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Cite This: ACS Cent. Sci. 2019, 5, 186−191 http://pubs.acs.org/journal/acscii

The Importance of Salt-Enhanced Electrostatic Repulsion in

Colloidal Crystal Engineering with DNA
Soyoung E. Seo,†,§ Martin Girard,‡,⊥ Monica Olvera de la Cruz,*,†,‡,§,⊥ and Chad A. Mirkin*,†,‡,§
†
Departments of Chemistry and ‡Materials Science and Engineering, §International Institute for Nanotechnology, and ⊥Physics and
Astronomy, Northwestern University, Evanston, Illinois 60208, United States
*
S Supporting Information

ABSTRACT: Realizing functional colloidal single crystals

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requires precise control over nanoparticles in three dimensions

across multiple size regimes. In this regard, colloidal
crystallization with programmable atom equivalents (PAEs)
composed of DNA-modified nanoparticles allows one to
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program in a sequence-specific manner crystal symmetry,

lattice parameter, and, in certain cases, crystal habit. Here, we
explore how salt and the electrostatic properties of DNA
regulate the attachment kinetics between PAEs. Counter-
intuitively, simulations and theory show that at high salt
concentrations (1 M NaCl), the energy barrier for crystal growth increases by over an order of magnitude compared to low
concentration (0.3 M), resulting in a transition from interface-limited to diffusion-limited crystal growth at larger crystal sizes.
Remarkably, at elevated salt concentrations, well-formed rhombic dodecahedron-shaped microcrystals up to 21 μm in size grow,
whereas at low salt concentration, the crystal size typically does not exceed 2 μm. Simulations show an increased barrier to
hybridization between complementary PAEs at elevated salt concentrations. Therefore, although one might intuitively conclude
that higher salt concentration would lead to less electrostatic repulsion and faster PAE-to-PAE hybridization kinetics, the
opposite is the case, especially at larger inter-PAE distances. These observations provide important insight into how solution
ionic strength can be used to control the attachment kinetics of nanoparticles coated with charged polymeric materials in
general and DNA in particular.

C olloidal crystals composed of nanoparticles are structures

that can be designed to have interesting optical and
electronic properties, based upon nanoparticle composition,
In atomic systems, large crystals can be realized by
kinetically impeding the formation of critical nuclei. This can
occur by either: (i) suppressing the formation of new nuclei, or
crystal lattice symmetry and spacing, and mesoscopic crystal (ii) expediting the growth of existing crystals to deplete the
habit and size.1−7 Because of their chemical programmability solution of the atom source (e.g., heterogeneous nucleation
and sequence-specific interactions, oligonucleotides have and growth).20 In the context of colloidal crystal engineering
emerged as versatile ligands to direct the assembly of with DNA, salt concentration can be used to control the
nanoparticles into higher order crystalline architectures.8−11 kinetics of DNA bond formation.21 At moderate monovalent
Indeed, nanoparticles functionalized with a dense shell of salt concentrations (below 0.5 M), the kinetics of PAE
upright and oriented DNA behave as “programmable atom reorganization in superlattices change as a function of solution
equivalents” (PAEs) that can be assembled into a diverse set of ionic strength primarily because the additional charge
crystalline structures following well-established design screening stabilizes the DNA linkages between adjacent
rules.8,9,11−15 PAEs once formed.22 Within this salt concentration range,
The size of colloidal crystals is an important design modified nonlinear Poisson−Boltzmann approaches can be
parameter for the preparation of device architectures, used to describe the electrostatic screening between PAEs.12
particularly those requiring control over the optical path
However, at high salt concentrations (above 0.5 M), the
length (i.e., the distance that light travels across the crystal in
kinetics of PAE interactions cannot be explained solely by
the orientation of interest);1,2,16 however, methods for
realizing single crystals with tunable sizes have yet to be charge screening as the association of ions becomes favorable
developed. Single crystals generated by the slow cooling of via ionic correlations, resulting in the formation of ion
PAEs typically fall in the 2 μm or less range when synthesized clusters.23−25 This has been explored experimentally where
in solutions with monovalent salt concentrations between 50 high salt concentration causes long-range repulsion between
and 500 mM.12 Silver ion17 and molecular intercalators18,19 nanoparticle surfaces26 and stabilizes dispersions of charged
have been used to postsynthetically strengthen DNA bonds
within such crystals, which have subsequently been utilized as Received: November 9, 2018
seeds for controlling the extended growth of crystals.18 Published: January 8, 2019

