Genetically Engineered Supercharged Polypeptide Fluids: Fast and Persistent Self-Ordering Induced by Touch

Article abstract of DOI:10.1002/anie.201803169

Mechanically induced disorder–order transitions have been studied in fluid surfactant solutions or polymer thermotropic liquid crystals. However, isothermally induced ordered phases do not persist after cessation of shear, which limits their technological

Full text of DOI:10.1002/anie.201803169

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Accepted Article
Title: Genetically engineered supercharged polypeptide fluids: fast and
persistent self-ordering induced by a touch
Authors: Lei Zhang, Chao Ma, Jing Sun, Baiqi Shao, Giuseppe Portale,
Dong Chen, Kai Liu, and Andreas Herrmann
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To be cited as: Angew. Chem. Int. Ed. 10.1002/anie.201803169
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Genetically engineered supercharged polypeptide fluids: fast and
persistent self-ordering induced by a touch
†
†
Lei Zhang , Chao Ma , Jing Sun, Baiqi Shao, Giuseppe Portale, Dong Chen, Kai Liu*, Andreas
Herrmann*
favorable properties. Therefore, maintaining an ordered state
induced from an isothermal disordered phase in polymer fluids in
absence of an applied shear force remains an important
Abstract: Mechanically induced disorder-order transitions have been
studied in fluid surfactant solutions or polymer thermotropic liquid
challenge.
crystals. However, the isothermally induced ordered phases do not
persist after cessation of shear, which limits their technological
applicability to a great extent. Moreover, no such stimuli-responsive
materials involving biomacromolecules have been reported although
biopolymer liquids are gaining a lot of attention. Here we introduce a
new type of biological fluid system in which anionic polypeptides are
complexed with cationic surfactants. The resulting fluids exhibited
very sensitive isotropic-nematic transition triggered by shear.
Surprisingly, the formed liquid crystal was preserved after cessation
of mechanical stimulus. Self-ordering behavior of the material was
achieved through water flow and finger pressing. The latter
mechanical induction resulted in the formation of complex pattern
that can be read out by birefringence allowing recording fingerprint
Supramolecular self-assembly has attracted considerable
interest for the fabrication of biomacromolecular soft materials.
[
15-17]
For instance, a series of biopolymer LCs and disordered
liquids made of nucleic acids,[18,19] polypeptides,
proteins,[22,23] and virus particles[24,25] have been reported.
However, to the best of our knowledge, no biological fluid that is
characterized by shear-induced disorder-order transition has
been disclosed. Such a new type of stimuli-responsive soft
biomaterial would be very appealing for several reasons. They
would facilitate biophysical measurements for structure
elucidation.[ Cross-linking of building blocks of biological fibers
in the ordered phase might result in biodegradable materials
with appealing mechanical properties. In biocatalysis,
structurally ordered enzymes might show improved catalytic
properties on their biomacromolecular substrates. Finally, the
incorporation of living systems in such type of materials might
lead to dynamic LCs and control of collective microbial
[20,21]
26]
[
27]
behavior. Therefore, the development of biological fluids with
mechanically induced disorder-order transition properties is an
attractive goal.
information.
Phase transitions of materials triggered by external stimuli,
including application of electric fields, magnetic fields,[2] light,[3]
[
1]
Herein, we prepared a new type of peptide-based liquids, which
were formed by electrostatic complexation of supercharged
polypeptides (SUPs) and cationic surfactants that contain an
aromatic azobenzene moiety (AZO). These protein fluids exhibit
fast and persistent self-ordering behavior triggered by different
external shear forces, which thus opens the opportunity for the
construction of force-responsive biodevices.
Supercharged polypeptides with the dominate pentapeptide
repeat motifs (GEGVP) and (GEPVE) were fabricated by
recombinant DNA technology and expressed in E. Coli. In
these SUP sequences, V is valine, P is proline, G is glycine, and
E denotes the negatively charged glutamic acid. Unfolded
peptide backbones with different chain lengths and charge
densities (single charge or double charge per repeat unit) were
produced. The series of negatively charged SUPs was
comprised of E18, EE36, E36, E72, EE108, and E144. E and EE
are abbreviations for the two repeat motifs while the digit
denotes the number of charges of the SUPs, e.g., E18 and
EE36 have the same degree of polymerization but charge
density of EE36 is double compared to E18. Thus, we
successfully achieved the production of SUPs with negative
charges ranging from 18, over 36, 72 and 108 to 144
[
4-6]
[7]
shear, or temperature changes are of great interest because
structural rearrangements within the materials result in abrupt
changes of material properties. Among them, shear-induced
disorder-order transitions in soft polymeric materials have been
extensively investigated because they are important for the
optimization of processing conditions within the oil and plastic
industry as well as for the function and properties of cell
membranes and biological fibers in Nature.[8-14] For instance,
isotropic-nematic (I-N) and isotropic-smectic (I-S) transitions
[28]
were realized in amphiphile micellar solutions[8-11] and
thermotropic liquid crystals (LCs)[
12,13]
under steady shear flow.
