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Chiral Metamolecules with Active Plasmonic Transition Tiantian Man, Wei Ji, Xiaoguo Liu, Chuan Zhang, Li Li, Hao Pei, and Chunhai Fan ACS Nano, Just Accepted Manuscript • DOI: 10.1021/acsnano.9b01942 • Publication Date (Web): 09 Apr 2019 Downloaded from http://pubs.acs.org on April 9, 2019

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Chiral Metamolecules with Active Plasmonic Transition Tiantian Man,† Wei Ji,† Xiaoguo Liu,‡ Chuan Zhang,*,‡ Li Li,† Hao Pei,*,† and Chunhai Fan*,‡ †Shanghai

Key Laboratory of Green Chemistry and Chemical Processes, School of Chemistry

and Molecular Engineering, East China Normal University, 500 Dongchuan Road, Shanghai, 200241, P. R. China ‡School

of Chemistry and Chemical Engineering, Shanghai Jiao Tong University, Shanghai

200240, China

ABSTRACT: Energy-dissipating self-assembly is at the basis of many important cellular processes, such as cell organization, proliferation and morphogenesis. Beyond equilibrium selfassembled molecular systems and materials, it is increasingly recognized that the control of assembly kinetics provides great opportunity for the next generation of molecular materials with intelligent behavior including programmed spatiotemporal organization. Here we show the transient self-assembly of active chiral plasmonic metamolecules (CPMs), which controlled by the proton flux generated from a positive-feedback chemical reaction network (pCRN). The fuelconversion kinetics allows for temporal control and adaptive tuning of multiple structures of plasmonic metamolecules (PMs). This approach enables autonomous tuning of chiroptical properties of metamolecules with dynamic behavior. Moreover, we show that 11-type spatial configurations of PMs are assembled, and 9-type temporal configurations CPMs are differed.

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KEYWORDS: chiral metamolecules, DNA nanotechnology, plasmonic, transient self-assembly, chemical reaction network Nature has developed functional out-of-equilibrium systems such as active self-assembly of microtubules and actin networks, which play an important role in life-distinguishing features.1 These active assemblies are regulated by continuous energy consumption to remain in far from thermodynamic equilibrium and carry out work.2 Such living biological systems provide deep inspirations to create artificial active systems with kinetically controlled dynamics and associated spatiotemporal features that cannot be obtained in equilibrium.3-6 They would provide a promising designable approach for the next generation of molecular materials with intelligent behavior in adaptive materials, drug delivery, and active separation.7-9 In the field of active plasmonics, there is significant interest in dynamic structural control of PMs since it is highly promising to implement active plasmonic devices, such as nano-optical modulators, transducers, switches, and filters.10,

11

The approach involving structural

reconfiguration usually requires precise control over the building blocks’ positions at the nanoscale.12-16 DNA self-assembly exploiting the inherent molecular recognition and programmability offers great designing potential for structural tuning of plasmonic nanostructures.17-24 Recent advances have developed few active plasmonic systems based on responsive DNA nanostructures with great success for regulating spatial configuration in response to oligonucleotide, light, and pH stimuli.25-28 However, only switchable control of active plasmonic systems in equilibrium conditions have been investigated to date. Temporal control and autonomous adaptive tuning of multiple structures of PMs in non-equilibrium conditions has not yet been demonstrated. These transient assembling systems that controlled by the kinetics of fuel conversion could serve as prototypical building blocks for further developments in active


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plasmonics with promising potential in realizing autonomous life-like functionality and complexity in continuous time and space. Herein, we experimentally demonstrate the transient self-assembly of active CPMs, in which lifetime and regenerative behavior can be modulated by fuel-conversion kinetics. The conceptual framework underlying transient self-assembly is orchestrating at least two antagonistic reactions to produce a nonlinear environment change.7 To realize non-equilibrium assembly in an autonomous way, we coupled a proton-responsive PMs to a pCRN as shown in Figure 1. External chemical energy input by increasing proton flux activated the building blocks via protonation of the cytosine-rich DNA strands on AuNRs, which then readily self-assembled onto a tetrahedronshaped DNA origami template. A deactivation reaction then occurred via a concurrent pathway, thereby triggering the disassembly process. To make the self-assembling metamolecules transform in an autonomous way, the activation and deactivation processes were chemically decoupled by pre-programming the environmental conditions (pH) with a pCRN, which temporally remodeled the energy landscape of the self-assembly system that induced the transient assembly.


