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Bioinspired and biomimetic silk spinning
Composites Communications 13 (2019) 85–96
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Short Review
Bioinspired and biomimetic silk spinning
T
Yawen Liu, Jing Ren , Shengjie Ling ∗∗
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School of Physical Science and Technology, ShanghaiTech University, 393 Middle Huaxia Road, Shanghai 201210, China
ARTICLE INFO
ABSTRACT
Keywords: Nanocomposites Silk Spinning Biomimetic Mechanical properties
Spiders and silkworms are outstanding material and engineering masters in nature. They design and spin silk fibers with unrivaled mechanical properties by utilizing the most simple and green approach. To emulate the intelligence of spiders and silkworms in the design and production of silk fibers, a variety of artificial spinning methods have been developed in the lab. These bioinspired and biomimetic strategies significantly improved the mechanical performance of the regenerated silk fibers and provided possibility for further functionalization of the fibers. This review, therefore, provides a summary of methods to design, spin and functionalize regenerated silk fibers through bioinspired and biomimetic approaches. Here, the bioinspired and biomimetic spinning methods are introduced as four different categories, includes: (i) mimicking the natural spinning environments; (ii) mimicking the geometries of the spinning ducts; (iii) producing the silk spinning dope with nematic structures; as well as (iv) combined biomimetic spinning strategies.
1. Introduction Silks that spun by silkworms and spiders have interested engineers and scientists over the past century [1–5]. As one of the most abundant protein materials in nature, applications of these natural proteins at recent years have even been extended from traditional textile industries to different high-tech fields, such as optics [6,7], electronics [8–12], biomedicine [13–16], and environmental engineering [17–20]. However, studies of silks lead to a question: how to optimize the structureproperty-function relationship of regenerated silk materials? Indeed, the properties of most artificial silk materials are still not comparable to those of natural ones. For example, natural silks often exhibit much higher mechanical performance than regenerated silk fibers [2,21]. More attractively, like other natural materials [22], multifunctionality of natural silks blurs the distinction between material and device. For instance, spider silk is not only a fiber material that used in building web, but also a functional device that fulfills several functions for the spiders, such as load sensing, lifeline, and balloon [23]. While it remains a significant challenge in material engineering that combining structure and function in a regenerated silk fiber system. These gaps in engineered and natural silks prove that spiders and silkworms are more intelligent at silk material design. Optimizing spinning processes and constructing hierarchical structure are two secrets to the success of nature. Spiders and silkworms produce silk fibers by spinning a pre-assembled silk protein dope directly. The dope will be
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solidified to a fiber immediately after it leaves the spinning ducts [24–26]. These processes are carried out under physiological and ambient conditions with the aid of pH, ionic and shearing modulation. Therefore, many studies these years center on constructing regenerated silk fibers through bioinspired spinning processing. These bioinspired strategies not only offer us opportunity to optimize the structureproperty-function relationships of regenerated silk fibers, but also deeply inspire us to exploit new routes to use silk materials. This review, therefore, provides a summary of silk materials produced from bioinspired and biomimetic approaches. We first demonstrate the natural silk spinning process and then introduced the related bioinspired spinning methods to spin regenerated/recombinant silk fibers. In this review, we introduce these bioinspired and biomimetic spinning methods as four different categories, includes: (i) mimicking the natural spinning environments; (ii) mimicking the geometries of the spinning ducts; (iii) producing the silk spinning dope with nematic structures; as well as (iv) combined biomimetic spinning strategies. 2. Natural silk spinning Spiders and silkworms spin silk fibers with unrivaled mechanical properties by utilizing a mild and green approach [24–27]. Fig. 1A and B sketches a detailed evolutionary process of natural silk spinning [24–26]. Silk protein is first synthesized at the epithelial wall of the tail with a concentration of ∼12 wt% (pH ∼8). Further, the protein travels
Corresponding author. Corresponding author. E-mail addresses: [email protected] (J. Ren), [email protected] (S. Ling).
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https://doi.org/10.1016/j.coco.2019.03.004 Received 28 February 2019; Received in revised form 19 March 2019; Accepted 21 March 2019 Available online 23 March 2019 2452-2139/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Illustration of natural silk spinning process. (A) A silkworm spinning gland. According to the evolution of silk protein during spinning, it is divided into three parts. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature. (B) Factors like pH, ions, shearing force, and geometries of the spinning ducts, dominate the transition of protein from aqueous micelles to solid fiber. Reprinted with permission from Ref. [24]. Copyright 2001 Springer Nature. (C) Assembly mechanism of silk fiber along the natural spinning apparatus. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature.
several biomimetic spinning methods (Fig. 2) have been designed to emulate the natural silk spinning processing. Depending on the spinning characteristics that they mimicked, biomimetic silk spinning can be divided into three different types.
forward in the sac or ampulla (middle division) with a gradual increase in concentration (∼25 wt%). In this middle division, the protein was assembled and stabilized as a micelle-like configuration (pH ∼6–7). When the protein flow through spinning duct, several factors, i.e., pH, ions, shearing force, and geometries of the spinning ducts, dominate the transition of protein from aqueous micelles to solid fiber. In this stage, the pH of spinning dope decreased gradually along the spinning ducts with variation of ion concentration. At the same time, shearing force flow is increased by geometric constriction of the spinning duct. The synergies of these four factors make the protein micelles assemble to anisotropic liquid crystals, allowing the molecules to flow in a prealigned manner (Fig. 1C). Finally, silk fiber is formed during pulling out from spigot, with stretching and dehydration conditions and under the shear stress. The silk fiber consists of repetitive amino acid sequences with alternative hydrophilic and hydrophobic segments and nonrepetitive regions. Here, β-sheet nanocrystals form in the repetitive region play a key role in the tensile strength and toughness of silks, while the semiamorphous region consists of random soil and/or helix structures mainly contributes to the elasticity. Just like other natural materials, the hierarchical structure plays an important role in determining the mechanical property of silk fibers, which remains difficult to completely imitate, but always provides a lot of inspirations for advanced material design.