However, it is hard to stabilize the resulting ordered phases after
cessation of shear,[
8-13]
which may limit harnessing their
Dr. L. Zhang, Dr. B. Shao, Prof. K. Liu
State Key Laboratory of Rare Earth Resource Utilization, Changchun
Institute of Applied Chemistry, Chinese Academy of Sciences, 130022,
Changchun, China. E-mail: kai.liu@ciac.ac.cn
‖
Dr. L. Zhang, C. Ma, J. Sun, Prof. G. Portale, Prof. A. Herrmann
Zernike Institute for Advanced Materials, Nijenborgh 4, 9747 AG
Groningen, The Netherlands. E-mail: herrmann@dwi.rwth-aachen.de
Dr. L. Zhang
Key Laboratory of Sensor Analysis of Tumor Marker, Ministry of Education,
College of Chemistry and Molecular Engineering, Qingdao University of
Science and Technology, 266042, Qingdao, China.
Prof. D. Chen
(Supporting Information).
Subsequently, we synthesized a cationic surfactant containing a
quaternary ammonium group and a hydrophobic alkyl chain that
are separated by an aromatic azobenzene moiety (Supporting
Information).[29] Both the SUPs and the oppositely charged
surfactant (AZO) were combined in an aqueous solution (Figure
Institute of Process Equipment, College of Energy Engineering, Zhejiang
University, Hangzhou, 310027, China.
‖
Present address: DWI-Leibniz Institute for Interactive Materials,
Forckenbeckstr. 50, 52056 Aachen, Germany and Institute of Technical
and Macromolecular Chemistry, RWTH Aachen University, Worringerweg
1
A). As a result, the solution became turbid (Figure S8A) and
after centrifugation an orange fluid was obtained at the bottom of
the tube (Figure S8B and S8C). After separation from the
2, 52074, Aachen, Germany
†
L. Zhang and C. Ma contributed equally to this work
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supernatant the SUP-AZO complexes exhibited gravity-induced
flow behavior at ambient conditions (Figure S8D and S8E). A
quantitative component determination of the SUP-AZO
complexes was carried out by nuclear magnetic resonance
spectroscopy (NMR). For the E18-AZO complex, a stoichiometry
of the E18 and AZO surfactant was measured to be 1:25 (i.e. ca.
the average diameter of the SUP-AZO complex. Based on a
rough estimation of volumes and comparison between TGA and
SAXS experimental data, the mesogen is composed of hydrated
SUP units of ~2.5 nm thickness separated by regions containing
disordered AZO surfactant molecules of ~1.7 nm thickness.
(Figure 1C, right curve). These results indicated a fast phase
transition from isotropic to nematic ordering of the E144-AZO
fluid material at room temperature, which was triggered by shear
force. Furthermore, glass substrates with parallel rubbing were
used to align the liquid sample for POM investigation. A change
from dark to birefringence was observed only after an
application of shear force (Figure S14). It thus suggests that this
phenomenon did not originate from molecular realignment.
1.4 AZO surfactant molecules per negative charge of the SUP)
(
Figure S9). This indicates that a small number of extra
surfactant molecules is present in the complex.
It should be noted that the long-range ordered lyotropic LC
phase was preserved over time after removal of the external
force (Figure S15). Only heating above 120°C can induce a
transition from the nematic phase to the isotropic state (Figure
S16). These results indicate that the shear-triggered LC phase is
a true low energy state. Furthermore, it was found that the
nematic SUP-AZO system reassembled into a smectic phase
upon water evaporation, and a preferential alignment of the
SUP-AZO complex was observed (Figure S17). Control
experiments involving the SUPs complexed with another type of
surfactant
lacking
the
azobenzene
moiety
(i.e.,
didodecyldimethylammonium bromide) did not show such self-
ordering behavior. Thus, the π-π interactions between adjacent
AZO surfactants organized around the SUP backbone might
play an important role in stabilizing the induced nematic phase in
the absence of an applied mechanical stimulus. Thus this new
class of SUP-AZO liquid materials is unique in regard to its
mechanical response due to its preserved mesophase. This is in
[
8-13]
stark contrast to other shear-triggered polymer fluid systems,
which show induced ordered phases only under shear while
after cessation of shear the isotropic phases are recovered.