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Figure 1. Scheme of non-equilibrium self-assembly of active plasmonic metamolecules. External energy input activates the building blocks via protonation of the cytosine-rich DNA strands on gold nanorods (AuNRs), which then self-assemble readily onto DNA template. A deactivation reaction then occurs via a concurrent pathway, thereby triggering the disassembly process. The activation and deactivation processes are chemically decoupled by pre-programming the environmental conditions (pH) with a pCRN. RESULTS AND DISCUSSION Fabrication of plasmonic metamolecules with different spatial configurations. First, we design a tetrahedron-shaped DNA origami template, which is folded from a long single-stranded M13 viral genomic DNA with a set of 214 short staple strands (Table S1) through sequencespecific hybridization. Each edge of the DNA tetrahedron composes of a six-helix bundle with a length of ~66 nm. Seven single-stranded (ss)DNA linker (Tables S2 and S3) extending from each edge of the DNA tetrahedron can be used to bind AuNRs modified with their complementary ssDNA when necessary. To describe the assembling system with DNA tetrahedron, a symbol of Rn (x1, x2…, xm) is used to represent their varied configurations, where n represents the number of assembled AuNRs and xm represents the encoded edge of DNA tetrahedron. 11 types of assembled metamolecules can be achieved by permutation and combination of (n, m). Schematic models are shown in Figure 2, including R1(x2), R2(x2, x4), R2(x2, x5), R3(x1, x2, x4), R3(x2, x4, x5), R3(x2, x4, x6), R3(x2, x3, x4), R4(x2, x3, x4, x5), R4(x2, x3, x5, x6), R5(x2, x3, x4, x5, x6), and R6(x1, x2, x3, x4, x5, x6). There are four possible structural isomerides of R3 type, wherein R3(x1, x2, x4) and R3(x2, x4, x5) are chiral isomers. In the case of R2 type and R4 type, they both have two possible structural isomerides. Transmission electron microscopy (TEM) was used to characterize the assembled PMs. TEM images in Figure 2 reveal the successful assembly of 11-type different


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metamolecules (Figure S1 for AuNRs and Figure S2 for DNA origami template). Although negative TEM can cause the collapse of the assembled nanostructures, the edge of DNA nanostructures and the AuNRs at the designed position could still be seen clearly, confirming that we successfully assembled 11-type different PMs. Note that the collapse became more severe in TEM imaging as the number of assembled AuNRs was increased, which is due to the hydrophobic drying force during the TEM sample preparation. Moreover, the absorbance of the assemblies gradually increased as more AuNRs were immobilized onto DNA origami (Figure S3). There was only weak surface plasmon resonance (SPR) coupling between the immobilized AuNRs due to relatively large distance, therefore resulting in negligible SPR peak shift in UV-Vis spectra.

Figure 2. Self-assembly of plasmonic metamolecules using a tetrahedral DNA origami and AuNRs. AuNRs modified with ssDNA can be assembled at designed binding sites of tetrahedron-


