Conformational Switching of Chiral Colloidal Rafts Regulates Raft–Raft Attractions and Repulsions
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Conformational switching of chiral colloidal rafts regulates raft–raft attractions and repulsions Joia M. Millera, Chaitanya Joshia, Prerna Sharmaa,b, Arvind Baskarana, Aparna Baskarana, Gregory M. Grasonc, Michael F. Hagana, and Zvonimir Dogica,d,1 aDepartment of Physics, Brandeis University, Waltham, MA 02454; bDepartment of Physics, Indian Institute of Science, Bangalore 560012, India; cDepartment of Polymer Science and Engineering, University of Massachusetts, Amherst, MA 01003; and dDepartment of Physics, University of California, Santa Barbara, CA 93106 Edited by Monica Olvera de la Cruz, Northwestern University, Evanston, IL, and approved June 19, 2019 (received for review January 25, 2019) Membrane-mediated particle interactions depend both on the membranes limits visualizing the nature of membrane-mediated properties of the particles themselves and the membrane envi- interactions and associated assembly pathways (17–26). ronment in which they are suspended. Experiments have shown Tunable depletion interactions enable the robust assembly that chiral rod-like inclusions dissolved in a colloidal membrane of monodisperse rod-like molecules into colloidal monolayer of opposite handedness assemble into colloidal rafts, which are membranes, structures that mimic many of the properties of the finite-sized reconfigurable droplets consisting of a large but pre- lipid bilayers yet are about 2 orders of magnitude larger (27–30). cisely defined number of rods. We systematically tune the chirality The 1-μm-thick colloidal membrane allows for direct visualization of the background membrane and find that, in the achiral limit, of inclusions within the membrane and the associated environ- colloidal rafts acquire complex structural properties and interac- mental deformations. For example, recent experiments have shown tions. In particular, rafts can switch between 2 chiral states of op- that chiral inclusions dissolved in a colloidal membrane of opposite posite handedness, which alters the nature of the membrane- chirality assemble into colloidal rafts, which are micrometer-sized – mediated raft raft interactions. Rafts with the same chirality have deformable liquid droplets consisting of a large but precisely de- long-ranged repulsions, while those with opposite chirality acquire fined number of rods (31–33). Here, we show that colloidal rafts attractions with a well-defined minimum. Both attractive and repul- can assemble even in achiral membranes and that such rafts can SCIENCES sive interactions are qualitatively explained by a continuum model switch between 2 distinct chiral states. Furthermore, we show that APPLIED PHYSICAL that accounts for the coupling between the membrane thickness interconverting between these 2 conformational states switches the and the local tilt of the constituent rods. These switchable interac- effective raft–raft pair interaction from a long-ranged repulsion to tions enable assembly of colloidal rafts into intricate higher-order a short-ranged attraction. These conformationally switchable self- architectures, including stable tetrameric clusters and “ionic crystal- assembled mesoscopic structures and interactions drive formation lites” of counter-twisting domains organized on a binary square lattice. Furthermore, the properties of individual rafts, such as their of diverse higher-order reconfigurable assemblages. Using the- sizes, are controlled by their complexation with other rafts. The oretical modeling, we show that the complex interaction behav- emergence of these complex behaviors can be rationalized purely ior can be explained by considering the coupling between the in terms of generic couplings between compositional and orienta- shape of raft interfaces and the tilt field of colloidal rods within tional order of fluids of rod-like elements. Thus, the uncovered prin- the membrane. We find that a minimal symmetry-based model of ciples might have relevance for conventional lipid bilayers, in which phase-separated and tilted membranes qualitatively describe most the assembly of higher-order structures is also mediated by complex membrane-mediated interactions. Significance self-assembly | membranes | liquid crystals | colloids We describe hierarchical assemblages of colloidal rods that mimic some of the complexity and reconfigurability of bi- hen suspended in a bulk isotropic liquid, colloids interact ological structures. We show that chiral rod-like inclusions Wby forces that have steric, electrostatic, or entropic origins dissolved in an achiral colloidal membrane assemble into rafts, (1). In comparison, the same particles suspended in an aniso- which are adaptable finite-sized liquid droplets