Hybrid Nano-Object Assembly: Equilibrium and Non-Equilibrium Organization, Notas de estudo de Engenharia de Produção

Baixe Hybrid Nano-Object Assembly: Equilibrium and Non-Equilibrium Organization e outras Notas de estudo em PDF para Engenharia de Produção, somente na Docsity! nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials 781 review article Published online: 6 sePtember 2009 | doi: 10.1038/nmat2496 Nanoscale objects are the focus of much attention not only as critical components in the emergence of cellular life1, but as small-scale materials with advanced functions and proper- ties that can be isolated or assimilated into numerous applications, such as in bioelectronics, sensing, drug delivery, catalysis and nano- composites2–6. In this review, we focus on hybrid nano-objects that are constructed by using organic components to coordinate the nucleation, growth, organization and transformation of inorganic nanophases to produce discrete integrated objects or higher-order structures under equilibrium or non-equilibrium conditions. Using illustrative examples, we systematize the concepts that underpin these assembly processes, and discuss theoretical considerations. integrative self-assembly We begin by surveying present strategies used to coordinate the structure and organization of discrete hybrid nano-objects under equilibrium conditions5,7. These materials consist of inorganic nano- components, such as metals (Au, Ag), metal-ion salts (Ca3(PO4)2, CaCO3), quantum dots (CdS), magnetic (Fe3O4) and photo active (TiO2) oxides, and glassy solids (SiO2), which are chemically integrated with discrete organic nano structures. We classify the construction processes leading to single nano-objects as ‘inte grative self-assembly’, and identify three systematic approaches: nano scale incarceration, supramolecular wrapping and nano structure templating (Fig. 1a–d). Nanoscale incarceration. In general, hybrid nano-objects com- prising entrapped inorganic components necessitate the pre- organization of persistent self-assembled organic architectures with hollow accessible interiors. An important archetype of this approach is the use and application of the capsid-like protein, apoferritin, for the controlled nucleation and confinement of inorganic nano- particles8. Addition of various inorganic reaction mixtures under appropriate conditions (such as low concentrations, slow reaction rates, substoichiometric ratios and so on) has led to the synthetic construction of a wide range of novel protein-encapsulated core– shell hybrid nano-objects; most recently, these include ferritins with incarcerated nanoparticles of CaCO3 (ref. 9), PbS (ref. 10), Ag self-assembly and transformation of hybrid nano-objects and nanostructures under equilibrium and non-equilibrium conditions stephen mann Understanding how chemically derived processes control the construction and organization of matter across extended and multiple length scales is of growing interest in many areas of materials research. Here we review present equilibrium and non- equilibrium self-assembly approaches to the synthetic construction of discrete hybrid (inorganic–organic) nano-objects and higher-level nanostructured networks. We examine a range of synthetic modalities under equilibrium conditions that give rise to integrative self-assembly (supramolecular wrapping, nanoscale incarceration and nanostructure templating) or higher- order self-assembly (programmed/directed aggregation). We contrast these strategies with processes of transformative self- assembly that use self-organizing media, reaction–diffusion systems and coupled mesophases to produce higher-level hybrid structures under non-equilibrium conditions. Key elements of the constructional codes associated with these processes are identified with regard to existing theoretical knowledge, and presented as a heuristic guideline for the rational design of hybrid nano-objects and nanomaterials. (ref. 11) and In (ref. 12), as well as Pd (ref. 13) or CoPt (ref. 14) for use in catalytic hydrogenation and magnetic storage, respectively. Similar approaches have been developed using viral capsids15–17. In both systems, inorganic reactants permeate the polypeptide shell through molecular channels within the self-assembled architec- ture, and nucleation occurs specifically within the internal cavity. Although molecular diffusion into the ferritin cage is passive, pH- induced swelling of the shell of cowpea chlorotic mottle virus can be used to access the internal environment16. Interestingly, under cer- tain conditions, the above protocols can be run in reverse such that preformed inorganic nanoparticles of appropriate size, shape and surface functionality can be used as platforms for the self-assembly of viral coat proteins15 or apoferritin subunits10. For example, coat proteins assemble spontaneously around gold nanoparticles func- tionalized with anionic moieties, specific nucleic-acid