3.1. Mimicking natural spinning environments To mimic the gradual lowering of pH along the spinning duct, a spinning system that construed by a series of pulled glass capillaries has been designed to mimic the physiological environment of silk spinning glands (Fig. 2A) [43,44]. During the spinning, highly concentrated spinning dope (aqueous spidroin solution in this case, blue) is introduced into the glass capillaries system. Meanwhile, aqueous buffers with different pH are pumped into the system and laminar flow is formed. It causes increased flow rate and shearing of the spinning dope. When moving through the device, the laminar flow also allows for diffusion at the solution interfaces, leading to a gradual lowered pH and increased pCO2 in the spinning dope [43]. By using such a similar spinning device (Fig. 3), recombinant spidroins with molecular weight of 33 kDa was spun into fibers with lengths larger than kilometer. The toughness of these regenerated silk fibers reached 45 MJ/m3, which is the highest value for as-spun artificial spider silk fiber up to now [44]. In addition to pH, metallic ions, such as potassium, calcium, and magnesium, also play important roles in silk fiber formation during natural spinning [24,45]. For instance, the content of calcium ions decreased continuously from the middle division to the spinning duct. High concentrations of calcium ions in the middle division allow silk micelles to be very stable at high concentrations [46]. This finding provided inspirations to spinning dope preparation with high silk concentration. An ideal spinning dope is an aqueous state with high silk concentration, which, however, cause more likely gelation of the
3. Bioinspired silk spinning Artificial spinning methods (e.g., wet-spinning [28–31], dry-spinning [32–39], and electrostatic spinning [40–42]) have been pursued in these decades to produce regenerated silk fibers, however, their mechanical properties are far inferior to natural ones (Table 1). Therefore, 86
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Table 1 Comparison of mechanical properties of regenerated silk fibers [21,29,32-38,44,47,51,64-112]*.a
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Table 1 (continued)
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Table 1 (continued)
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Table 1 (continued)
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The blue and red regions are mechanical properties of regenerated silkworm silk fibers, the blue and red region are spun by wet-spinning and dry-spinning method, respectively. The green region is mechanical properties of regenerated and recombinant spider silk fibers. b Spinning dope is expressed as “solute/solvent, concentration”. c The mechanical properties of as-spun fibers (without any post-treatments) are expressed as: stress (GPa), strain (%), modulus (GPa). d These values are calculated from true stress/strain. RSF = regenerated silk fibroin; ADF-3 = Araneus diadematus (MaSp2) fibroin 3; eADF-3 = engineered variants of Araneus diadematus (MaSp2) fibroin 3; MaSp = Major ampullate Spidroin; TuSp = Tubuliform Spidroin; TFA = Trifluoroacetic acid; HFIP=Hexafluoroisopropanol; NMMO=N-Methyl-Morpholine-Noxide; HFA= Hexafluoroacetone hydrate; EMIMCl = 1-Ethyl-3-methylimidazolium Chloride; U.C. = unclear. *Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature.
spinning dope. Recently, calcium ions have been introduced into spinning dope to improve the stability of the protein [47]. The resultant spinning dope with silk concentration of 15–20 wt% has high viscosity along with stability, allowing for continuous wet-spinning for more than kilometers [47].
container, the materials (silk microfibril as an example) are aligned along the flow direction due to large velocity gradient of flow. At the next stage, depending on their radial location, the silk microfibrils are subjected to laminar shear or plug flow. In the plug flow zone, where r < r0, spatial variations in velocity are negligible, so shear stress only has limited impact on silk microfibrils. Under these circumstances, Brownian motion gradually offsets the initial extensional alignment, while negligible additional alignment occurs at the same time. Outside the plug flow area (where r0 < r < R), the shear stress (τ) is larger than the yield stress (τ0). The silk microfibrils network can break into flocs owing to the yielding under shear. Thus, microfibril rotation and flocculation, as well as shear force, affect silk microfibril orientation in different and competing modes in this area. These cumulative effects
3.2. Mimicking the geometries of the spinning ducts In artificial silk spinning, syringe needles are the simplest and most widely used spinnerets, but usually are not the optimized choices due to their unfavorable hydrodynamic behaviors. Fig. 4 illustrates the hypothetical effect of flow regions inside syringe spinnerets [48,49]. When the nematic spinning dope enters the spinneret from the
Fig. 2. Bioinspired silk spinning process. (A) A spinning system mimics the gradual lowering of pH along the spinning duct of natural silk. Reprinted with permission from Ref. [43]. Copyright 2015 Springer Nature. (B) A microfluidic channel on a spinning chip to emulate the specific geometry of the natural spinning duct. Reprinted with permission from Ref. [51]. Copyright 2016 Springer Nature. (C) A dry-spinning process mimics liquid crystalline spinning of natural silk using a nematic silk microfibril solution. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature. 91
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Fig. 4. The hypothetical effect of flow regions inside the syringe spinneret. (A) The nematic spinning dope enters the spinneret from the container, the materials will be aligned along the flow direction. (B) Hypothetical flow profile for a shear-thinning fluid with a yield stress in a nozzle of radius R. v and τ are velocities and shear stress in fluid layers at a radial distance r from the center. When τ exceeds the yield stress τ0, the outer radius of the plug flow region is r0. The shear stress at the wall τw is proportional to the pressure drop over the nozzle and inversely proportional to the capillary length divided by its diameter. Reprinted with permission from Ref. [48]. Copyright 2006 Wydawnictwo Uniwersytetu Przyrodniczego.
