Feeding Single-Walled Carbon Nanotubes or Graphene to Silkworms

Letter pubs.acs.org/NanoLett

Feeding Single-Walled Carbon Nanotubes or Graphene to Silkworms for Reinforced Silk Fibers Qi Wang, Chunya Wang, Mingchao Zhang, Muqiang Jian, and Yingying Zhang* Department of Chemistry and Center for Nano and Micro Mechanics, Tsinghua University, Beijing 100084, PR China S Supporting Information *

ABSTRACT: Silkworm silk is gaining significant attention from both the textile industry and research society because of its outstanding mechanical properties and lustrous appearance. The possibility of creating tougher silks attracts particular research interest. Carbon nanotubes and graphene are widely studied for their use as reinforcement. In this work, we report mechanically enhanced silk directly collected by feeding Bombyx mori larval silkworms with single-walled carbon nanotubes (SWNTs) and graphene. We found that parts of the fed carbon nanomaterials were incorporated into the as-spun silk fibers, whereas the others went into the excrement of silkworms. Spectroscopy study indicated that nanocarbon additions hindered the conformation transition of silk fibroin from random coil and α-helix to β-sheet, which may contribute to increased elongation at break and toughness modules. We further investigated the pyrolysis of modified silk, and a highly developed graphitic structure with obviously enhanced electrical conductivity was obtained through the introduction of SWNTs and graphene. The successful generation of these SWNT- or graphene-embedded silks by in vivo feeding is expected to open up possibilities for the large-scale production of high-strength silk fibers. KEYWORDS: Silkworm silk, carbon nanotubes, graphene, mechanical property, carbonization

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wet-spinning process,18 which involves the utilization of strong acids or organics. There is also an attempt to obtain reinforced silk through an in situ functionalization approach, in which MWNTs with diameters around 30 nm were fed to silkworms. Obviously, single-walled CNTs (SWNTs) with diameters around 1−2 nm are more suitable for incorporation into the crystalline structures of silk fibroins. Besides, GR, the new family of carbon materials, is also a potential reinforcer due to its atomic thickness, excellent mechanical properties, and abundant production. Recently, it was reported that a mechanically reinforced spider silk was obtained by spraying spiders with SWNTs and GR aqueous dispersions,19 although whether the incorporation occurred postspinning or in situ remains unclear. Obviously, the practical production of spider silk is challenging because of the territorial and cannibalistic natural instincts of most spiders.20 In contrast, silkworms are gentle and can be raised in a large scale. However, the in vivo incorporation of SWNTs and GR into silkworm silks has not been explored. In this work, we fed Bombyx mori silkworms with diets containing carbon nanomaterials (SWNTs or GR) and directly obtained intrinsically reinforced silkworm silk fibers. The obtained silk showed enhanced mechanical properties with superior fracture strength and elongation-at-break, demonstrating the validity of the production of reinforced silk fibers by feeding diets through a natural process. We analyzed both

atural biomaterials are of considerable interest because of their superior properties and ecological friendliness. In particular, silkworm silk, as a type of mass-produced natural protein resource, is gaining significant attention from the textile industry and research society because of its outstanding mechanical properties (high modulus, high fracture strength, and exceptional extensibility), lustrous appearance, biocompatibility, and large-scale production.1−3 To enhance silk performance, various functional components such as dyes,4,5 fluorescent proteins,6 antimicrobial agents,7 metal and semiconductor nanoparticles, and conductive polymers8,9 have been incorporated into silk. A pair of strategies are used to prepare functionalized silk fibers (i.e., postfunctionalization and in situ functionalization). Traditional postfunctionalization approaches have facilitated the production of high-strength silk fibers from regenerated silk fibroin solution with additives through dry or wet spinning.10,11 These approaches inevitably require the use of toxic chemical solvents and complex, multistep procedures. In contrast, recently developed easy and green in situ functionalization approaches enable the production of functionalized silk fibers by directly feeding specific diets to silkworms.12 Carbon nanotubes (CNTs) and graphene (GR), which possess superior mechanical properties, are widely applied as reinforcement in preparing high-performance materials.13−16 In particular, several attempts have been undertaken to incorporate CNTs into silk to further enhance the mechanical properties of silk. For example, reinforced regenerated silk fibers have been prepared from multiwalled CNT (MWNT)− silk fibroin mixture solutions by the electrospinning17 or the © 2016 American Chemical Society