packaging signals, or a monolayer of carboxy-terminated polyethylene gly- col18–20 (Fig. 2a). Nanoscale incarceration of inorganic components within inte- grated hybrid objects can also occur under special conditions by confinement within lyotropic organic mesophases that are con- strained in particle size. Although less common than cage-mediated entrapment, this process is intriguing as the hybrid nano-objects do not adopt core–shell architectures but instead have unusual meso- structured interiors. For example, quenching of synthesis mixtures of cationic amphiphiles and silicon alkoxides by rapid aerosol drying gives rise to the spontaneous co-assembly of spherical silica– surfactant nanoparticles with ‘onion-like’ internal architecture, in which the inorganic phase is incarcerated within a concentrically arranged lamellar mesostructure21 (Fig. 2b). In contrast, rapid dilu- tion and neutralization of analogous reaction mixtures produces oblate ellipsoidal nanoparticles of the hexagonally ordered silica– surfactant mesophase MCM-41, which have a highly unusual modulated mesostructure owing to structure-induced shape transformations during nucleation22 (Fig. 2c). Supramolecular wrapping. In this approach, supramolecular assemblies or macromolecules with well-defined persistent Centre for Organized Matter Chemistry, School of Chemistry, University of Bristol, Bristol BS8 1TS, UK. e‑mail: s.mann@bris.ac.uk nmat_2496_OCT09.indd 781 14/9/09 09:52:11 © 2009 Macmillan Publishers Limited. All rights reserved 782 nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials review article NatUre materials doi: 10.1038/nmat2496 three-dimensional architectures are enveloped in a continuous inorganic coating under near-equilibrium conditions to produce discrete core–shell hybrid nano particles23. This approach is related to templating strategies (see below), but is differentiated by the con- tinuous nature of the inorganic component and general absence of surface patterning. Sol–gel reactions, particularly those involving the hydrolysis and condensation of silica precursors, seem to be very compatible with high-fidelity wrapping. For example, organo- gel nanostructures have been successfully transcribed into silicified hybrids with cylindrical24 or helical morphology25, and similar pro- cedures have been used to prepare silica-coated porphyrin-based nanotapes26,27 and collagen fibrils28. Increasing attention is being placed on maintaining the func- tionality of the organic architectures after silica-shell wrapping to produce core–shell hybrids with integrated properties. Ideally, the organic functionality should be retained after assimilation of the inorganic component, and remain accessible to external stimuli such as changes in pH or optical excitation27. In practice, these triggers are transmitted to the embedded organic nanostructure through nanopores in the ultrathin silica envelope, thereby enabling collective functions to operate within a single hybrid nano-object. Significantly, these experimental protocols have been extended to the silica/organoclay wrapping of single molecules of polysaccha- rides29,30, proteins30–32, enzymes31,33 and DNA32 (Fig. 2d). In each case, the wrapped biomolecules remain structurally intact and maintain their functionality even under adverse conditions. Nanostructure templating. A wide range of self-assembled organic architectures have been used as supramolecular templates for the construction of original hybrid nano-objects under equilibrium conditions. In general, slow reaction rates — aided by, for exam- ple, low levels of supersaturation and reactant concentrations — are used to facilitate favourable inter actions specifically at the organic surface so that nanoscale inorganic deposition occurs preferen- tially along the accessible surfaces of the template (Fig. 2e). This site selectivity is improved in many cases by sequential exposure of the preorganized organic nanostructure to the individual inorganic reactants34. In practice, this often involves the substoichiometric binding of metal cations to the template surface, followed by adding ions/molecules that trigger inorganic deposition or crystallization. These procedures are particularly effective for the templating of metal or semiconductor nano particles within spherical objects such as dendrimer nano particles35, or on the surface of highly anisotropic biological nanostructures such as DNA36 and self-assembled micro- tubules37. Similarly, arrays of Au, Ag or Pt nanoparticles have been prepared by in situ deposition on the external or internal surface of rod-shaped tobacco mosaic virus particles34,38,39. As these hybrids are uniform in length and width, mechanically robust and accessible to physical manipulation, they may have important technological uses as components of digital memory devices39 or as electrically conducting nanowires40. A diverse range of synthetic organic molecules has been