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shaped DNA origami to form 11 types of plasmonic metamolecules, which were demonstrated by representative TEM images of 3D metamolecules with different spatial configurations. Scale bars: 50 nm. Experimental and theoretical characterizations of the proton-responsive reconfigurable CPMs. In this work, we chose two kinds of triplex DNA segments with different TAT/CGC contents that are sensitive to pH = 7.2 and pH = 6.6 (Tables S3 and S4) respectively to reconfigure CPMs. Figure 3A demonstrates the working principle of pH-sensitive DNA triplex, which is formed through sequence-specific parallel Hoogsteen interactions (dots) between a pH-sensitive ssDNA and a pH-insensitive DNA duplex with Watson-Crick base pairings (dashed).27, 29 The DNA triplex segment for controlling AuNRs consists of a duplex located on the struts of x1 and x5 of DNA origami template and a thiolated ssDNA modified on AuNR (L-thiolated ssDNA or Rthiolated ssDNA), by which we could control the pH-regulated triplex formation and trigger conformational changes from Off-state to L-state or R-state of metamolecules (Figures 3C and 3D). This proton-responsive reconfiguration was reflected in the morphology of resultant nanostructures, as demonstrated by TEM imaging. We also carried out circular dichroism (CD) measurements to characterize the optical properties of the assembled CPMs. As displayed in Figure 3B, the R-R3(x2, x4, x5) generates a characteristic bisignate CD signal with a dip-peak profile (blue line); whereas L-R3(x1, x2, x4) produces a mirror-symmetric peak-dip CD signal (red line), indicating they are indeed a pair of CPMs. Next, in order to gain deeper insights into the mechanism of the chirality of the obtained CPMs, finite-element simulations (using the COMSOL Multiphysics software package) was carried out on the CPMs consisting of pure AuNRs but without the DNA origami template.18, 30 For simplicity, the AuNR was modeled as a cylinder with two hemispherical caps at both ends (Figure S4), and only the situation that circularly polarized


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light (CPL) propagates on the perpendicular direction to the x2 and x5 struts were considered (Figure S5A). The distances between AuNRs for theoretical calculation were determined from TEM measurements and displayed in Figure S5B. The simulation results (Figure S6) agree well and reproduce the profile of the experimental CD spectra (Figure 3B) of R-R3(x2, x4, x5) and LR3(x1, x2, x4). Under the excitation of light with right circular polarization (RCP), the simulated model L-R3(x1, x2, x4) exhibits a single plasmonic resonance at 740 nm in the extinction spectrum; on the other hand, an opposite excitation of light with left circular polarization (LCP) excites different collective plasmon modes and shifts the resonance to 727 nm (Figure S5C). This resonance shift is indeed consistent with the observed experimental CD peak shift and further proves the L characteristics of the assembled CPMs. In addition, the simulated surface charge distribution profiles of L-R3(x1, x2, x4) (Figure S5D) further indicate that the observed chiroptical response is indeed due to optical modulation from the collective oscillation modes of the neighboring AuNRs under the excitation of the helical external field. As displayed in Figure S5D, for LCP, the quasi-paralleled oscillation between neighboring AuNRs increases the resonance energy; whereas for RCP, the anti-paralleled oscillation decreases the resonance energy, resulting in a red-shifted resonance compared to LCP. Noting that similar discussion and analysis applies to the R-R3(x2, x4, x5) CPMs, in which a nearly mirrored CD spectrum is expected (Figure 3B and Figure S5E, F). Next, the switching kinetics was characterized by monitoring the CD signal at 708 nm. The time-dependent CD response (Figure S7 and bottom of Figure 3C, D) shows that the reconfiguration takes places in 20 min upon a proton flux. Note that the system’s pH was adjusted to 6.6 to reset both L-R3(x1, x2, x4) and R-R3(x2, x4, x5) to the Off-state.