3.3. Producing the silk spinning dope with nematic structures Artificial spinning can be simplified as an extrusion-based process, which requires stable fluids with adequate viscosity to ensure continuous extrusion without clogging. On the other hand, once the spinning dope passed through the spinneret, it needs to be solidified immediately in coagulation bath (wet-spinning) or even needs to selfstand at air condition (dry-spinning). In extrusion based spinning processing, the relationship between radial shear stress of the nozzle (τ) and nozzle size can be estimated by the following equation [55],
Fig. 3. Biomimetic spinning of artificial spider silk. (A) Image of highly concentrated spinning dope in a syringe is pumped into a low-pH aqueous collection bath. Fibers are collected and rolled up onto frames (arrow). (B) Image of a fiber spun in the low-pH aqueous bath. (C) Wet fiber nest in the lowpH aqueous bath. (D) Fibers rolled and collected on a frame. Scale bar in a, 3 cm; b, 3 mm; c, d, 5 mm. Reprinted with permission from Ref. [44]. Copyright 2017 Springer Nature.
=
P r 2L
(1)
where ΔP is the maximum pressure applied at the nozzle, r is the radial position form the center to the edge of the nozzle, and L is the nozzle length. Using the spinner's maximum radial size of the nozzle (rmax), the maximum shear stress (τmax) of the spinner can be determined from this equation. Dynamic yield stresses (τy) of spinning dope can be obtained from oscillatory experiments. The dynamic yield stress is defined as the yield stress at G″ = G′ and is directly related to solid content of the dope. If τy > τmax, the dope would experience a plug flow, which leads to a region of dope that does not yield a constant velocity, thereby causing no shear flow. Thus, a critical solid content of materials in spinning dope can be obtained at τy = τmax. When the solid content of materials is lower than the critical concentration, the critical radius (rc) can be estimated from the yield stress data (τy) and Eq. (1), while the dope is expected to undergo shear flow. This estimation for biopolymers requires the spinning solution to have sufficiently high elastic moduli (G′), typically higher than few kPa, and yield stresses on the order of a few 102 Pa [56]. This value is still hard to reach for aqueous silk solution. Nature solves these problems by liquid crystalline spinning [24,57]. The silk proteins in the spinning ducts of spiders and silkworms are liquid crystalline, which makes proteins possible to be stacked in a compact conformation and allows it to be processed at high concentrations. Liquid crystallinity provides desirable rheological properties, which enables it to efficiently spin fiber from protein molecules as large as spidroins and silk fibroins (∼350 kDa). As shown in Fig. 1B, the silk proteins in the spinning duct form a nematic phase, which allows flowing as a liquid but sustains some order-aligned characteristic of a crystal. Liquid crystallinity thus enables the viscous dope to travel
lead to the silk microfibrils in the fiber periphery being more random than that in the fiber core. After the dope passed through nozzle, the oriented biopolymer nanofibrils in the fiber can be fixed and even enhanced during coagulation and dehydration. Yet in some cases, the orientation of as-spun fibers obtained from dehydration is still relatively weak, thus in most cases, the post-drawing processing is needed to further increase silk microfibril orientation. By contrast, spinning ducts of both spiders and silkworms are made up of contracted channels with hyperbolic geometries [50–52]. For instance, the diameter of the tapered Nephila edulis S-duct decreases from the funnel as a two-stage hyperbolic curve. When it reaches to a region called the draw down taper, the diameter decreases more rapidly as a two-stage exponential function [51,52]. The contraction of spinning ducts makes the spinning dope flows through the channel in a favorable manner (laminar flow) and enables a compact spinning dope which is further pre-aligned under elongation and shearing forces. Accordingly, microfluidic-based spinning systems have been designed, and some three-dimensional spider-inspired spinnerets have been achieved [52–54]. As presented in Fig. 2B, a biomimetic microfluidic channel was created on a spinning chip to emulate the specific geometry of natural spinning ducts [52]. Geometric contraction-induced shearing flow substantially contributed to the microfibrils compact aggregation in spinning dope. The additional post-drawing and coagulation processes further improved the hierarchical structure of fibers. As a result, for the resultant recombinant spider silk fibers with a low molecular weight of 47 kDa, the tensile strength and elongation reached up to 510 MPa and 15%, respectively [52]. 92
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Fig. 5. Examples of functional regenerated silk fibers (RSFs). (A) Illustration of the structure of conductive core–shell RSFs, with SEM images of the surface area at different magnifications. (B) Conductive RSFs are woven in a cloth. (C, D) Resistance response of the functional RSF cloth for finger-touching and human breathing. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature.