used to prepare anisotropic nanostructures (such as filaments, tubes, helicoids and so on) that promote the template-directed assembly of integrated hybrid nanoscale objects under equilibrium condi- tions. Some representative examples include chiral lipids41,42, pep- tide-based surfactants43,44, block copolymers45,46, dendron rod–coil triblocks47,48 and T-shaped dendro-calixarene amphiphiles49 (Fig. 3). Self-assembling peptides with sequences programmed to have appropriate polar or charged surface amino acid residues50,51 that induce β-sheet (amyloid) formation52,53, or initiate coiled-coil inter- molecular interactions54, have also been investigated. In many cases, these molecules self-assemble in water into nanostructured objects by enthalpic and entropic processes, and adopt highly anisotropic architectures because of the intricacies of molecular shape and size, and specificity of the intermolecular interactions. In general, the above amphiphiles and peptides show certain key characteristics that are designed into the molecular structure to facilitate their use as effective templates for nanoscale inorganic ba c ed 50 nm 80 nm 30 nm 20 nm a b c d e f Figure 1 | Present approaches to the construction and organization of discrete hybrid nano-objects under equilibrium conditions. a–d, Integrative assembly. Nanoscale incarceration by confinement of inorganic reactions within preformed supramolecular organic containers (a), or by self‑assembly of organic subunits around preformed inorganic nanoparticles (b). Wrapping of supramolecular organic nano‑objects with ultrathin inorganic shells (c). Site‑directed templating of inorganic components on organic nanostructures (d). e,f, Higher‑order assembly of unitary nano‑object constructs by programmed aggregation (e), and extended nanostructures by multicomponent reconstitution (f). Figure 2 | transmission electron microscopy (tem) images of hybrid nano-objects produced by integrative self-assembly. a, Nanoscale incarceration of a single preformed gold particle by self‑assembly of viral coat proteins20. b,c, Incarceration of SiO2 within nanoparticles of ordered lyotropic surfactant mesophases showing interiors with concentric lamellae (b)21, and a modulated hexagonal structure (c)22, viewed side‑on. d, Supramolecular wrapping of a single‑plasmid DNA molecule in a continuous ultrathin shell of condensed organoclay oligomers32. e, Template‑directed deposition of gold nanoparticles on the surface of a nanostructured tobacco mosaic virus rod‑like particle to produce metallized biostructures with high shape anisotropy34. Figures reproduced with permission: a, © 2006 ACS; b, © 1999 NPG; c, © 2002 Wiley‑VCH; d, © 2007 ACS; e, © 2008 RSC. nmat_2496_OCT09.indd 782 14/9/09 09:52:13 © 2009 Macmillan Publishers Limited. All rights reserved nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials 785 review articleNatUre materials doi: 10.1038/nmat2496 or non-interacting spherical nanoparticles, which produces close-packed, high-symmetry arrangements, typical of many col- loidal nano crystals prepared by evaporation-induced assembly from organic solvents containing hydrophobically functionalized inorganic nanoparticles2,3. The hydrophobic and near-contact van der Waals attractive energies are proportional to e–d/λ and 1/d respectively (d = distance between surfaces, λ = 1–2 nm)70. Moreover, high perfection in lattice ordering demands stringent levels of uniformity in particle size and shape, which are often difficult to achieve synthetically. Interestingly, incarceration of inorganic nanoparticles in spherical capsid-like architectures (for example, ferritin, cowpea brome mosaic virus) can circumvent problems associated with polydispersity of the inorganic phase, as well-defined molecular interactions between the protein shells override the imperfections to produce very accurate placement of the hybrid nanoparticles71. Deviations from close packing of spherical nanoparticles can be accomplished under certain conditions — for example, low-density diamond-like lattices have been assembled from strongly electrostat- ically interacting spherical nanoparticles in the presence of counter- ion screening effects72, where the attractive/repulsive energies scale proportionally with eκ/r (r = distance between ions, κ–1 = screen- ing length)70. However, it is generally true that increased levels of organization in nanoparticle-based higher-level structures require interparticle specificity and directionality. Specificity is increased considerably in systems comprising spherical nano-objects by pro- grammed aggregation using DNA-based coupling with appropriate design of biomolecular linkers and thermal pathways73,74. a b d c gf Au 100 nm ATP Release Mg2+ + K+ e 400 nm 100 nm 100 nm 100 nm Figure 4 | Higher-order assembly of nanoscale hybrid objects. a–e, Self‑assembly of unitary nano‑objects. a, Programmed aggregation based on DNA‑directed attachment of gold‑nanoparticle