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Figure 3. Experimental and theoretical characterizations of the proton-responsive reconfigurable CPMs. (A) Top left: illustration of CGC and TAT triplet formation through Watson-Crick and Hoogsteen interactions. Top right: pH-sensitive triplex DNA segment. (B) Experimental CD spectra of the L-state (red) and R-state (blue) of CPMs. (C) and (D) Top: Models of mirrorsymmetric CPMs switching between Off-state and left-handed (L)-state (red) or right-handed (R)state (blue) in response to pH below pKa. Bottom: Kinetic characterization of L-R3(x1, x2, x4) (red) and R-R3(x2, x4, x5) (blue) with a critical assembly value pKa = 7.2 upon increasing proton flux. Adaptive modulation of CPM regeneration by pCRN. Next, we demonstrate that the reconfiguration of our CPMs can be rationally controlled by regulating the proton flux via a pCRN.31, 32 As schematically illustrated in Figure 4A, we coupled a pCRN to the pH-responsive CPMs to achieve a dissipative self-assembly. The addition of chemical fuel makes the system’s pH lower than the critical assembly value pKa. As a result, CPMs start to form due to the formation of DNA triplex, which is reflected by a substantial CD signal increase. As the enzyme catalyzes


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the hydrolysis of urea to produce NH3, the system’s pH gradually increases until it raises above pKa, the CPMs start to disassemble, resulting in CPMs transforming from Off→On→Off states. We first investigated the dependence of the system’s pH on fuel concentration. We can control the system’s pH within ranges of [4.5, 6.2], [4.5, 6.9], and [4.5, 8.4] by adjusting the urea concentration from 2 M, 4 M, to 6 M. At the outset we sought to perform a transient self-assembly cycle on a single system, R-R3(x2, x4, x5) with a critical assembly value of pKa = 7.2 (50% TAT). Thus, the pCRN with effective pH range of 4.5 to 8.4 is utilized to drive the self-assembly of CPMs in nonequilibrium. By repeated adding the chemical fuels, we continuously monitored the changes of system’s pH (Figure 4B) and CD signal at 708 nm (Figure 4C) in real time. Gradual amplitude decreases in system’s pH and CD response were observed with increasing number of cycles. This can be attributed to attenuated urease activity during cycling, dilution effects resulting from continuous input of fuel. Note that the CD signal decreased more rapidly (dropped ~40%, from -1 to -0.591) than system’s pH (pH range narrowed down ~32%, from [4.61, 8.38] to [5.01, 7.58]), which is likely due to decreased reconfiguration efficiency with changing reaction conditions.


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Figure 4. Feedback-induced transient self-assembly in non-equilibrium. (A) A general transient self-assembly controlled by a pCRN from Off-state to the temporary CPMs. When pH value of the system is lower than pKa, both R- and L-states of the CPMs start to assemble; as the enzyme catalysts urea to produce NH3, pH of the system begins to rise, upon above the pKa, R- and Lstates of the CPMs start to disassemble, eventually returning to initial state. (B) Reversible pH changes of the system following repeated additions of chemical fuels over time. (C) Relative CD response for R-R3(x2, x4, x5) following repeated additions of chemical fuels. Experimental conditions: 0.20 mg/mL urease, 6 M urea, 6 mM CA/Na3C. Spatiotemporal control of CPMs dissipative self-assembly. Given the strong dependence of the self-assembly behavior on system’s pH, we are able to further control the transient lifetimes of the CPMs by reaction kinetics and fuel levels of the pCRN (Figure 5A). Evidently, the kinetics of the pCRN at play can be controlled by regulating the urease concentrations, with initial reaction rate varying from 0.322 min-1 (v1, 0.5 mg/mL urease), 0.105 min-1 (v2, 0.2 mg/mL urease), and 0.040 min-1 (v3, 0.05 mg/mL urease), respectively (Figure 5B). Note that, the higher urea concentration results in a wider pH change of the system, while higher urease concentration increases the pH regulation kinetics of the system. First, we investigated the single-component system (Figure 5C) consisting of L-R3(x1, x2, x4) or R-R3(x2, x4, x5) with a critical assembly value of pKa = 7.2 (50% TAT), respectively. When the system’s pH was controlled by a relatively fast pCRN (v1 = 0.322 min-1), the system remained in the Off-state, resulting in a negligible CD response. This is consistent with our prediction since the time required for the structural reconfiguration of pH-responsive CPMs (~20 min, Figure 3C, D and Figure S7) far exceeds the time at which the system is below pKa = 7.2 (~3 min). Similar results were also observed in the dual-component systems (mixture state 1: L and R with molar