overcome Brownian diffusion and align the cellulose nanofibrils along flow (fiber long axis) direction. After the flow stretching is ceased, Brownian diffusion continues to weaken the nanofibril alignment, but meanwhile, the electrolytes or acid ions (based on the pH) in the shell layer diffuse into the dope and trigger surface-charge-controlled gelation. The weaken (disorientation) effects are prevented when the gel transition occurs. The aligned nanofibrils are fixed in gels and thus can be maintained in the final fibers. Using such a spinning system, the preferential nanofibril orientation along the filament direction can be controlled by regulating process parameters, such as flow rate, flow acceleration, and ionic strength. The resultant regenerated CNF/silk-based fibers show dramatically increased mechanical properties, which are approximately 55 GPa, 1015 GPa, and 55 MJ/m3 for stiffness, strength, and toughness respectively [59]. These values are higher than those of other regenerated biopolymer fibers, and are even higher than most natural cellulose nanofibril-based fibers [60], but are still weaker than single cellulose nanocrystal (100–160 GPa [61]) and cellulose nanofibril (∼100 GPa [62]).
slowly through spinning duct while the silk proteins form complex alignment patterns [24]. In order to emulate liquid crystalline spinning of natural silk, a nematic silk microfibril solution has been synthesized through partial dissolution of B. mori silk fiber [21] (Fig. 2C). This nematic silk spinning dope was further spun into regenerated silk fibers at the air condition by using a simple dry-spinning device. The nematic silk microfibrils can be directly reeled out continuously and no further post-drawing process are required, allowed for building different sophisticated one to threedimensional constructions. Different from regenerated silk fiber generated from silk solution, the fiber spun from silk microfibrils maintained the hierarchical structure of natural silks and thus retained the mechanical advantages of natural silks. For example, the modulus of these regenerated silk fiber reached 11 ± 4 GPa [21], which is even higher than natural spider silk (∼10 GPa [1]). In addition, because this biomimetic spinning process does not require additional post-processing, such as solidification, curing, and post-stretching, it can be further functionalized by introducing conductive layers, such as carbon nanotube or graphene coating. The resultant conductive regenerated silk fibers have been confirmed to be able to swift with changes of humidity and temperature (Fig. 5), showing promising applications in wearable textile, biosensor, and implant devices.
4. Conclusions and perspectives The inherent complexity and polydispersity of silks create severe difficulties in designing and manipulating silk materials for practical applications [63]. Therefore, learning how spiders and silkworms use these materials is very important, so that scientists and engineers can optimize their design and application strategies of silk materials for site-specific applications. In this review, we summarized the most recent bioinspired and biomimetic spinning approaches to produce regenerated silk fibers. By using these bioinspired and biomimetic strategies, significant improvements have achieved in artificial silk spinning. For example, the mechanical properties of regenerated silk fibers are often superior to those of fibers spun from industrial-based spinning techniques. However, some challenges remain, an ideal spinning technique remains difficult to achieve. Compared to wet-spinning and dry-spinning, microfluidic-based spinning indeed can obtain fibers with much higher mechanical performance, but this technique is more complex and difficult to scale up. The potential functional applications of regenerated silk fibers are another aspect that is not well-explored, despite several works proposing several promising applications,
3.4. Combined biomimetic spinning strategies In practice, different biomimetic spinning strategies were often combined. For instance, microfluidic spinning can emulate the geometries of spinning ducts, control the dope flow as well as optimize processing parameters. Meanwhile, some natural spinning environmental parameters, such as the gradients of pH, salt, and shear-flow, can also be applied in a microfluidic system using double concentric channels [24,25]. Most recently, a flow-focusing spinning system (Fig. 6A) was developed to control the alignment of nematic cellulose nanofibril (CNF)/silk solution and to produce high-performance regenerated CNF/silk fibers. A simplified schematic to explain the nanofibril alignment process during spinning is shown in Fig. 6B [58]. At the intersection of three microfluidic channels, the core flow of spinning dope is subjected to shell flows, colliding with it from sides. When the velocities of shell layers are higher than that of core flow, the shell layers can create an extensional flow in the core, which helps to
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Fig. 6. Schematic of the flow-assisted organization of cellulose nanofibrils into macroscale fibers. (A) Double flow-focusing channel for cellulose nanofibril assembly. The cellulose nanofibrils suspension (brown) is injected in the core flow, deionized water (blue) in the first sheath, and acid (green) in the second sheath flows. Arrows indicate the flow direction. Reprinted with permission from Ref. [113]. Copyright 2018 American Chemical Society. (B) The bottom-right schematic reveals the evolution of cellulose nanofibril orientation during the microfluidic-assisted spinning. The cellulose nanofibrils are illustrated as pink rods. The diffusion of Na+, from the NaCl focusing liquid, is illustrated as blue tints. The rows of small images above and below illustrate the hydrodynamical, molecular and electrochemical processes involved. Brownian diffusion is illustrated with the black dashed arrows. The a, b, c and d corresponded to the a, b, c and d region in (A). Hydrodynamically induced alignment is illustrated by grey solid arrows. Reprinted with permission from Ref. [58]. Copyright 2014 Springer Nature. Hydrodynamic and electrostatic interactions at different positions along the channel are illustrated schematically on the right.
including fiber sensors [21] and cell carriers [59]. Acknowledgments This work was supported by grants from the National Natural Science Foundation (No. U1832109), Shanghai Pujiang Program (18PJ1408600) and the starting grant of ShanghaiTech University. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.coco.2019.03.004.