satellites to single nanoparticles of mesoporous silica59. b, Coupling of oligonuceotide‑functionalized gold nanoparticles to ferritin molecules adsorbed onto the surface of a CNT through a streptavidin linker62. The TEM image shows the specific disassembly of the gold nanoparticles (imaged as larger dark dots) by heat‑induced dehybridization of the DNA linkages. The iron oxide cores of ferritin (smaller, less‑ dense spots) remain firmly attached to the CNT platform. c, Scheme showing triggered release of a single semiconductor nanoparticle from a chaperonin– CdS nanoconstruct63. d, Patterned electrostatic assembly of gold nanoparticles on individual block‑copolymer cylindrical co‑micelles of (4). e, Scheme showing self‑assembly of a gold/chaperonin ring‑shaped architecture from gold‑nanoparticle‑tagged protein subunits68. f,g, Higher‑order extended structures. f, TEM image showing spontaneous assembly of linear chain of spherical gold nanoparticles with branching bifurcations77. The graphic illustrates dipolar interactions associated with ligand partitioning on the gold nanoparticle surfaces. g, Mesocrystal of BaCO3 showing helical stacking of iso‑oriented crystals produced by selective adsorption of a phosphonated double hydrophilic poly(ethylene oxide‑oxabutylacrylate ester) block copolymer onto the (110) face of the nanocrystals during aqueous precipitation91. Figures reproduced with permission: a, © 2005 Wiley‑VCH; b, © 2005 RSC; c, © 2003 NPG; d, © 2007 ACS; e, © 2002 NPG; g, © 2005 NPG. nmat_2496_OCT09.indd 785 14/9/09 09:52:15 © 2009 Macmillan Publishers Limited. All rights reserved 786 nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials review article NatUre materials doi: 10.1038/nmat2496 Alternatively, higher-order arrays of hybrid nano-objects with considerable spatial directionality can be constructed by exploiting interparticle dipole–dipole interactions. Significantly, when these interactions are dominant over competing interparticle forces — for example, for particles with considerable intrinsic magnetic75 or electric dipoles76 — then one-dimensional linear chains of iso- metric nanoparticles self-assemble spontaneously in the dispersed medium. Chain assembly can be facilitated also by modifications in the hybrid nature of the nanoparticles. For example, reducing the screening effect of the organic stabilization layer that surrounds spherical CdTe semiconductor nanoparticles promotes linear chain aggregation owing to increases in the interparticle electric dipole–dipole interactions76. Unlike semiconductor quantum dots, face-centred-cubic metallic nanoparticles show no intrinsic electric dipole, yet gold nano particles spontaneously assemble into linear arrays when conjugated with several types of surface-attached ligands77,78 (Fig. 4f). Clustering of the organic molecules into discrete domains on the inorganic surface produces an extrinsic electric dipole that is sufficient to align the nanoparticles through cumu- lative dipolar interactions to produce linear chains and networks showing plasmonic coupling6,77. In contrast to spherical nano-objects, the construction of spatially aligned higher-level superstructures from components with considerable shape anisotropy, such as nano-sheets and nano- rods, is inherently directional owing to entropic ordering79. As a consequence, nanoparticles such as hydrophobically stabilized Au (ref. 80), Co (ref. 81) or BaCrO4 (ref. 82) nanorods will sponta- neously self-assemble into linear chains by side-on ordering. The ordering process is further enhanced by enthalpic processes related to intermolecular interactions between the surface-adsorbed sur- factant molecules on the side faces of neighbouring nanoparticles. These can result, for example, in the formation of an interdigitated bilayer between adjacent particles in the assembled superstructure, particularly if the nanorods have well-defined crystal faces82. Recent studies have developed this concept by attaching polystyrene mol- ecules specifically to the end faces of surfactant-coated gold nano- rods83. Similarly, enthalpy-driven interactions are often used for the spontaneous assembly of ordered mesolamellar structures from dispersions of hybrid nanosheets. For example, electrostatic inter- actions between dispersed polymer-stabilized graphene sheets have been used to promote the assembly of novel nanostructures in the form of electrically conductive thin films84 and DNA-intercalated bio-nanocomposites85. Mesocrystals. The above examples consider systems of higher-order equilibrium assembly of spherical or anisotropic hybrid nano-objects, in which the inorganic-based building components are intrinsically stable with respect to structural transformation and interparticle fusion. There are however, a growing number of reports of non- classical crystallization processes involving the oriented attachment and partial fusion of nanoscale hybrid units86, which result in