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ratio of 1:1; mixture state 2: L and R with molar ratio of 2:1; Figure 5D, E left). In the case of pCRN with medium reaction rate (v2 = 0.105 min-1), the CD signal of L-R3(x1, x2, x4) gradually increases along with incubation time and reaches maximum at ~22 min, indicating that the structural reconfiguration closely follows the kinetics of pCRN. When the system’s pH further increases above 7.2, the CPMs start to disassemble, resulting in a substantial CD amplitude decrease (Figure 5C middle, red dots). Similarly, the R-R3(x2, x4, x5) exhibits a nearly mirrored pH/time dependence (Figure 5C middle, blue dots). Notably, further decreasing the urease concentration (0.05 mg/mL urease, v3 = 0.040 min-1) could substantially prolong the lifetime of the chiral structures (increase from ~5 min to ~40 min, Figure 5C right).


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Figure 5. Spatiotemporal control of the CPMs in non-equilibrium by tuning the kinetics of pCRN. (A) Scheme of a pCRN. (B) The kinetic characterization of the urease-based enzymatic pCRN in different concentrations of urease. Control of the transient lifetimes of the CPMs in single- and dual-component systems: (C) L- or R- state, (D) mixture state 1 (L- and R-state with molar ratio of 1:1), and (E) mixture state 2 (L- and R-state with molar ratio of 2:1) by fuel-conversion kinetics. The relative CD signal was monitored over time at 708 nm. Experimental conditions: 0.5 mg/mL (v1), 0.2 mg/mL (v2), 0.05 mg/mL (v3) urease; 6 M urea; 6 mM CA/Na3C. The lifetime of transient assembly is dictated by the kinetics of pCRN at play, thus we are able to control the lifetime of system’s chirality by varying the urease concentration as well as the system component. For instance, in a dual-component system (mixture state 1: L and R with molar ratio of 1:1), when the system’s pH is below 6.6 (i.e., t < 18 min), both L-R3(x1, x2, x4) and RR3(x2, x4, x5) start assembling at nearly the same rate and co-exist, thus resulting in a negligible CD response. When the system’s pH continues to increase above 6.6 (18 min < t < 22 min), RR3(x2, x4, x5) with pKa = 6.6 dissembles into Off-state, and L-R3(x1, x2, x4) with pKa = 7.2 remains intact. This is reflected by an abrupt CD amplitude increase (Figure 5D middle, red dots). As such, the CD signal increases until the system reaches another CPM’s critical assembly value of pKa = 7.2, as shown in Figure 5D middle and left. Subsequent pH increases (t > 22 min) dissemble LR3(x1, x2, x4) into Off-state, a sharp decrease in CD response is observed, indicating that the both CPMs are transformed into Off-state. The reverse case of LpKa = 6.6 + RpKa = 7.2 shows a nearly mirrored CD response (Figure 5D middle, blue dots). Similarly, in the system containing L and R in non-equimolar amounts (e.g., 2 × LpKa = 6.6 + RpKa = 7.2), similar CD response was observed earlier in the case of pCRN with medium or slow reaction rate (v2 = 0.105 min-1, v3 = 0.040 min-1; Figure 5E middle and right, red dots). Moreover, we can build a more complex transient CPMs with