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Short Review
Bioinspired and biomimetic silk spinning
T
Yawen Liu, Jing Ren , Shengjie Ling ∗∗
∗
School of Physical Science and Technology, ShanghaiTech University, 393 Middle Huaxia Road, Shanghai 201210, China
ARTICLE INFO
ABSTRACT
Keywords: Nanocomposites Silk Spinning Biomimetic Mechanical properties
Spiders and silkworms are outstanding material and engineering masters in nature. They design and spin silk fibers with unrivaled mechanical properties by utilizing the most simple and green approach. To emulate the intelligence of spiders and silkworms in the design and production of silk fibers, a variety of artificial spinning methods have been developed in the lab. These bioinspired and biomimetic strategies significantly improved the mechanical performance of the regenerated silk fibers and provided possibility for further functionalization of the fibers. This review, therefore, provides a summary of methods to design, spin and functionalize regenerated silk fibers through bioinspired and biomimetic approaches. Here, the bioinspired and biomimetic spinning methods are introduced as four different categories, includes: (i) mimicking the natural spinning environments; (ii) mimicking the geometries of the spinning ducts; (iii) producing the silk spinning dope with nematic structures; as well as (iv) combined biomimetic spinning strategies.
1. Introduction Silks that spun by silkworms and spiders have interested engineers and scientists over the past century [1–5]. As one of the most abundant protein materials in nature, applications of these natural proteins at recent years have even been extended from traditional textile industries to different high-tech fields, such as optics [6,7], electronics [8–12], biomedicine [13–16], and environmental engineering [17–20]. However, studies of silks lead to a question: how to optimize the structureproperty-function relationship of regenerated silk materials? Indeed, the properties of most artificial silk materials are still not comparable to those of natural ones. For example, natural silks often exhibit much higher mechanical performance than regenerated silk fibers [2,21]. More attractively, like other natural materials [22], multifunctionality of natural silks blurs the distinction between material and device. For instance, spider silk is not only a fiber material that used in building web, but also a functional device that fulfills several functions for the spiders, such as load sensing, lifeline, and balloon [23]. While it remains a significant challenge in material engineering that combining structure and function in a regenerated silk fiber system. These gaps in engineered and natural silks prove that spiders and silkworms are more intelligent at silk material design. Optimizing spinning processes and constructing hierarchical structure are two secrets to the success of nature. Spiders and silkworms produce silk fibers by spinning a pre-assembled silk protein dope directly. The dope will be
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solidified to a fiber immediately after it leaves the spinning ducts [24–26]. These processes are carried out under physiological and ambient conditions with the aid of pH, ionic and shearing modulation. Therefore, many studies these years center on constructing regenerated silk fibers through bioinspired spinning processing. These bioinspired strategies not only offer us opportunity to optimize the structureproperty-function relationships of regenerated silk fibers, but also deeply inspire us to exploit new routes to use silk materials. This review, therefore, provides a summary of silk materials produced from bioinspired and biomimetic approaches. We first demonstrate the natural silk spinning process and then introduced the related bioinspired spinning methods to spin regenerated/recombinant silk fibers. In this review, we introduce these bioinspired and biomimetic spinning methods as four different categories, includes: (i) mimicking the natural spinning environments; (ii) mimicking the geometries of the spinning ducts; (iii) producing the silk spinning dope with nematic structures; as well as (iv) combined biomimetic spinning strategies. 2. Natural silk spinning Spiders and silkworms spin silk fibers with unrivaled mechanical properties by utilizing a mild and green approach [24–27]. Fig. 1A and B sketches a detailed evolutionary process of natural silk spinning [24–26]. Silk protein is first synthesized at the epithelial wall of the tail with a concentration of ∼12 wt% (pH ∼8). Further, the protein travels
Corresponding author. Corresponding author. E-mail addresses: [email protected] (J. Ren), [email protected] (S. Ling).
∗∗
https://doi.org/10.1016/j.coco.2019.03.004 Received 28 February 2019; Received in revised form 19 March 2019; Accepted 21 March 2019 Available online 23 March 2019 2452-2139/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Illustration of natural silk spinning process. (A) A silkworm spinning gland. According to the evolution of silk protein during spinning, it is divided into three parts. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature. (B) Factors like pH, ions, shearing force, and geometries of the spinning ducts, dominate the transition of protein from aqueous micelles to solid fiber. Reprinted with permission from Ref. [24]. Copyright 2001 Springer Nature. (C) Assembly mechanism of silk fiber along the natural spinning apparatus. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature.
several biomimetic spinning methods (Fig. 2) have been designed to emulate the natural silk spinning processing. Depending on the spinning characteristics that they mimicked, biomimetic silk spinning can be divided into three different types.
forward in the sac or ampulla (middle division) with a gradual increase in concentration (∼25 wt%). In this middle division, the protein was assembled and stabilized as a micelle-like configuration (pH ∼6–7). When the protein flow through spinning duct, several factors, i.e., pH, ions, shearing force, and geometries of the spinning ducts, dominate the transition of protein from aqueous micelles to solid fiber. In this stage, the pH of spinning dope decreased gradually along the spinning ducts with variation of ion concentration. At the same time, shearing force flow is increased by geometric constriction of the spinning duct. The synergies of these four factors make the protein micelles assemble to anisotropic liquid crystals, allowing the molecules to flow in a prealigned manner (Fig. 1C). Finally, silk fiber is formed during pulling out from spigot, with stretching and dehydration conditions and under the shear stress. The silk fiber consists of repetitive amino acid sequences with alternative hydrophilic and hydrophobic segments and nonrepetitive regions. Here, β-sheet nanocrystals form in the repetitive region play a key role in the tensile strength and toughness of silks, while the semiamorphous region consists of random soil and/or helix structures mainly contributes to the elasticity. Just like other natural materials, the hierarchical structure plays an important role in determining the mechanical property of silk fibers, which remains difficult to completely imitate, but always provides a lot of inspirations for advanced material design.