© 2019 American Chemical Society 186 DOI: 10.1021/acscentsci.8b00826

ACS Cent. Sci. 2019, 5, 186−191
ACS Central Science Research Article

colloids in molten salts.27 Furthermore, simulations have

shown that the strength of interparticle interactions depends
on the surface charge density of nanoparticles; at high salt
concentration, weakly charged nanoparticles have a depletion-
type attraction, whereas nanoparticles with moderate to high
surface charge densities experience long-range repulsion
attributed to ionic correlations.25 In particular, for DNA-
mediated colloidal assemblies, high salt concentration has been
shown to induce phase transitions28 and nanoparticle
aggregation in the absence of hybridization interactions.29
However, it is difficult with the current tools to gain a full
understanding of the mechanism of how surface grafting
densities and electrostatic energies cause salting out and affect
crystal formation in systems with complementary linkers. Full
atom and implicit solvent coarse-grained simulations show that
the fraction of clusters with 5−8 ions increase rapidly as the
salt concentration increases from 0.3 to 1 M.25 We hypothesize
that these clusters electrostatically interact with the DNA
corona surrounding the nanoparticle and incur a significant
energetic penalty associated with charge repulsion when the
PAEs are in close proximity, resulting in a reduction of the
attachment kinetics during PAE crystallization.

■ RESULTS AND DISCUSSION

To explore the free-energy landscape across which nucleation
takes place with varying salt concentrations, molecular
dynamics (MD) simulations were used to calculate PAE
interaction potential energies (Figure 1A). These simulations
used a PAE design consisting of two 15 nm spherical gold
nanoparticles, each functionalized with one of two DNA
sequences bound to linker strands with complementary “sticky
ends” (Figure 1). These PAEs assemble into bcc superlattices.
The foundation for these simulations is based on the
assumptions that (i) the interaction between the comple-
mentary PAEs is the main driving force for crystallization, (ii)
the interaction with the second nearest neighbors (i.e., Figure 1. (A) A snapshot of two complementary PAEs at different salt
noncomplementary PAEs) is negligible, and (iii) similar trends concentrations in simulations. The centers of the 15 nm nanoparticles
in the free energy are observed at room temperature (25 °C) are 370 Å apart in this snapshot. (B) Pair potential energies between
complementary PAEs were calculated across a range of interparticle
and elevated temperature. Effective pair potential energies were distances. PAEs exhibit a well-defined equilibrium interparticle
calculated by modeling two complementary PAEs at 25 °C distance at potential minimum. At an interparticle distance of 380
with the 3SPN force-field, which included DNA-hybridization Å, the attachment barrier peaks; this increases with increasing salt
attraction, stacking interactions, excluded volume repulsion, concentration. (C) Mean crystal size obtained without coarsening as a
and electrostatic interactions between phosphate groups and function of the attachment rate to the surface.
explicit ions.30,31 The strong parallels between the modeled
and experimental results (DNA melting temperature increases
with increasing salt concentration) indicate that the binding nm as opposed to the sub-nanometer length predicted by
energy between the PAEs increases with increasing salt DLVO.25 Consistently, above certain salt concentrations,
concentration (Figures 1B, S4). simulations that include hybridization interactions show
The impact of salt concentration on the interaction potential short-range attraction from hybridization interactions at
between a pair of PAEs was studied by calculating the potential distances where the DNA coronae overlap and longer range
energies as a function of interparticle distance (i.e., core-to- repulsion extending to distances where they do not overlap
core distance) ranging from 30 to 40 nm. Previous studies on (Figure 1B). This results in an energetic barrier greater than
nanoparticles with noncomplementary DNA strands exhibit the thermal energy (kBT) (i.e., the thermal fluctuation of the
repulsion forces between nanoparticles that are longer range system must cross over the nucleation barrier to initiate
than the repulsion predicted by DLVO theory when the salt crystallization), which slows the attachment kinetics between
concentration increases above 0.3 M,25 which is in agreement complementary PAEs. Thus, we hypothesize that the PAEs
with experiments on repulsion between charged surfaces at assemble to form larger crystals at higher solution ionic
high monovalent salt concentrations.26,27 This electrostatic strengths due to this nucleation barrier (Figures 1C, S1−S2).
interaction depends on multiple factors, including grafting To investigate whether PAE assembly at elevated salt
density, temperature, and ionic strength, and can even lead to concentrations leads to the growth of larger microcrystals, two
salting out.25,29 For nanoparticles grafted with strongly charged sets of 15 nm spherical PAEs with complementary DNA
polymer chains at similar grafting densities (e.g., PAEs), the sequences were prepared. Each sample was assembled in
effective screening length was measured to be between 2 and 5 solution at three different salt concentrations (0.3, 0.5, and 1
187 DOI: 10.1021/acscentsci.8b00826
ACS Cent. Sci. 2019, 5, 186−191
ACS Central Science Research Article