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dampling feature using pCRN with slow reaction rate and non-equimolar system. As shown in Figure 5E right, the system’s pH stays below 6.6 until 40 min, thus substantially prolong the lifetime of transient assembly compared to equimoar system shown in Figure 5D. Further increasing pH between 6.6 and 7.2 (40 min < t < 49 min) disassemble LpKa = 6.6 and RpKa = 7.2 remains intact, where inversed CD response is reasonably expected. When the system’s pH continues to increase until 7.2 (t > 49 min), the overall CD response of the mixture decreases because both the LH and RH structures are in Off-state. Similarly, another non-equimolar system (e.g., LpKa = 7.2 + 2 × RpKa = 6.6) exhibits a nearly mirrored pH/time dependence (Figure 5E right, blue dots). All these results elucidate excellent control selectivity of different CPMs via pCRN. It is this autonomous control of material function in time that can be attractive in a wide range of applications. CONCLUSION We have outlined a general approach to realize transient self-assembly of CPMs based on DNA templet. In this work, we constructed a pair of proton-responsive PMs by introducing temporary formation and dissociation of DNA triplex. Next coupling a pCRN, we realized the kinetically transient self-assembly of metamolecules in non-equilibrium. By controlling proton concentration changing kinetic, we demonstrated how control the consequently lifetime of metamolecules formed in non-equilibrium system. Also this transient self-assembly system could be fueled several times by addition of chemical fuel. Compared with some self-assembled materials in other non-equilibrium states,3-6 we use DNA nanotechnology which is programmable at the nanoscale,33-36 combined with a positive feedback chemical reaction network, achieving transient self-assembly of the metamolecules. 1) By controlling the kinetics of the CRN realize the lifetime of the activated building blocks, controlling


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the lifetime of the structures. 2) Realizing excellent spatiotemporal control: the structures could self-classify according to its own critical assembly value, so that the PMs can be selectively selfassembled. Out-of-equilibrium self-assembly has great potential for the use of dynamic and responsive materials.2, 7-9 Due to the dynamic nature of the materials, these materials are endowed with lifelike properties in a non-equilibrium, for example, self-healing, erasable, adaptable, and repairable properties with adjustable life and activity.3-6 Although the number of man-made materials formed by out-of-equilibrium self-assembly remains limited to concept until now, the examples of successful materials under out-of-equilibrium are increasing.7, 37 And the basis of life activities is controlled by out-of-equilibrium systems, there will definitely be exciting applications in out-ofequilibrium self-assembly. We envision that the transient assembly in out-of-equilibrium system could help control function of the structures and give an opportunity for mimicry of behavior dynamic structures found in nature system. METHODS Materials. Staple DNA strands of PAGE grade, capture DNA strands of PAGE grade and thiolated DNA strands of HPLC grade were bought from Sangon Biotech. M13mp18 scaffold DNA strands were purchased from New England Biolabs (US). Tetrachloroauric acid (HAuCl4), cetyltrimethyl ammonium bromide (CTAB), sodium dodecylsulfate (SDS), silver nitrate (AgNO3), sodium borohydride (NaBH4) and ascorbic acid (AA) were supplied by Sigma. Ntrimethoxysilylpropyl-N, N, Ntrimethylammonium chloride (TMAPS) (50% in methanol) and tetraethyl orthosilicate (TEOS) were purchased from TCI, Japan. Urease from Canavalia ensiformis (Jack bean) was purchased from Sigma. Urea was purchased from Sinopharm Chemical