Moreover, the isothermal I-N transition properties of the SUP-
AZO fluid materials depend on the molecular weight of the SUPs.
POM investigations of E36, E72, and E144 fluids revealed that
the backbone lengths is reciprocal to the amount of shear
needed for inducing self-ordering necessitating the application of
forces of ~600, ~450, and ~200 kPa, respectively (Figure S18-
S20).
Figure 1. Preparation and characterization of the mechanically responsive
SUP-AZO fluids. (A) SUP fluid materials are formed by electrostatic
complexation of SUPs and AZO surfactants. (B) POM analysis of the shear-
induced I-N phase transition of the E144-AZO sample. The right image with
nematic textures was captured after exertion of shear force. Scale bar is 100
μm. (C) SAXS analysis of the shear-induced I-N transition of the E144-AZO
liquid. The broad diffraction peak at q ≈ 4 nm is due to the kapton, which was
used for sealing of the SUP-AZO fluid samples. The inset represents the
molecular packing model of the nematic phase of the SUP-AZO complex
-
1
(SUPs are represented in blue, surfactant head groups in green and the
hydrophobic part of the surfactant in grey).
Further
characterization
of
the
liquid
material
by
thermogravimetric analysis (TGA) showed that the hydrophobic
SUP-AZO complexes exhibit water contents of 50-60 % (w/w)
(Figure S10). The water-rich polypeptide liquid droplet could be
easily transferred to a glass slide by a pipette to conduct
polarized optical microscopy (POM) and conoscopy analysis. In
order to avoid water evaporation, a cover glass was used and all
the glass edges were sealed by a plastic film. No birefringence
was observed in case of the E144-AZO fluid (Figure 1B, left
image and Figure S11). The absence of any diffraction pattern
as seen by small-angle X-ray scattering (SAXS) (Figure 1C, left
curve; Figures S12 and S13) combined with POM and
conoscopic microscopy (Figure S11) suggests that no ordered
structures are present within the E144-AZO complex and no
alignment was induced by the substrates. However, once a
small pressing force (~200 kPa) was exerted on the glass cover
slip, the sample immediately became birefringent and typical
nematic textures were observed (Figure 1B, right image). The
corresponding SAXS profile showed one broad diffraction peak
corresponding to a d spacing of 42.0 Å, which was attributed to
Figure 2. Investigation of the fluid behavior of the SUP-AZO fluids by a shear
rheometer. (A, B) Storage (G’) and loss (G’’) moduli curves as a function of
time with a frequency of 1 Hz and a strain of 1. The increased store moduli
with shear are marked with red dotted line. (C) POM analysis of the E144-AZO
fluid material before the application of shear force. (D) POM analysis of the
E144-AZO sample after applying shear for 6 min. The image was captured
after cessation of shear. Scale bar is 100 μm.
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Fluid behavior of the SUP-AZO complexes was further
investigated by a shear rheometer. G’’ was found to be higher
than G’ over the time course of the experiment (Figures 2A and
Motivated by the above results we made the attempt to generate
complex pattern induced by shear forces. Therefore, we applied
the device described above to record fingerprint information by
touching the thin tape surface with the tip of different fingers. It
was found that shear-induced I-N transition took place within
only 1-2 sec of pressing (~100 kPa) and the resulting pattern of
birefringence textures was in agreement with the corresponding
fingerprint (Figure 4A and 4B). Characteristic LC textures were
collected for different fingers (Figure 4B-4D). This suggests that
various fingerprint types (i.e., arch, loop and whorl) controlled
the orientation of the SUP-AZO molecules and thus determined
the appearing birefringence patterns of the fluid material.
2
B), indicating liquid-like behavior.[22] However, the values of the
storage moduli increased with shearing for about 5 min of the
E144-AZO liquid (Figure 2A, marked with red dotted line).
Notably, POM investigation indicated a phase transition from
isotropic to nematic state during this process (Figure 2C and 2D).
This indicates that the shear-induced nematic structure is
responsible for the increase of storage moduli. In case of E72-
AZO complex, mechanical moduli are lower than for E144-AZO
due to the deceased SUP molecular weight. But similar behavior
was detected only after 10 min (Figure 2B). These results on the
one hand suggest that the storage moduli of the fluid materials
are associated with the shear-induced I-N transition. On the
other, they indicate that the mechanical sensitivity of the I-N
transition of the materials is determined by mechanical moduli of
the materials. The higher mechanical moduli of the samples with
increased molecular weight result in easier realization of I-N
transition.