the formation of mesocrystals that are crystallographically continu- ous and morphologically well-defined in three dimensions87. These crystals consist of an iso-oriented higher-order superstructure of coherently interconnected nanoscale inorganic domains with inter- calated organic constituents — usually in the form of water-soluble polymers — that together significantly influence both the texture and mechanical properties. Mechanistically, binding of the organic mac- romolecules to crystal faces of the primary inorganic nano particles produces hybrid conjugates with shape and surface modifications that promote coordinated aggregation of the superstructure with high levels of orientational, but not positional, order87–90. Remarkably, the latter can be strongly influenced by macro molecular encoding of a subset of the crystal faces of the primary nanoparticles, with the con- sequence that non-geometric forms such as helical microstructures are spontaneously propagated by vectorial aggregation91 (Fig. 4g). How the nanocrystalline subunits attain such high levels of alignment is not known. However, it seems likely that the interplay between the minimization of the nanoparticle surface energy by fusion and coherent extension of the crystal lattice, and the steric- repulsion energy associated with the adsorbed polymers in the confined medium, is an important factor in this coordinated proc- ess of alignment. As the steric-repulsion energy is proportional to e−d/R (R = radius of gyration)70, both polymer structure and packing density within the aggregates at the early stages of their formation must be important considerations. Furthermore, polarization forces and dipole fields have been proposed as mechanisms for mediating the alignment process92,93. As these competing forces are operating under near-equilibrium conditions, the perturbations caused by the ordering process are minimal and locally confined. In contrast, major structural modifications might be expected if the aggregated nanoparticle subunits and organic constituents are metastable and coupled through in situ phase transformations. This and other examples of non-equilibrium self-assembly involving nanoscale hybrid building blocks are discussed in the following sections. transformative self-assembly The prescriptive nature of equilibrium-based strategies of integrative self-assembly limits the versatility to which multiple length scales and higher-order complexity can be embedded within the result- ing hybrid constructs. In contrast, divergent pathways of construc- tion involving nano-objects that undergo spontaneous ordering or transformation across several length scales can result in complex hierarchical states88. We classify these processes as ‘transforma- tive self-assembly’ to distinguish their nonlinearity and emergent behaviour from mechanisms of higher-order self-assembly oper- ating under equilibrium conditions. Three systematic approaches involving self-organizing media, reaction–diffusion systems or cou- pled-mesophase transformations, are highlighted below. Nanoscale ordering in self-organizing media. Many non- equilibrium systems spontaneously transform into complex patterns and forms because of instability thresholds associated with spatio– temporal gradients in temperature, pressure, viscosity and chemi- cal potential94. Some of these processes, such as viscous fingering, diffusion-limited aggregation, myelination, vortexation and foam generation, produce self-organized media that in principle could be exploited for the non-equilibrium self-assembly of inorganic nano-objects into materials with spatial patterns and complex mor- phologies. For example, sol–gel reactions have been coupled with the spontaneous formation of myelin-like tubular structures of the diblock copolymer amphiphile, poly(ethylene oxide)-b-poly(1,2- butylene oxide)95. The myelin outgrowths, which are metastable intermediates between the gel-like lamellar phase and dispersed multilamellar vesicles, are trapped in the form of highly anisotropic silica–polymer hybrid nanotubes by the addition of tetraethoxysi- lane to the polymer gel before immersion in water (Fig. 5a). As a con- sequence, chaotic outgrowth of the multilamellar myelin filaments is concurrent with silica deposition at the polymer/water interface to produce mineralized replicas of the emergent nanostructures. Other studies have exploited microphase partitioning to enforce the spatial confinement and organization of nanoscale objects. For example, a wide range of hierarchically organized monolithic mate- rials (for example, SiO2, V2O5 and TiO2) have been produced using air–liquid foams in association with sol–gel chemistry96,97. In many cases, the scaffold walls consist of coherently packed inorganic nanoparticles and are often porous across a range of length scales. Significantly, changing the drainage properties of the foams by alter- ing the their liquid fraction results in