Received: August 26, 2016 Published: September 13, 2016 6695

DOI: 10.1021/acs.nanolett.6b03597 Nano Lett. 2016, 16, 6695−6700

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Figure 1. As-spun silk fibers reinforced with SWNTs or GR. (a) Schematic showing the natural process to incorporate SWNTs or GR into silk by feeding silkworms with mulberry leaves spray-coated with SWNT or GR solutions. (b) Photographs of the as-obtained typical cocoons from silkworms fed with five different diets, showing no observable difference. (c−g) SEM images showing the morphology of degummed silk fibers corresponding to cocoons shown in (b). Scale bars: 5 μm. (h) Stress−strain curves of degummed silk fibers. The error bars show the standard deviation of elongation at break (horizontal axis) and fracture strength (vertical axis).

silk fibers from the obtained cocoons reveal similar morphology of silk fibers (Figure 1c−g and Table S1), indicating that feeding of SWNTs and GR does not exert apparent influence on fiber morphology. The obtained SWNT1-S and GR1-S showed considerably improved mechanical properties with fracture strength and elongation-at-break of 0.59 GPa and 12.59% for SWNT1-S and 0.57 GPa and 10.33% for GR1-S, which distinctly exceeds that of the control-S with 0.36 GPa and 9.39%, as shown in Figure 1h (see detailed data in Tables S2−S6). Evidently, the toughness modulus, which is defined as the area under the stress−strain curve, is 4.82 GJ m−3 for SWNT1-S, exhibiting a 2.12-fold increase in comparison with that of control-S. Similarly, the toughness modulus of GR1-S, 3.80 GJ m−3, is considerably higher than that of control-S. However, SWNT2-S and GR2-S, which should contain more nanofillers, both exhibit a low fracture strength of 0.28 GPa and low elongation-at-break of 5.76% and 3.95%, respectively. These findings indicate that excessive incorporation of carbon nanomaterials leads to deteriorated mechanical properties of silk fibers. Table 1 shows a summary of the mechanical properties of the obtained fibers. Noted that the previously reported fracture strength of silk fibers is in the range of 0.3−0.7 GPa, and the elongation at break is in the range of 4−26%,6,21−24 indicating a large

dissolved silk fibers and silkworm excrement by Raman spectra and confirmed the incorporation of parts of fed carbon nanomaterials into the as-obtained silk fibers. In addition, the influence of carbon nanomaterials on the crystalline structures of the as-obtained silks was characterized and analyzed. Furthermore, the structures of carbonized silk fibers were analyzed to further confirm the incorporation of carbon nanomaterials into the silk fibers. Figure 1a illustrates the strategy to obtain intrinsically reinforced silkworm silk fibers by feeding larval silkworms with mulberry leaves sprayed with SWNTs or GR dispersion solutions. SWNTs or GR were uniformly dispersed in deionized water with the assistance of a surface-active agent named calcium lignosulfonate (LGS). Diets containing SWNTs (two kinds) and diets containing GR (two kinds) were prepared by spraying fresh mulberry leaves with SWNTs or GR solutions with different concentrations. The silk fibers obtained by feeding diets containing SWNTs with solution concentration of 0.2 and 1.0 wt % and GR at the concentration of 0.2 and 2.0 wt % were denoted by SWNT1-S, SWNT2-S, GR1-S, and GR2-S, respectively. A diet with only LGS was also prepared for raising silkworms as a control group, which was denoted as control-S. A total of 100 Bombyx mori silkworms divided into five groups were raised from their third instars to spinning periods by feeding with the previously mentioned five kinds of diets. No differences between the silkworms fed with different diets were observed until cocoons were produced, indicating that diets containing small proportion of SWNTs and GR used in this study are safe for raising silkworms. Figure 1b shows photographs of the as-obtained cocoons, which exhibit similar colors and uniform sizes. Before further characterization, all the silk cocoons are degummed to completely remove the sericin coating on the silk fibers. Scanning electron microscopy (SEM) images of the degummed

Table 1. Mechanical Properties of Degummed Silk Fibers

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sample

fracture strength [GPa]

elongation at break [%]

toughness modulus [MPa]

control-S SWNT1-S SWNT2-S GR1-S GR2-S

0.36 0.59 0.28 0.57 0.28

9.39 12.59 5.76 10.33 3.95

22.7 48.24 10.33 38.04 6.40 DOI: 10.1021/acs.nanolett.6b03597 Nano Lett. 2016, 16, 6695−6700

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Figure 2. Raman spectra of the nanocarbons in the silk fibers and excrements of silkworms fed with the diets compared to the spectra of the original nanocarbons. (a) Raman spectra obtained from the SWNT1-S precipitation after dissolving the silk fibroin, the excrements of silkworms fed with the diet, and the original SWNTs. (b) Raman spectra obtained from the GR1-S precipitation after the dissolution of silk fibroin, excrements of silkworms fed with the diet, and the original GR.

