under a single polarizer consisting of purple and blue colors along the orientation of the GNRs (Fig. 17b).⁹¹

Not only the two-dimensional structure, but the nanorods also form three-dimensional structures in the medium of chiral-induced liquid crystals (Fig. 17c).¹²³ Within viral films, nanorods form helicoidal structures, exhibiting axis-symmetric rotation with a specific azimuthal angle. This may serve as a coatable plasmonic optical filter with circular dichroism as the result of collective linear polarization effects.

Directional alignment within an anisotropic matrix also governs electrical properties. Water-soluble modifications of conducting polymers yield anisotropic structures when incorporated into a biopolymer medium during deposition, induced by controlled nucleation and growth, or during the drying process through phase separation (Fig. 18).^153,154 Thiophene-based polymers engage in dipole–dipole interactions with DNA phosphate groups and align under the DNA layer due to the molecular grooves of DNA (Fig. 18a).¹⁵³ The resulting composite demonstrates anisotropic electrical behavior in the part of an organic field-effect transistor (OFET), where electron or hole transport properties vary based on the interchain and intrachain direction. Furthermore, the electrical properties are regulated by the external optical stimuli in an anisotropic manner due to the aligned structure (Fig. 18b).¹⁵⁴ Perylene-based molecules intercalate between DNA base pairs through π–π interactions and form a helical structure in the solution coating process. The deposited film selectively interacts with the circularly polarized light displaying an ON/OFF behavior in the OFET device. These examples underscore the significant potential for further research on the application of anisotropic transfer induced by co-dispersion, coupled with other material characteristics.

Conclusions

In this review, we have presented current research findings regarding the self-assembly phenomena and deposition process of anisotropic biopolymers and colloids induced by evaporation (Table 1). Based on the Onsager theory, anisotropic biomaterials exhibiting a liquid crystalline phase above a specific concentration undergo a phase transition to a liquid crystalline state during the solution's evaporation. The resulting liquid crystalline structure is then mirrored in the deposited film during the deposition process. To comprehend the mechanisms governing the formation of these structures driven by the liquid crystal phase within the film and to exercise control over them through the solution process, extensive experimentation involving the manipulation of various parameters was conducted. Our approach aimed to advance the understanding of the formation mechanism by employing theoretical foundations comprehending the flow characteristics in evaporating solutions, polymer rheology, and the elastic properties of liquid crystal materials. Furthermore, recent report suggests the initial steps for practical applications of anisotropic biopolymers as fundamental building blocks,¹⁷⁰ aiming to enrich the material value of anisotropic biopolymers and unravel their distinctive behavior in confined, non-equilibrium systems.

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean Government (MSIT) (RS-2023-00273025, 2021M3H4A3A01050378).

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