modifications in the curvature and dimensions of the plateau border, which in turn influence the shape and size of the self-organized polygonal framework. A similar approach, in which viscous dextran gels containing metal salts or nmat_2496_OCT09.indd 786 14/9/09 09:52:15 © 2009 Macmillan Publishers Limited. All rights reserved nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials 787 review articleNatUre materials doi: 10.1038/nmat2496 inorganic nano particles are decomposed into foams under slow thermal processing has been recently reported98 (Fig. 5b). Reaction–diffusion systems. Diffusion-limited reaction fronts comprising spatially and temporally coupled chemical gradients have been reported for a wide range of non-equilibrium phenom- ena99. In general, pattern formation depends on the competition and delicate balance between reaction and diffusion, and can be described mathematically by a set of partial differential equations that account for the spatio–temporal distribution of concentrations in open and closed nonlinear systems100. Significantly, the resulting concentration patterns may become fixed in time and space to pro- duce persistent structures with complex organization101–105. Thus, it seems feasible that reaction–diffusion structures could be used in numerous systems to organize nanoscale components into patterned arrangements not readily accessible by equilibrium processes. For example, several studies have demonstrated that patterned arrange- ments of inter connected inorganic nanoparticles can be spontane- ously produced by injecting a liquid metal alkoxide into aqueous ammonium hydroxide (Fig. 5c)106–108. The studies indicate that the ordering process is dependent on the spontaneous formation of a thin semi-permeable metal oxide membrane at the alkoxide/water interface, followed by subsequent spatio–temporal patterning of the nanoparticulate product by microphase separation along the diffusion-limited reaction front. It is well established that time- and spatial-dependent oscillations in reactant concentrations and conditions are accentuated when supersaturated solutions are contained within viscous media such as silica or polymer hydrogels, and that such systems produce macro- scale precipitation patterns often with banded or periodic organiza- tion109,110 (Fig. 5d). Grzybowski and colleagues have exploited this process to prepare planar materials with spatial gradients, multi- colour nanopatterns and multilevel surfaces by using agarose stamps to transfer a reactant solution into films of dry gelatine doped with a co-reactant99. Such materials have been developed as prototypes for static sensing, for example to detect changes in molecular con- figuration by modifications in the mass-transfer properties of thin gelatin films111. Significantly, recent studies have shown that many of the long- range patterns produced in viscous polymer gels are constructed from the hierarchical ordering of nano-sized particles and crystal- lites112–114. Organization of the nano-objects within the viscous envi- ronment is dependent to a large extent on the interplay between internal forces (crystallization) and external fields associated with diffusion–precipitation fronts that propagate through the system. The studies indicate that these factors are strongly influenced by the morphology and chemical activity of the system. For example, radial patterns comprising regular bands of crystallographically ordered CaCO3 nanocrystallites are predominant in thin hydrogel films con- taining poly(acrylic acid) (PAA) owing to the continuous nature of the reaction medium112 (Fig. 5e), whereas crystallization of amor- phous CaCO3 particles in the presence of poly(styrene sulphonate) produces hollow microspheres by spontaneous redistribution of matter from the interior to the outer surface115 (Fig. 5f). In the latter g dca b fe 500 nm 100 µm 5 µm 1 cm 1 µm 1 µm 100 µm Figure 5 | Non-equilibrium spontaneous assembly of hybrid nanostructures. a,b, Use of self‑organized media. TEM image showing SiO2–polymer nanotubes formed by myelination of poly(ethylene oxide)‑b‑poly(1,2‑butylene oxide)–tetraethoxysilane gel particles in water (a)95, and scanning electron microscopy (SEM) image showing a polyhedral framework of zeolite and SiO2 nanoparticles produced by microphase separation and spatial patterning within the interstitial voids of a dextran‑derived foam of CO2 gas bubbles (b)98. c–g, Examples of reaction–diffusion systems in higher‑order self‑assembly of nanostructures. c, Hierarchically ordered TiO2 produced by non‑equilibrium sol–gel reactions. The SEM image shows the cross‑section of the internal structure of a macroscopic TiO2 fibre comprising a de‑mixed arrangement of ordered capillaries and nanostructured walls106. d, Optical image showing macroscopic ordering of iron oxide (white rust) in agar gel produced by diffusion–reaction precipitation of Fe(ii)/Fe(iii) under the influence of a