Figure 3. Influence of SWNT or GR additives on the crystalline structure of silk fibroin fibers. (a) FTIR spectra of degummed silk fibroin of the five kinds of silk samples. (b) Content of secondary structures in different silk samples obtained according to the amide I band in FTIR spectra. (c) Schematic illustration showing the interactions between SWNT and silk fibroin and between GR and silk fibroin, respectively (PDB of fibroin heavy chain is 3UA0).

that some of the SWNTs fed to the silkworms were successfully incorporated into the silk fibers, while others went into the excrement. The similar position and intensity ratio of the Raman spectra of SWNTs in Figure 2a indicate that whether in silkworm excrements or in the silk, the nanocarbon materials keep their original morphology and properties without observable change, which could be ascribed to the high chemical and physical stability of the SWNTs. Figure 2b, which corresponds to the Raman spectra of GR, shows similar results. Natural silkworm silk-spinning processes involve the conversion of helical and random coils to β-sheet structures as the concentration of silk fibroin increases. Under the action of shear and drawing stress, the fibroin solution is converted into solid filaments.26−28 Because the mechanical properties of silk fibers are highly related to the secondary structure, which

variability from sample to sample that may derive from difference in raising environment of silkworms, degumming process, testing parameters and analysis approaches. Thus, we only compared the mechanical properties of our silk fibers obtained with the same raising environment in this study. The SWNTs or GR in the diets are partially incorporated into silk fibers through the natural process, which is confirmed by the Raman spectra of silkworm excrement, as well as silk cocoons. Figure 2 shows the Raman spectra of the nanocarbons obtained from silkworm excrement and silk fibers (see detailed sample preparation in the Methods section and the spectra of controlled samples in Figure S1). Raman features corresponding to SWNTs, including the radial breathing mode (RBM) peak, D-band (∼1350 cm−1), G-band (∼1580 cm−1), and G′band (∼2700 cm−1),25 could be seen in Figure 2a, indicating 6697

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Figure 4. Structure and electrical conductivity of carbonized silk fibers with and without SWNTs or GR. (a,b) Raman spectra of carbonized silk fibers showing the influence of SWNTs (a) and GR (b) on graphitization degree. (c−g) High-resolution TEM images of carbon structures derived from control-S, SWNT1-S, SWNT2-S, GR1-S, and GR2-S fibers, respectively. Scale bars: 10 nm. (h) Electrical conductivity of carbonized silk fibers derived from different samples.

consists of helical and random coils, β-sheet, and β-turn, the toughness and extensibility of silk fibers can be tuned through adjusting the proportion of the secondary structure of silks. Fourier transform infrared spectroscopy (FTIR) is one of the most powerful and nondestructive techniques for studying the secondary structure of silk fibroin.29,30 Figure 3a shows the secondary derivative spectra of the degummed silk fibroin of different silk samples. The peaks centered at 1698 cm−1 are classified as β-turn. Quantitative analysis was carried out through investigating the spectral region corresponding to the amide I (1600−1 and 700 cm−1). The Knights assignment was adopted to ascertain the adsorption characteristic peaks.31−33 The absorption peak around 1647 cm−1 is attributed to the random coil or helical conformation or both. The peaks from 1615 to 1640 cm−1 are related to the β-sheet structure. The content of secondary structures and deconvolution details in different silk samples are shown in Figures 3b and S2, revealing that the SWNT and GR modified silks contained more α-helix and random coil structures and fewer β-sheets than controlled silk. On the basis of the above observations, we suppose that the presence of SWNTs or GR in the silk matrix may hinder the transformation of α-helix and random coils to β-sheet structures, which could be attributed to steric hindrance effects and noncovalent interactions between nanocarbon materials and silk fibroin through physisorption. It is reported that, in physiological environments, amino acids can possess partial charges in amine and carboxylate ends, and the dipolar nature of amino acid may contribute to a stronger van der Waals interaction between the zwitterionic amino acid and SWNTs and GR in the adsorption process.34,35 Figure 3c illustrates the structures of SWNT- or GR-modified silk. Given that the α-