3.1. Mimicking natural spinning environments To mimic the gradual lowering of pH along the spinning duct, a spinning system that construed by a series of pulled glass capillaries has been designed to mimic the physiological environment of silk spinning glands (Fig. 2A) [43,44]. During the spinning, highly concentrated spinning dope (aqueous spidroin solution in this case, blue) is introduced into the glass capillaries system. Meanwhile, aqueous buffers with different pH are pumped into the system and laminar flow is formed. It causes increased flow rate and shearing of the spinning dope. When moving through the device, the laminar flow also allows for diffusion at the solution interfaces, leading to a gradual lowered pH and increased pCO2 in the spinning dope [43]. By using such a similar spinning device (Fig. 3), recombinant spidroins with molecular weight of 33 kDa was spun into fibers with lengths larger than kilometer. The toughness of these regenerated silk fibers reached 45 MJ/m3, which is the highest value for as-spun artificial spider silk fiber up to now [44]. In addition to pH, metallic ions, such as potassium, calcium, and magnesium, also play important roles in silk fiber formation during natural spinning [24,45]. For instance, the content of calcium ions decreased continuously from the middle division to the spinning duct. High concentrations of calcium ions in the middle division allow silk micelles to be very stable at high concentrations [46]. This finding provided inspirations to spinning dope preparation with high silk concentration. An ideal spinning dope is an aqueous state with high silk concentration, which, however, cause more likely gelation of the
3. Bioinspired silk spinning Artificial spinning methods (e.g., wet-spinning [28–31], dry-spinning [32–39], and electrostatic spinning [40–42]) have been pursued in these decades to produce regenerated silk fibers, however, their mechanical properties are far inferior to natural ones (Table 1). Therefore, 86
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Table 1 Comparison of mechanical properties of regenerated silk fibers [21,29,32-38,44,47,51,64-112]*.a
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Table 1 (continued)
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The blue and red regions are mechanical properties of regenerated silkworm silk fibers, the blue and red region are spun by wet-spinning and dry-spinning method, respectively. The green region is mechanical properties of regenerated and recombinant spider silk fibers. b Spinning dope is expressed as “solute/solvent, concentration”. c The mechanical properties of as-spun fibers (without any post-treatments) are expressed as: stress (GPa), strain (%), modulus (GPa). d These values are calculated from true stress/strain. RSF = regenerated silk fibroin; ADF-3 = Araneus diadematus (MaSp2) fibroin 3; eADF-3 = engineered variants of Araneus diadematus (MaSp2) fibroin 3; MaSp = Major ampullate Spidroin; TuSp = Tubuliform Spidroin; TFA = Trifluoroacetic acid; HFIP=Hexafluoroisopropanol; NMMO=N-Methyl-Morpholine-Noxide; HFA= Hexafluoroacetone hydrate; EMIMCl = 1-Ethyl-3-methylimidazolium Chloride; U.C. = unclear. *Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature.
spinning dope. Recently, calcium ions have been introduced into spinning dope to improve the stability of the protein [47]. The resultant spinning dope with silk concentration of 15–20 wt% has high viscosity along with stability, allowing for continuous wet-spinning for more than kilometers [47].
container, the materials (silk microfibril as an example) are aligned along the flow direction due to large velocity gradient of flow. At the next stage, depending on their radial location, the silk microfibrils are subjected to laminar shear or plug flow. In the plug flow zone, where r < r0, spatial variations in velocity are negligible, so shear stress only has limited impact on silk microfibrils. Under these circumstances, Brownian motion gradually offsets the initial extensional alignment, while negligible additional alignment occurs at the same time. Outside the plug flow area (where r0 < r < R), the shear stress (τ) is larger than the yield stress (τ0). The silk microfibrils network can break into flocs owing to the yielding under shear. Thus, microfibril rotation and flocculation, as well as shear force, affect silk microfibril orientation in different and competing modes in this area. These cumulative effects
3.2. Mimicking the geometries of the spinning ducts In artificial silk spinning, syringe needles are the simplest and most widely used spinnerets, but usually are not the optimized choices due to their unfavorable hydrodynamic behaviors. Fig. 4 illustrates the hypothetical effect of flow regions inside syringe spinnerets [48,49]. When the nematic spinning dope enters the spinneret from the
Fig. 2. Bioinspired silk spinning process. (A) A spinning system mimics the gradual lowering of pH along the spinning duct of natural silk. Reprinted with permission from Ref. [43]. Copyright 2015 Springer Nature. (B) A microfluidic channel on a spinning chip to emulate the specific geometry of the natural spinning duct. Reprinted with permission from Ref. [51]. Copyright 2016 Springer Nature. (C) A dry-spinning process mimics liquid crystalline spinning of natural silk using a nematic silk microfibril solution. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature. 91
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Fig. 4. The hypothetical effect of flow regions inside the syringe spinneret. (A) The nematic spinning dope enters the spinneret from the container, the materials will be aligned along the flow direction. (B) Hypothetical flow profile for a shear-thinning fluid with a yield stress in a nozzle of radius R. v and τ are velocities and shear stress in fluid layers at a radial distance r from the center. When τ exceeds the yield stress τ0, the outer radius of the plug flow region is r0. The shear stress at the wall τw is proportional to the pressure drop over the nozzle and inversely proportional to the capillary length divided by its diameter. Reprinted with permission from Ref. [48]. Copyright 2006 Wydawnictwo Uniwersytetu Przyrodniczego.