pH gradient (reproduced with permission from www.damtp.cam.ac.uk/user/gold/research.html). e, SEM image showing periodic patterning of oriented calcium carbonate (calcite) nanoscale needle‑like crystals in a spin‑coated hydrogel of cholesterol‑functionalized pullulan containing poly(acrylic acid). The bands are about 0.8 μm in width, and the calcite crystals are aligned along the crystallographic c axis112. f, SEM image showing a partially broken CaCO3 hollow microsphere prepared by spontaneous self‑transformation at 70 °C and pH 10.5 in the presence of poly(styrene sulphonate). The shell wall consists of vaterite nanocrystallites115. g, SEM image of a hierarchically ordered K2SO4 superstructure produced by evaporation‑induced crystallization in the presence of poly(acrylic acid). The image shows the macroscopic scaffold constructed from the episodic deposition of plates interspaced with polycrystalline columns of K2SO4 crystallites117. Figures reproduced with permission: b, © 2004 Wiley‑VCH; e, © 2003 Wiley‑VCH; g, © 2005 Wiley‑VCH. nmat_2496_OCT09.indd 787 14/9/09 09:52:17 © 2009 Macmillan Publishers Limited. All rights reserved 790 nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials review article NatUre materials doi: 10.1038/nmat2496 In contrast to the above processes, non-equilibrium processes of higher-order nanoscale construction typically involve diver- gent pathways of assembly. The numerous length scales contained within these complex structures necessitate construction pathways that are system-generated and cumulative, non-prescriptive with regard to the initial state, and highly sensitive to small changes in intrinsic and extrinsic factors (Table 1). As we have discussed, these systems typically involve temporal- and spatial-dependent coupling of several constituents that sustain and propagate the spontaneous ordering and transformation of hybrid nano-objects without the apparent intervention of any principal organizing factor. Unfortunately, such strategies are not readily amenable to system- atic evaluation because of the inherent complexity associated with these emergent systems. Indeed, although progress has been made in understanding many aspects of non-equilibrium self-assembly across several length scales99,132, there still seems to be no coherent theory of these systems. In general, emergent structures and non-equilibrium pattern formation derive from the interplay between competitive and cooperative processes, under the imposition of local constraints, associated for example with diffusion-limited reaction fields, and maintained by energy dissipation99,133. The pathways show no deter- ministic dependence on the starting conditions or nature of the initial reactants and building blocks; instead they are contingent on many factors that together influence the type and transforma- tion of instability thresholds in the free-energy landscape. Typically, these include symmetry breaking, microphase separation, selection pressures between various intermediates, and the interplay between collective correlations and non-equivalence in the size of the com- ponents94. Such nonlinear factors are highly demanding with regard to the information-generating capacity of a system, and are there- fore dependent on a continuous flux and dissipation of energy to maintain complex interactions between many components. These attributes are characteristic of living systems, and it is expedient to compare the static non-equilibrium hybrid nanostructures we have described in this review with the dynamic and adaptive nature of biologically assembled materials. The latter are delicately poised in metastable states so that they can respond effectively, both structur- ally and functionally, to external stimuli to generate processes such as force transmission, motility, self-healing and self-replication1. These non-equilibrium states are maintained through biochemical networks that are displaced from equilibrium by coupling chemical reactions with diffusion-limited membrane-transport processes. In terms of a possible synthetic analogy, this would necessitate that the construction and transformation of nanoscale objects are controlled and directed by interactive linkages to a non-equilibrium chemical network that is capable of adapting to changes in environmental con- ditions, and feeding these back into correlated modifications in the structural and functional states of the hybrid material. For example, the coupling of an oscillating chemical reaction with a precipitation– dissolution process has been recently described134, and Grzybowski and colleagues have suggested coupling pH-driven nanoparticle assembly with a chemical-clock reaction cycling between acidic and alkaline pH values70. The development of many of the processes described in this review, as well as the extension of our theoreti- cal understanding of non-equilibrium self-assembly, will no doubt facilitate the realization of such ambitious research goals. references 1. Mann, S. Life as a nanoscale phenomenon. Angew. Chem. Int. Ed. 47, 5306–5320 (2008). 