that exhibit tropic liquid crystals, or at a fluid interface, distort their envi- 2 distinct chiral states of opposite handedness. Interconverting ronment and thus acquire fundamentally different interactions. between these 2 states switches the membrane-mediated raft interactions between long-ranged repulsions and attractions. For example, colloids in a liquid crystal alter the nematic director Rafts with switchable interactions assemble into analogs of field, generating topological defects, which lead to unique long- electrostatic complexation observed in charged particulate range interactions that drive the assembly of complex architec- matter. Our results demonstrate a robust pathway for self- – – tures (2 5). Colloids bound to oil water interfaces provide an- assembly of reconfigurable colloidal superstructures that does other example in which long-ranged attractive or repulsive not depend on tuning the shape and interactions of the ele- interactions are caused by the interface deformations. These in mental units, but rather on the complexity of the emergent turn are determined by how the interface wets the colloids (6, 7). membrane-mediated interactions. Lipid membranes provide a complex environment that combines both liquid crystalline-like anisotropy due to the alignment of the Author contributions: J.M.M. and Z.D. designed research; J.M.M., C.J., and Arvind Baskaran performed research; P.S. acquired preliminary data; J.M.M., C.J., Arvind Baskaran, Aparna fatty chains and interface deformations due to effective 2D Baskaran, and G.M.G. analyzed data; and J.M.M., M.F.H., and Z.D. wrote the paper. confinement (8). Inclusions distort both the membrane thickness The authors declare no conflict of interest. and the chain alignment, leading to interactions that are even This article is a PNAS Direct Submission. more multifaceted than those observed for colloids in liquid Published under the PNAS license. – crystals or on interfaces (9 12). For example, even inclusions 1To whom correspondence may be addressed. Email: [email protected]. with purely repulsive interactions may form stable clusters due to This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the interplay of overlapping regions of membrane deformation in 1073/pnas.1900615116/-/DCSupplemental. lipid bilayers (13–16). However, the nanometer size of lipid www.pnas.org/cgi/doi/10.1073/pnas.1900615116 PNAS Latest Articles | 1of10 Downloaded by guest on September 30, 2021 of the experimental observations. Our results demonstrate how mains of either handedness have the same spacing. This criterion properties of the membrane environment can be tuned to generate reveals that colloidal membranes composed of 63% Y21M and complex self-assemblages from structurally simple building blocks. 37% wt rods are effectively achiral. Based on these findings, we define the chiral parameter: ϕch = ðrM13KO7 − 0.37Þ=0.63, where Assembly of Rafts in Achiral Colloidal Membranes rM13KO7 = nM13KO7=ðnM13KO7 + nM13KO7−Y21M Þ, is the fraction of fd We used M13KO7 and bacteriophage, which are both rod-like left-handed rods, and nM13KO7 and nM13KO7−Y21M are the concen- colloidal particles with ∼7-nm diameter and 2.8-μm persistence trations of long rods. For achiral mixtures, ϕch = 0,while ϕch = 1 length (34). M13KO7 is 1,200 nm long, while fd-wt is 880 nm indicates maximally left-handed rod composition. Achiral colloidal long. Addition of a nonadsorbing polymer to a virus solution membranes composed of fd-wt and fd-Y21M exhibit an edge in- induces attractive interactions, causing the viruses to assemble stability that is consistent with the absence of rod twist (40). into colloidal membranes, which are liquid-like monolayers of Colloidal membranes comprised of a uniform mixture of rods rods, aligned lengthwise, with lateral dimensions reaching hun- of opposite chirality, such as M13KO7 and fd-Y21M, force the dreds of microns (27, 28). Local twisting of rods as preferred by constituents within the membrane interior to untwist. However, their intrinsic chirality is fundamentally incompatible with the rods with opposite chirality and different lengths can form chiral global constraints of the 2D membrane geometry. Consequently, colloidal rafts that allow the twist to penetrate the membrane all of the rods within the membrane interior are forced into a interior and thus lower the system free energy. These colloidal higher-energy untwisted state, while rods within a twist pene- rafts are finite-sized equilibrium droplets of 1-handedness and tration length of the membrane edge are free to twist and thus length that coexist with the background membrane of the op- lower their energy (35). This frustration leads to chiral control of posite handedness and different thickness (31). The finite twist at the membrane edge tension (36). a raft’s edge decays