Figure 2. (A) Williamson-Hall analysis of SAXS data (Figures S5−S6) can be used to deconvolute peak broadening arising from grain size
(intercept) and microstrain (slope). (B) Scheme (top) showing the dimension that was measured for the statistical analysis of crystal size
distribution using SEM images. (i), (ii), and (iii) are schematic representations of three different orientations of the microcrystals commonly
observed on the substrate. The length “a” (edge length) was measured and mathematically converted to convey the length shown in the top
drawing. Size analyses of approximately 150 microcrystals, assembled at (C) 0.3, (D) 0.5, and (E) 1 M NaCl, show an increase in average crystal
size with increasing salt concentration. SEM images of silica-encapsulated bcc gold nanoparticle microcrystals, interlinked with DNA and assembled
at (F) 0.3, (G) 0.5, and (H) 1 M NaCl confirm faceted rhombic dodecahedra. For this set of data, nanoparticle assemblies were done using
complementary seven-base pair sticky ends. Scale bars are 2 μm.

M NaCl) and then slowly cooled. This process enables DNA- to extract information about grain size (eqs S12−13).32
driven crystallization that favors the formation of single- Consistent with both the hypotheses and the calculations of
crystalline rhombic dodecahedra with the gold nanoparticles in interaction potentials, a significant increase in average grain
a bcc crystallographic symmetry (over a polycrystalline size is observed when the salt concentration was increased
assembly).11,12 The effect of salt concentration on PAE from 0.5 to 1 M for nanoparticle assemblies using both six- and
assembly above 1 M NaCl was not probed in this study seven-base pair sticky ends (Figures 2A, S7). This further
because the PAEs no longer crystallize into rhombic confirms the assumption that similar trends in the free energy
dodecahedron single crystals. Single crystals were chosen as are observed at different temperatures. Although the grain size
the subject of this study because the crystal domain size is
generally increases with increasing salt concentration, it
easier to identify and compare between samples. Superlattices
decreases with increasing particle concentration (Figure S8).
were then characterized by small-angle X-ray scattering
(SAXS), electron microscopy (EM), and selected area A decrease in mean crystal size with increasing particle
diffraction (SAD). concentration can be attributed to the increase in chemical
First, SAXS line shape analysis was used to deconvolute peak potential (eq S2). Since the nucleation rate is strongly
broadening arising from grain size and microstrain (Figure S6), dependent on the chemical potential of the system, increasing
and the grain sizes were compared using Williamson-Hall the chemical potential leads to a faster nucleation rate (i.e., a
analysis (Figures 2A, S7). Stokes-Wilson strain broadening can greater number of nuclei forms), and thus, the formation of
be combined with Scherrer size broadening in scattering peaks smaller microcrystals is expected. Note that the chemical
188 DOI: 10.1021/acscentsci.8b00826
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potential difference is a thermodynamic driving force for regime is present, and crystals with irregular shapes and
crystallization. disordered nanoparticles form.35 However, in the case of slow
To further examine the effect of salt concentration on crystal attachment rates (i.e., j is small), faceted microcrystals form.
size along with crystal habit (e.g., facet), we used SEM to When most of the nanoparticles are consumed, diffusion can
determine the size distribution of approximately 150 micro- no longer sufficiently transport materials to the crystal−
crystals for each salt concentration. Since the formation of solution interface. Beyond this regime, crystal growth is limited
microcrystals mediated by the slow cooling approach is similar by diffusion, where the growth rate is significantly slowed
to conventional homogeneous nucleation (i.e., the crystal- (crystal size ≈ t1/2).36 The growth rate in this regime is entirely
lization starts from dispersed precursors), a broad range of determined by the diffusion constant and the supersaturation,
crystal sizes is expected from classical theory. To prepare given by c − ceq, where c and ceq are the current and
samples for SEM imaging, slow-cooled samples were equilibrium concentrations of the free nanoparticles in
encapsulated in silica using a sol−gel process,33 dispersed in solution, respectively. The transition between interface-limited
50% EtOH in water, and slowly dried on a silicon substrate. to diffusion-limited regimes has been reported for colloidal
Although microcrystals generated in solution with different salt crystals using MD simulations.37
concentrations are all rhombic dodecahedra (Figure 2F−H, The combination of MD simulations and experiments
S9−S10), the overall crystal size increases with increasing salt suggests that the reduction in the PAE attachment rate at 1