helix and random coil conformation consists of easily movable chains,36−38 it is expected the higher content of α-helix and random coil in SWNT1-S and GR1-S silk fibers could lead to larger breaking elongation and higher toughness modules in comparison with the control-S fibers. Besides, SWNTs or GR in the silk matrix could act as “knots”. The slipknot structure, which is widely found in biological structures such as proteins and DNA strands,39,40 performs a key function as a frictional element to reshape the constitutive law of fiber and dissipate the additional fracture energy, also leading to increased breaking elongation. However, with excessive SWNTs and GR in the silk, these nanofillers may aggregate and act as defects, resulting in low fracture strength and a low percentage of elongation. To further confirm the existence of carbon nanofillers in the as-spun silk as well as to investigate the influence on the silk structures, we carbonized the as-spun silk fibers and performed more characterization steps. Nanocarbon materials carbonized from natural biomaterials have attracted marked interest because of their high electrical conductivity, flexibility, and the facile and green fabrication approach.41−45 The B. mori silk containing rich β-sheet conformations could reconstruct to a carbonaceous solid with sp2-hybridized hexagonal structures when treated in an inert atmosphere.43,46−49 We surmised that the presence of SWNTs or GR in silk fibers may induce enhanced graphitization of nearby silk fibroin under thermal treatment. We treated the control-S, SWNT1-S, SWNT2-S, GR1-S, and GR2-S at 1050 °C in Ar and then compared the structures and electrical conductivities. Panels a and b of Figure 4 show the Raman spectra of the carbonized silk fibers. The Gband around 1580 cm−1 corresponds to the sp2 graphite structure, while the D-band around 1350 cm−1 is related to 6698

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ultrasonication for 180 min and centrifuging at 15 000 rpm. A solution containing only 5 g of LGS was also prepared as the control group. The obtained solutions were uniformly sprayed on fresh mulberry leaves using an airbrush, which were then used as diets for silkworms directly. A total of 100 Bombyx mori silkworms in third instars were divided into five groups and raised under a condition of 25 °C and relative humidity of 20% by feeding the diets. Preparation of Degummed Silk Fibers. The obtained cocoons were cut into pieces and boiled three times in an aqueous solution of Na2CO3 for 30 min and then rinsed thoroughly with DI water. The collected degummed silks were dried at 70 °C in an oven for 6 h. Characterization. SEM characterization was carried out using a FEI Quanta microscope operated at 10 kV. Raman spectra were recorded at room temperature using a 532 nm laser (HORIBA Evolution). For Raman measurements of nanocarbons in the silk fibers, 30 mg of degummed silk fibers were dissolved in 5 mL of concentrated nitric acid. The obtained solutions were diluted 20 times by DI water and then treated using ultrasonication. Vacuum filtration was used to remove the dissolved silk fibroin, and the spectra were taken from the precipitation left on the filter papers. Besides, the Raman spectra of silkworm excrement in Figure 2 are normalized with respect to the strongest peak of 1615 cm−1 in control-S excrements (Figure S1), and then the normalized control-S excrement spectra is subtracted to present the spectra clearly. FTIR was carried out on a Nicolet 6800 FTIR spectrometer with a diamond attenuated total reflectance accessory. The spectra were obtained with a resolution of 4.0 cm−1. The protein secondary structure contents were calculated by performing Fourier deconvolution over the amide I region (1600−1700 cm−1) and integrating the peak area. The strain− stress curves were measured using degummed silk fibers with a gauge length of 10 mm and at a rate of extension of 1.0 mm min−1 with a SHIMADZUAG-IS tensile tester. A total of 100 fibers (5 randomly selected fibers for each cocoon and 20 cocoons for each group) were measured for statistical analysis. The thermal degradation of silk fibers was measured by thermogravimetric analysis (TGA) from 30 to 800 °C in N2 (99.99%) at a scanning speed of 5 °C/min. Figure S3 shows the results. Carbonization of Silk and Characterization. The degummed silk fibers were heated in a tube furnace with Ar atmosphere (100 standard cubic centimeter per minute of 99.9992% Ar) using the following heating schedule. The silk fibers were heated to 150 °C for 120 min to remove water and then heated to 350 °C (5 °C min−1) and kept for 180 min to form the incipient conjugated carbon structure. Afterward, the temperature was increased from 350 to 1050 °C at a rate of 2 °C min−1 and maintained for 120 min to induce the stacked polyaromatic carbon microstructures to graphitic structures. TEM and Raman spectra analysis were carried out on the obtained samples, as mentioned before. The carbonized samples were ground and dispersed in ethanol, and the samples were then dropped on TEM grids for characterization. Highresolution TEM images were recorded using a TEM (Titan 80−300, FEI). The electrical conductivity of carbonized silk fibers was measured at 25 °C using a two-probe method (2400, Keithley).