3.3. Producing the silk spinning dope with nematic structures Artificial spinning can be simplified as an extrusion-based process, which requires stable fluids with adequate viscosity to ensure continuous extrusion without clogging. On the other hand, once the spinning dope passed through the spinneret, it needs to be solidified immediately in coagulation bath (wet-spinning) or even needs to selfstand at air condition (dry-spinning). In extrusion based spinning processing, the relationship between radial shear stress of the nozzle (τ) and nozzle size can be estimated by the following equation [55],
Fig. 3. Biomimetic spinning of artificial spider silk. (A) Image of highly concentrated spinning dope in a syringe is pumped into a low-pH aqueous collection bath. Fibers are collected and rolled up onto frames (arrow). (B) Image of a fiber spun in the low-pH aqueous bath. (C) Wet fiber nest in the lowpH aqueous bath. (D) Fibers rolled and collected on a frame. Scale bar in a, 3 cm; b, 3 mm; c, d, 5 mm. Reprinted with permission from Ref. [44]. Copyright 2017 Springer Nature.
=
P r 2L
(1)
where ΔP is the maximum pressure applied at the nozzle, r is the radial position form the center to the edge of the nozzle, and L is the nozzle length. Using the spinner's maximum radial size of the nozzle (rmax), the maximum shear stress (τmax) of the spinner can be determined from this equation. Dynamic yield stresses (τy) of spinning dope can be obtained from oscillatory experiments. The dynamic yield stress is defined as the yield stress at G″ = G′ and is directly related to solid content of the dope. If τy > τmax, the dope would experience a plug flow, which leads to a region of dope that does not yield a constant velocity, thereby causing no shear flow. Thus, a critical solid content of materials in spinning dope can be obtained at τy = τmax. When the solid content of materials is lower than the critical concentration, the critical radius (rc) can be estimated from the yield stress data (τy) and Eq. (1), while the dope is expected to undergo shear flow. This estimation for biopolymers requires the spinning solution to have sufficiently high elastic moduli (G′), typically higher than few kPa, and yield stresses on the order of a few 102 Pa [56]. This value is still hard to reach for aqueous silk solution. Nature solves these problems by liquid crystalline spinning [24,57]. The silk proteins in the spinning ducts of spiders and silkworms are liquid crystalline, which makes proteins possible to be stacked in a compact conformation and allows it to be processed at high concentrations. Liquid crystallinity provides desirable rheological properties, which enables it to efficiently spin fiber from protein molecules as large as spidroins and silk fibroins (∼350 kDa). As shown in Fig. 1B, the silk proteins in the spinning duct form a nematic phase, which allows flowing as a liquid but sustains some order-aligned characteristic of a crystal. Liquid crystallinity thus enables the viscous dope to travel
lead to the silk microfibrils in the fiber periphery being more random than that in the fiber core. After the dope passed through nozzle, the oriented biopolymer nanofibrils in the fiber can be fixed and even enhanced during coagulation and dehydration. Yet in some cases, the orientation of as-spun fibers obtained from dehydration is still relatively weak, thus in most cases, the post-drawing processing is needed to further increase silk microfibril orientation. By contrast, spinning ducts of both spiders and silkworms are made up of contracted channels with hyperbolic geometries [50–52]. For instance, the diameter of the tapered Nephila edulis S-duct decreases from the funnel as a two-stage hyperbolic curve. When it reaches to a region called the draw down taper, the diameter decreases more rapidly as a two-stage exponential function [51,52]. The contraction of spinning ducts makes the spinning dope flows through the channel in a favorable manner (laminar flow) and enables a compact spinning dope which is further pre-aligned under elongation and shearing forces. Accordingly, microfluidic-based spinning systems have been designed, and some three-dimensional spider-inspired spinnerets have been achieved [52–54]. As presented in Fig. 2B, a biomimetic microfluidic channel was created on a spinning chip to emulate the specific geometry of natural spinning ducts [52]. Geometric contraction-induced shearing flow substantially contributed to the microfibrils compact aggregation in spinning dope. The additional post-drawing and coagulation processes further improved the hierarchical structure of fibers. As a result, for the resultant recombinant spider silk fibers with a low molecular weight of 47 kDa, the tensile strength and elongation reached up to 510 MPa and 15%, respectively [52]. 92
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Fig. 5. Examples of functional regenerated silk fibers (RSFs). (A) Illustration of the structure of conductive core–shell RSFs, with SEM images of the surface area at different magnifications. (B) Conductive RSFs are woven in a cloth. (C, D) Resistance response of the functional RSF cloth for finger-touching and human breathing. Reprinted with permission from Ref. [21]. Copyright 2017 Springer Nature.