concentration (Figure 2C−E). Because the microcrystals dried M NaCl likely impedes the formation of stable clusters/critical
on a substrate lie in different orientations on the substrate, nuclei and drastically slows the interface-limited regime,
mathematical corrections on each measurement of “a” (edge meaning the system at high salt conditions enters the
length) were performed (Figures 2B, S11, Table S2). SEM diffusion-limited regime much later than the other two
results show similar size distributions for the 0.3 and 0.5 M salt systems. Thus, by suppressing nuclei formation, large single
concentration samples with mean sizes of 3.6 ± 1.6 and 3.5 ± crystals are realized. Since this phenomenon occurs at a large
1.3 μm, respectively (Figure 2D, E). However, similar to the interparticle distance (i.e., before the particles are fully locked
conclusions drawn based on the SAXS data, a noticeable into a particular structure) and solely depends on the
increase in the crystal size distribution is observed for the 1 M interactions between salt ions and the DNA corona, this
NaCl sample with a calculated mean size of 4.9 ± 2.6 μm approach can be generalized for different particle cores and
(Figure 2F). As noted earlier, a wide distribution of crystal lattice symmetries. We presume that a similar trend will be
sizes is predicted for crystal growth via homogeneous observed when the rate of cooling is changed. It is worth
nucleation and growth. However, it is worthwhile to note noting that there is a possibility of large crystal growth
that in addition to the average crystal size analyzed from both occurring through coalescence and restructuring processes,
SEM and SAXS (Figures 2A, 2C−E, S7), the number of where two or more stable crystals merge to form a single
crystals that are smaller than 2 μm decreases drastically with crystal. In atomic systems, coarsening typically occurs by
increasing salt concentration; i.e., there were no crystals below Ostwald-like ripening processes;38 however, this process is very
2 μm in the 1 M NaCl sample (Figure 2C−E). Remarkably, slow and unlikely to occur in colloidal systems. On the other
these crystals can grow up to 21 μm (the length shown in hand, it has been shown that the coarsening in colloidal
Figure 2B, top) when the PAEs are assembled at high solution systems could happen by grain-rotation induced coalescence.39
ionic strength (Figure 2H).
Similar coarsening has been observed for PAE systems in MD
The crystallization process is usually described by the
simulations (see Simulation section in the Supporting
formation of critical nuclei (i.e., nucleation) followed by
Information for further discussion).37
subsequent growth. Generally, the nucleation rate is dependent
Because defects and inhomogeneity in the superlattice can
on both the energy barrier of nanoparticle cluster formation
affect the optical response of these materials, it is crucial to
and the attachment rate of the interacting nanoparticles. An
produce high-quality crystals.40 Each SAXS pattern shows,
emergence of long-range repulsion at high salt concentration
regardless of the solution ionic strength, a high degree of
(Figure 1B) results in a reduction of the attachment rate A,
which can be understood from the following relationship: single-crystalline ordering of nanoparticles arranged into a bcc
crystallographic symmetry (Figure S5). The crystallinity was
j = ν0 exp( −ΔG′/kBT ) (1) further characterized by performing SAD using a transmission
electron microscope (TEM) (Figure 3). This characterization
where j is the frequency at which two nanoparticles come
together, ν0 is the trial rate (a constant, units in 1/time), and
ΔG′ is the repulsion barrier that nanoparticles must overcome
to initiate crystallization (see Simulation section in the
Supporting Information for detailed discussion). Thus, from
this equation, one can extract that the frequency of
nanoparticle attachment events decreases exponentially with
an increasing energy barrier. In the case where the long-range
diffusion is required, two rate-limiting processes, interface- and
diffusion-limited growth, affect the growth rate. The initial
Figure 3. (A) and (B) Transmission electron microscopy (TEM)
stage of crystal growth is limited by interfacial attachment images of a thin (∼100 nm) section of silica-encapsulated
barriers. In this regime, crystal size increases linearly with time microcrystals, initially crystallized in 1 M NaCl. (C) Well-defined
(crystal size ≈ At, where A is the growth rate proportional to j SAD patterns were obtained by subjecting a parallel beam of high-
and t is the time).34 In the case where the nanoparticle energy electrons to a thin section of one of the large microcrystals
attachment occurs extremely fast (i.e., nanoparticle interactions shown in (B). Scale bars are 5 μm, 200 nm, and 100 μm−1 for (A),
are extremely favorable and j is large), no interface-limited (B), and (C), respectively.