defects in the carbon materials. The intensity ratio of the Dband to the G-band (ID/IG), which decreases with increasing degree of graphitization, is an indicator of graphite crystalline degree.50 The ID-to-IG ratio of carbonized SWNT1-S, SWNT2S, GR1-S, and GR2-S are all lower than that of the carbonized control-S fiber. Both the addition of SWNTs or GR, which have intrinsic strong G peaks in the fibers, and the enhanced graphitization of silk fibers during reconstruction due to the template effect of SWNTs or GR could lead to the decrement of the ID-to-IG ratio. The atomic-scale morphologies of carbonized SWNTs−GR silk revealed by transmission electron microscopy (TEM) are consistent with the above Raman results. Compared with the amorphous graphite of the carbonized controlled-S fibers(Figure 4c), the carbonized SWNT−GR silk fibers show regions with highly ordered graphitic structures, which exhibit an interlayer spacing of d002 = 0.34 nm (Figure 4d−g). In addition, we measured the electrical conductivity of carbonized silk fibers. As shown in Figure 4h, the carbonized SWNT2-S, GR2-S, SWNT1-S, and GR1-S silk fibers showed evidently enhanced electrical conductivity in comparison with that of the carbonized control-S fiber. This enhancement could be attributed to the increased degree of graphitization of the samples containing SWNTs or GR. In summary, we demonstrated that mechanically enhanced silk fibers could be naturally produced by feeding silkworms with diets containing SWNTs or GR. The as-spun silk fibers containing nanofillers showed evidently increased fracture strength and elongation-at-break, demonstrating the validity of SWNT or GR incorporation into silkworm silk as reinforcement through an in situ functionalization approach. By analyzing the silk fibers and the excrement of silkworms, we conclude that parts of the fed carbon nanomaterials were incorporated into the as-spun silk fibers, while others went into excrement. FTIR spectroscopy of silks showed that SWNTand GR-modified silks contained more α-helix and random coil structures and fewer β-sheets than controlled silk. This composition may contribute to increased breaking elongation and toughness modules, as the coil conformation consists of more movable chains than β-sheet. Besides, the SWNTs and GR may work as “slipknots,” leading to increased breaking elongation. We further investigated the influence of the carbon nanofillers on the structures and electrical conductivity of carbonized silk and found that the introduction of SWNTs or GR promoted silk graphitization. This natural feeding strategy could be easily scaled up, paving a new path for the production of supertough silk fibers at a large scale. It is worth noting that there are still several interesting and important questions that cannot be answered by our current work, such as what is the safety limit of nanocarbons in the diets for the silkworms, how much of the nanocarbons taken by the silkworms are incorporated into the silk, and what is the detailed biological process. Further studies regarding these interdisciplinary questions will be very interesting and valuable. Methods. Preparation of Diets and Feeding of Silkworms. SWNTs were grown with chemical vapor deposition. The diameters of the SWNTs are in the range of 1−2 nm, and the length is in the range of 10−30 μm. Graphene nanoplates with a thickness of 6−8 nm and a width of 5 μm were purchased from J & K Scientific Ltd., China. To prepare the solutions, SWNTs (0.2 and 1 g) and GR (0.2 and 2 g) were mixed with 5 g of LGS in an agate mortar, respectively. Then, deionized (DI) water (100 mL) was added to each sample, followed by 6699

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.nanolett.6b03597. Tables showing the average diameters of different silk fibers and the mechanical properties of degummed fibers. Figures showing the deconvolution of FTIR spectra in amide I band of five different silks and TGA curves and first-derivative plots of the TGA. (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the NSF of China (51672153, 51422204, and 51372132) and the National Key Basic Research and Development Program (2016YFA0200103 and 2013CB228506).

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REFERENCES

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DOI: 10.1021/acs.nanolett.6b03597 Nano Lett. 2016, 16, 6695−6700