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Reagent Co., Ltd. Agarose was bought from BioRad, Germany. Gel Red was purchased from Solarbio Life Science (Beijing, China). Carbon-coated copper grids were purchased from Beijing Zhongjingkeyi Technology Co., Ltd (Beijing, China). Freeze N Squeeze spin columns were purchased from BioRad, Germany. Atomic force microscope (AFM) tips were purchased from Bruker. All reagents were used as received without further purification. All experimental consumables were used as received. Synthesis of AuNRs. AuNRs were prepared using a seeded growth method according to a previously described procedure.38 Synthesis of AuNP seeds: CTAB solution (9 mL, 0.10 M) was first mixed with 1 mL HAuCl4 of 2.5 mM under vigorous stirring, followed by the addition of 0.60 mL of ice-cold 0.01 M NaBH4, resulting in a brownish yellow solution. The mixture was continuously stirred for 2 min and then the seed solution was aged for 5 min. Growth of AuNRs: The 12 nm × 50 nm AuNRs were synthesized as follows. 10 mL of 2.5 mM HAuCl4 was added into 40 mL of 0.10 M CTAB solution at 25 °C, followed by the addition of 1.25 mL of 0.04 M AgNO3 solution and 0.35 mL of 0.0788 M AA. Finally, 60 μL of the previously prepared seed solution was injected to grow AuNRs. The resultant solution was mixed by gentle inversion for 10 s and then left undisturbed for several hours. Functionalization of AuNRs with DNA.18 1 mL of 0.95 nM AuNRs was mixed with 10 μL of 500 μM thiolated DNA in 1 × TBE buffer containing 0.01% SDS, and the mixture was incubated at room temperature for several hours. 5 M NaCl was then added into the reaction solution for 10 times in 5 h to reach a final NaCl concentration of 0.5 M. Then, the mixture solution was transferred to a thermo-mixer (Eppendorf) set at 300 rpm (25 °C) for 12 h. After that, the AuNRsDNA conjugates were collected by centrifugation and washed with 1 × TBE buffer three times to remove excess ssDNA.


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Preparation of tetrahedron-shaped DNA origami template. M13mp18 scaffold strands, staple DNA strands (Table S1), and capture DNA strands (Table S2) were mixed in 1 × TAE-Mg2+ (40 mM Tris, 20 mM acetic acid, 2 mM EDTA, and 12.5 mM Mg2+) buffer at a ratio of 5:5:1. The final concentrations of the scaffold, staple strands, and capture strands were 5 nM, 50 nM, and 50 nM, respectively. The tetrahedron-shaped DNA origami nanostructures were formed by slowly cooling down from 65 °C to 25 °C over the course of ~12 h in a thermo-cycling machine (SimpliAmpTM, Thermo Fisher Scientific). Purification of tetrahedron-shaped DNA origami nanostructures. To remove excess staples, agarose gel electrophoresis system was used. That is, the mixtures were loaded into 0.5% agarose gels containing 1 × Gel Red in 1 × TAE-Mg2+ buffer and subjected to gel electrophoresis at 100 V for 1 h in an ice water bath. Then the specific band was cut and extracted using Freeze N Squeeze spin columns (BioRad, Germany). The concentration of DNA origami was estimated by its absorption at 260 nm. TEM characterization. All carbon-coated copper grids were glow discharged for 10 s before use. The samples were first coated with an amorphous silica layer following a silicification protocol reported by Fan et al.39 to improve the rigidity of nanostructure during TEM characterization procedure. The samples for TEM imaging were prepared by depositing a 5 μL of the sample solution on the TEM grid. After 5 min, the excess solution was wicked from the edge of the grid using filter paper. To remove the deposited salt, the grid was washed with 5 μL of water for 3 min and the excess water was wicked away using filter paper. 5 μL of a 0.75% uranyl acetate solution was used to treat the grid for 40 s twice, and the excess solution was wicked away. To remove the excess uranyl acetate, the grid was washed with 5 μL of water for 3 min and the excess water was wicked away using filter paper. All the grids were kept at room temperature. Imaging