189 DOI: 10.1021/acscentsci.8b00826

ACS Cent. Sci. 2019, 5, 186−191
ACS Central Science Research Article

technique provides a diffraction pattern of a thin crystalline

specimen within a selected area, which can be used to identify
■
*
ASSOCIATED CONTENT
S Supporting Information
local crystal structures and examine defects, such as twinning The Supporting Information is available free of charge on the
and dislocations. Here, we used SAD to qualitatively evaluate ACS Publications website at DOI: 10.1021/acscents-
the crystallinity of local areas within these microcrystals. ci.8b00826.
Indeed, the appearance of distinct spots in the diffraction
patterns of a large single crystal indicates high-quality crystals Experimental procedures, including simulation details,
and that the microstrain is mostly isotropic without random oligonucleotide sequences, nanoparticle functionaliza-
defects (Figure 3C). tion and assembly, and characterization/analysis techni-
Furthermore, it is important to have independent control ques (SAXS, SEM, and TEM), and additional figures
(PDF)

■
over the interparticle distance, while retaining crystallinity and
habit, because each structural control can be used to influence
material properties. A uniform shift in peak position, however, AUTHOR INFORMATION
indicates that there is a 5% decrease in the DNA bond length Corresponding Authors
as the salt concentration is raised from 0.3 to 1 M (Figure 4A). *(C.A.M.) E-mail: [email protected].
*(M.O.C.) E-mail: [email protected].
ORCID
Soyoung E. Seo: 0000-0003-1593-4474
Chad A. Mirkin: 0000-0002-6634-7627
Notes
The authors declare no competing financial interest.

■ ACKNOWLEDGMENTS
We thank Dr. Andrew J. Senesi for his helpful discussion on
SAXS data analysis. This work was supported by the following
awards: the Center for Bio-Inspired Energy Science, an Energy
Frontier Research Center funded by the U.S. Department of
Energy, Office of Science, Basic Energy Sciences Award DE-
Figure 4. (A) The bcc unit cell lattice parameter at different salt SC0000989 (oligonucleotide syntheses and purification,
concentrations. (B) The change in lattice parameters induced by salt simulations); the Air Force Office of Scientific Research
is reversible. The arrows from (i) to (ii) and (iii) to (iv) show the Award FA9550-17-1-0348 (DNA-functionalization of gold
changes in lattice parameters after 1 to 0.3 M and 0.3 to 1 M salt nanoparticles); and the National Science Foundation’s
exchange, respectively.
Materials Research Science and Engineering Center program
(DMR-1121262) and made use of its Shared Facilities at the
Materials Research Center of Northwestern University (EM
characterization). SAXS experiments were carried out at
However, since the interactions between the DNA bonds and
beamline 5-ID of the DuPont-Northwestern-Dow Collabo-
ions are electrostatic in nature, the lattice parameters of these
rative Access Team at the Advanced Photon Source. Use of the
superlattices can be altered simply by salt exchange (Figure
Advanced Photon Source at Argonne National laboratory was
4B). By changing the salt concentration after the crystals are
supported by the U.S. Department of Energy, Office of
grown, the salt-induced transition in interparticle spacing is
Science, Office of Basic Energy Sciences, under Contract No.
fully reversible, and SAXS patterns collected before and after
DE-AC02-06CH11357 (SAXS characterization). S.E.S. ac-
salt exchange do not show noticeable changes in the SAXS
knowledges partial support from the Center for Computation
peak widths (Figures 4, S13).
and Theory of Soft Materials Fellowship.

■
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191 DOI: 10.1021/acscentsci.8b00826

ACS Cent. Sci. 2019, 5, 186−191