Figure 4. Investigation of the isotropic-LC phase transition of the SUP-AZO
fluids triggered by finger pressing. (A) Photograph of
a simple device
containing the SUP-AZO materials used for recording fingerprints. (B-D) Three
fingers with different fingerprint types were applied to induce the LC phase of
the E144-AZO liquid materials. Specific birefringence patterns display the
different fingerprints. Scale bar is 500 μm. Due to the high magnification of the
polarized optical microscope in our laboratory, only small parts of the recorded
fingerprints can be shown but the whole fingerprints cannot be visualized in a
single image. (E, F) Two consecutive experiments to illustrate the
reproducibility of the fingerprint-induced birefringence textures in the SUP-
AZO fluids. Note, the weak “background” birefringence in B-F originated from
the plastic films.
Figure 3. Investigation of water flow-induced phase transition of the SUP-AZO
fluids. (A) Photograph of a simple device for detection of water flow. The
E144-AZO sample was injected on a glass slide and sealed with a plastic film
by double sided sticky tape. (B) POM analysis of the sample before the
application of water flow. (C) Photograph of the applied water flow at a rate of
Furthermore, two consecutive experiments were carried out to
illustrate the reproducibility of finger imprint on the SUP-AZO
liquid material (Figure 4E and 4F). It was demonstrated that
virtually the same pattern was obtained for the same region of
the fingertip. Therefore, the fast self-ordering behavior of the
polypeptide soft material system triggered by external force
provides a simple concept for recording of fingerprint information
and individuals identification. Moreover, this strategy largely
differs from reported methods for fingerprint recognition. It does
not require the application of ink nor does it require,
electrochemiluminescence, photoluminescence, or plasmonics
as read-outs.[30,31]
A new type of mechanically responsive polymer fluids based on
genetically engineered supercharged polypeptides and
azobenzene surfactants has been developed. An isothermal
phase transition from the isotropic liquid phase to the nematic
ordered state was realized by mechanotransduction. In stark
contrast to previously reported shear-induced liquid systems, the
triggered nematic lyotropic LC state is maintained in the SUP-
40 mL/sec (water pressure 0.35 kPa, nozzle diameter 0.8 cm) on the device
containing E144-AZO material. (D) POM analysis of the formed birefringence
textures of the SUP-AZO liquid (5 minutes water flushing). The image was
captured after cessation of the water stream. Scale bar is 100 μm.
To show the generality of mechanical response of the SUP-AZO
fluids with regard to other external shear forces, water flow was
employed to induce the I-N transition. 10 µL of the E144-AZO
complex liquid was loaded on a glass slide and sealed with a
thin plastic film by double sided glue tape (Figure 3A). The
primitive device gave no birefringence without water flow and the
active material remained in its disordered state (Figure 3B).
Upon flushing water at a flow pressure of 0.35 kPa over the thin
tape (Figure 3C), an orientated LC texture was observed (Figure
3
D). This indicated the successful realization of fast self-ordering
behavior of the SUP-AZO complexes by a stream of water within
min. When the flow pressure was decreased to 0.15 kPa, no
5
birefringence was observed (Figure S21), suggesting that the I-
N phase transition is sensitive to the shear strength induced by
the water flow.
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flows induce a phase transition in the SUP-AZO complexes
enabling the recording of the resulting LC birefringence as
reliable signal to distinguish different flow pressure. Moreover,
active SUP-AZO complex fluid layers allow the ink-free transfer
of complex pattern as obtained for fingerprints, which are
translated into easily recordable birefringence read-outs. In the
future, we will investigate further the mechanism of maintaining
the ordered lyotropic LC phase without exerting force and we will
exploit these materials to generate more complex dynamic
systems responding to light, catalytic turnover or biomolecular
recognition events.
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COMMUNICATION
COMMUNICATION
Lei Zhang, Chao Ma, Jing Sun,
Giuseppe Portale, Kai Liu*, Andreas
Herrmann*
Page No. – Page No.
Genetically engineered supercharged
polypeptide fluids: fast and persistent
self-ordering induced by a touch
Stimuli-responsive protein fluids: a new type of bio-based fluids exhibiting shear-
induced phase transitions have been generated by electrostatic complexation of
supercharged polypeptides with aromatic surfactants. This sensitive, fast, and
persistent self-ordering behaviour was exploited for water flow detection and
capturing of fingerprints information by easily recordable birefringence.
This article is protected by copyright. All rights reserved.