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was performed using a Tecnai G2 spirit Biotwin (FEI, USA) operated at an acceleration voltage of 120 kV. Images were acquired using a Gatan 832 CCD camera. AFM characterization. AFM imaging was conducted on a Multimode Nanoscope VIII instrument (Bruker). For imaging DNA nanostructures in fluid, 5 μL of purified samples were deposited onto a freshly cleaved mica and left to adsorb for 3 min. 1 × TAE-Mg2+ buffer was added to the mica and the sample was scanned with “Scanasyst in fluid” mode using Scanasyst-Fluid+ tips (Bruker). To promote a stronger bond between the DNA samples and the mica surface, 10 mM NiCl2 was used in the imaging buffer. Fabrication of chiral plasmonic metamolecules (CPMs). AuNRs-DNA conjugates were added to the purified DNA origami with a molecular ratio of 5:1. The final Mg2+ concentration was raised to 12.5 mM by adding a 10 × TAE-Mg2+ buffer. The mixture was slowly cooling down from 40 °C to 25 °C over the course of ~12 h in a thermo-cycling machine. The product was loaded into 0.5% agarose gels in 1 × TAE-Mg2+ buffer and subjected to gel electrophoresis at 100 V for 40 min in ice water bath. Specific bands were cut and extracted using Freeze `N Squeeze spin columns. Circular dichroism (CD) characterization. CD spectra were recorded using a Jasco-815 CD spectrometer with a scanning speed of 100 nm/min and optical path of 1 cm at room temperature. All measurements were carried out with a 200 µL solution (in 1 × TAE-Mg2+ buffer) containing ~1 nM CPMs after agarose gel purification. The baseline was corrected using 1 × TAE-Mg2+ buffer. Generally, small amounts but high concentrations of the chemical fuel containing urease were used for driving the assembly to eliminate the dilution effect.


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Switching between R- or L-state and Off-state upon the pH change. CPMs functionalized with pH-insensitive DNA duplex segments (Table S3) in x1 or x5 were diluted to reach a final concentration of ~1 nM in 1 × TAE-Mg2+. Then, the proton-responsive AuNRs-DNA conjugates were added to the CPMs mixture with a molecular ratio of 10:1, followed by the addition of acetic acid to adjust the pH below pKa. CD spectra of the CPMs at different time points was then collected. (Figure S5) Theoretical calculation of CPMs. Theoretical calculations were performed using commercial software COMSOL Multiphysics based on a finite element method.18, 20 In these calculations, the AuNRs were modeled as a cylinder with two hemispherical caps at both ends. For simplicity, only the situation that the circularly polarized light (CPL) propagates on the direction which were perpendicular to the x2 and x5 was considered, as shown in Figure S7A. AuNRs had an aspect ratio of 3.62 ± 0.58 with an average diameter of 14.78 nm ± 2.06 nm and average length of 52.62 nm ± 4.12 nm. Urease activity for metamolecules system. Urease activity assays were performed by measuring the pH change upon addition of 0.67 µL urea with a concentration of 2 M, 4 M, and 6 M. Here we first added chemical fuels (900 mM CA/Na3C, 9:1), which was a concentrated acidic buffer contained different concentrations of urea, to reach a pH of 4.5. Then we monitored the pH change of the system in time (Figures 3C and 3D). We also made a thorough study on the influence of different urease concentrations (0.05 mg/mL, 0.20 mg/mL, and 0.50 mg/mL) on the pH changes (Figure 5B).

ASSOCIATED CONTENT


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Supporting Information. The Supporting Information is available free of charge on the ACS Publications website. Characterizations of AuNRs, DNA origami templates and 11 types of (C)PMs, theoretical calculation, simulated CD spectra and DNA sequences, including Figures S1-S7 and Tables S1S4 (PDF) The authors declare no competing interests.

AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]. *E-mail: [email protected]. *E-mail: [email protected]. ORCID Hao Pei: 0000-0002-6885-6708 Li Li: 0000-0001-8494-4997 Chunhai Fan: 0000-0002-7171-7338 Chuan Zhang: 0000-0002-9311-0799 Author Contributions H.P., C.F. and C.Z. supervised the project. T.M., C.Z., H.P., and C.F. conceived and designed the experiments. T.M. and W.J. performed the experiments. X.L. provided reagents/materials/analysis


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tools. T.M., W.J., and L.L. performed data analysis. T.M., C.Z., L.L., and H.P. wrote the paper, and all authors read and approved the manuscript. ACKNOWLEDGMENT This work was supported by the National Science Foundation of China (Grant No. 21722502), Shanghai Rising-Star Program (19QA1403000) and Shanghai Science and Technology Committee (STCSM) (Grant No. 18490740500).

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