overcome Brownian diffusion and align the cellulose nanofibrils along flow (fiber long axis) direction. After the flow stretching is ceased, Brownian diffusion continues to weaken the nanofibril alignment, but meanwhile, the electrolytes or acid ions (based on the pH) in the shell layer diffuse into the dope and trigger surface-charge-controlled gelation. The weaken (disorientation) effects are prevented when the gel transition occurs. The aligned nanofibrils are fixed in gels and thus can be maintained in the final fibers. Using such a spinning system, the preferential nanofibril orientation along the filament direction can be controlled by regulating process parameters, such as flow rate, flow acceleration, and ionic strength. The resultant regenerated CNF/silk-based fibers show dramatically increased mechanical properties, which are approximately 55 GPa, 1015 GPa, and 55 MJ/m3 for stiffness, strength, and toughness respectively [59]. These values are higher than those of other regenerated biopolymer fibers, and are even higher than most natural cellulose nanofibril-based fibers [60], but are still weaker than single cellulose nanocrystal (100–160 GPa [61]) and cellulose nanofibril (∼100 GPa [62]).
slowly through spinning duct while the silk proteins form complex alignment patterns [24]. In order to emulate liquid crystalline spinning of natural silk, a nematic silk microfibril solution has been synthesized through partial dissolution of B. mori silk fiber [21] (Fig. 2C). This nematic silk spinning dope was further spun into regenerated silk fibers at the air condition by using a simple dry-spinning device. The nematic silk microfibrils can be directly reeled out continuously and no further post-drawing process are required, allowed for building different sophisticated one to threedimensional constructions. Different from regenerated silk fiber generated from silk solution, the fiber spun from silk microfibrils maintained the hierarchical structure of natural silks and thus retained the mechanical advantages of natural silks. For example, the modulus of these regenerated silk fiber reached 11 ± 4 GPa [21], which is even higher than natural spider silk (∼10 GPa [1]). In addition, because this biomimetic spinning process does not require additional post-processing, such as solidification, curing, and post-stretching, it can be further functionalized by introducing conductive layers, such as carbon nanotube or graphene coating. The resultant conductive regenerated silk fibers have been confirmed to be able to swift with changes of humidity and temperature (Fig. 5), showing promising applications in wearable textile, biosensor, and implant devices.
4. Conclusions and perspectives The inherent complexity and polydispersity of silks create severe difficulties in designing and manipulating silk materials for practical applications [63]. Therefore, learning how spiders and silkworms use these materials is very important, so that scientists and engineers can optimize their design and application strategies of silk materials for site-specific applications. In this review, we summarized the most recent bioinspired and biomimetic spinning approaches to produce regenerated silk fibers. By using these bioinspired and biomimetic strategies, significant improvements have achieved in artificial silk spinning. For example, the mechanical properties of regenerated silk fibers are often superior to those of fibers spun from industrial-based spinning techniques. However, some challenges remain, an ideal spinning technique remains difficult to achieve. Compared to wet-spinning and dry-spinning, microfluidic-based spinning indeed can obtain fibers with much higher mechanical performance, but this technique is more complex and difficult to scale up. The potential functional applications of regenerated silk fibers are another aspect that is not well-explored, despite several works proposing several promising applications,
3.4. Combined biomimetic spinning strategies In practice, different biomimetic spinning strategies were often combined. For instance, microfluidic spinning can emulate the geometries of spinning ducts, control the dope flow as well as optimize processing parameters. Meanwhile, some natural spinning environmental parameters, such as the gradients of pH, salt, and shear-flow, can also be applied in a microfluidic system using double concentric channels [24,25]. Most recently, a flow-focusing spinning system (Fig. 6A) was developed to control the alignment of nematic cellulose nanofibril (CNF)/silk solution and to produce high-performance regenerated CNF/silk fibers. A simplified schematic to explain the nanofibril alignment process during spinning is shown in Fig. 6B [58]. At the intersection of three microfluidic channels, the core flow of spinning dope is subjected to shell flows, colliding with it from sides. When the velocities of shell layers are higher than that of core flow, the shell layers can create an extensional flow in the core, which helps to
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Fig. 6. Schematic of the flow-assisted organization of cellulose nanofibrils into macroscale fibers. (A) Double flow-focusing channel for cellulose nanofibril assembly. The cellulose nanofibrils suspension (brown) is injected in the core flow, deionized water (blue) in the first sheath, and acid (green) in the second sheath flows. Arrows indicate the flow direction. Reprinted with permission from Ref. [113]. Copyright 2018 American Chemical Society. (B) The bottom-right schematic reveals the evolution of cellulose nanofibril orientation during the microfluidic-assisted spinning. The cellulose nanofibrils are illustrated as pink rods. The diffusion of Na+, from the NaCl focusing liquid, is illustrated as blue tints. The rows of small images above and below illustrate the hydrodynamical, molecular and electrochemical processes involved. Brownian diffusion is illustrated with the black dashed arrows. The a, b, c and d corresponded to the a, b, c and d region in (A). Hydrodynamically induced alignment is illustrated by grey solid arrows. Reprinted with permission from Ref. [58]. Copyright 2014 Springer Nature. Hydrodynamic and electrostatic interactions at different positions along the channel are illustrated schematically on the right.
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