2. Shevchenko, E. V., Talapin, D. V., Kotov, N. A., O’Brien, S. & Murray, C. B. Structural diversity in binary nanoparticle superlattices. Nature 439, 55–59 (2006). 3. Wang, X., Zhuang, J., Peng, O. & Li, Y. D. A general strategy for nanocrystal synthesis. Nature 437, 121–124 (2005). 4. Mirkin, C. A. & Niemeyer, C. M. Nanobiotechnology II (Wiley-VCH, 2007). 5. Katz, E. & Willner, I. Integrated nanoparticle-biomolecule hybrid systems: synthesis, properties, and applications. Angew. Chem. Int. Ed. 43, 6042–6108 (2004). 6. Girard, C., Dujardin, E., Li, M. & Mann, S. Theoretical near-field optical properties of branched plasmonic nanoparticle networks. Phys. Rev. Letts. 97, 100801 (2006). 7. van Bommel, K. J. C., Friggeri, A. & Shinkai, S. Organic templates for the generation of inorganic materials. Angew. Chem. Int. Ed. 42, 980–999 (2003). 8. Yamashita, I. Biosupramolecules for nano-devices: biomineralization of nanoparticles and their applications. J. Mater. Chem. 18, 3813–3820 (2008). 9. Li, M., Viravaidya, C. & Mann, S. Polymer-mediated synthesis of ferritin- encapsulated inorganic nanoparticles. Small 3, 1477–1481 (2007). 10. Hennequin, B. et al. Biocompatible, aqueous near infrared fluorescent labels based on apoferritin-encapsulated PbS quantum dots. Adv. Mater. 20, 3592–3596 (2008). 11. Kramer, R. M., Li, C., Carter, D. C., Stone, M. O. & Naik, R. R. Engineered protein cages for nanomaterial synthesis. J. Am. Chem. Soc. 126, 13282–13286 (2004). 12. Okuda, M. et al. Self-organized inorganic nanoparticle arrays on protein lattices. Nano Lett. 5, 991–993 (2005). 13. Ueno, T. et al. Size-selective olefin hydrogenation by a Pd nanocluster provided in an apo-ferritin cage. Angew. Chem. Int. Ed. 43, 2527–2530 (2004). 14. Warne, B., Kasyuich, O. I., Mayes, E. L., Wiggins, J. A. J. & Wong, K. K. W. Self assembled nanoparticulate Co: Pt for data storage applications. IEEE Trans. Magn. 36, 3009–3011 (2000). 15. Aniagyei, S. E., DuFort, C., Kao, C. C. & Dragnea, B. Self-assembly approaches to nanomaterial encapsulation in viral protein cages. J. Mater. Chem. 18, 3763–3774 (2008). 16. Douglas, T. & Young, M. Host–guest encapsulation of materials by assembled virus protein cages. Nature 393, 152–155 (1998). 17. Liu, C. et al. Magnetic viruses via nano-capsid templates. J. Magn. Magn. Mater. 302, 47–51 (2006). 18. Loo, L., Guenther, R. H., Lommel, S. A. & Franzen, S. Encapsidation of nanoparticles by red clover necrotic mosaic virus. J. Am. Chem. Soc. 129, 11111–11117 (2007). 19. Goicochea, N. L., De, M., Rotello, V. M., Mukhopadhyay, S. & Dragnea, B. Core-like particles of an enveloped animal virus can self-assemble efficiently on artificial templates. Nano Lett. 7, 2281–2290 (2007). 20. Chen, C. et al. Nanoparticle-templated assembly of viral protein cages. Nano Lett. 6, 611–615 (2006). 21. Lu, Y. et al. Aerosol-assisted self-assembly of mesostructured spherical nanoparticles. Nature 398, 223–226 (1999). 22. Sadasivan, S., Fowler, C. E., Khushalani, D. & Mann, S. Nucleation of MCM-41 nanoparticles by internal reorganization of disordered and nematic-like silica- surfactant clusters. Angew. Chem. Int. Ed. 41, 2151–2153 (2002). 23. Perkin, K. K., Turner, J. J., Wooley, K. L. & Mann, S. Fabrication of hybrid nanocapsules by calcium phosphate mineralization of shell crosslinked polymer micelles and nanocages. Nano Lett. 5, 1457–1461 (2005). 24. Jung, J. H., Ono, Y. & Shinkai, S. Novel silica structures which are prepared by transcription of various superstructures formed in organogels. Langmuir 16, 1643–1649 (2000). 25. Jung, J. H., Ono, Y., Hanabusa, K. & Shinkai, S. Creation of both right-handed and left-handed silica structures by sol-gel transcription of organogel fibres comprised of chiral diaminocyclohexane derivatives. J. Am. Chem. Soc. 122, 5008–5009 (2000). 26. Tamaru, S., Takeuchi, M., Sano, M. & Shinkai, S. Sol-gel transcription of sugar-appended porphyrin assemblies into fibrous silica: unimolecular stacks versus helical bundles as templates. Angew. Chem. Int. Ed. 41, 853–856 (2002). 27. Meadows, P. J., Dujardin, E., Hall, S. R. & Mann, S. Template-directed synthesis of silica-coated J-aggregate nanotapes. Chem. Commun. 3688–3690 (2005). 28. Ono, Y. et al. Preparation of novel hollow fibre silica using collagen fibres as a template. Chem. Lett. 28, 475–476 (1999). 29. Numata, M. et al. Beta-1,3-glucan polysaccharide can act as a one-dimensional host to create novel silica nanofibre structures. Chem. Commun. 4655–4657 (2005). 30. Ichinose, I., Hashimoto, Y. & Kunitake, T. Wrapping of bio-macromolecules (dextran, amylopectin, and horse heart cytochrome c) with ultrathin silicate layer. Chem. Lett. 33, 656–657 (2004). 31. Patil, A. J., Muthusamy, E. & Mann, S. Synthesis and self-assembly of organoclay-wrapped biomolecules. Angew. Chem. Int. Ed. 43, 4928–4933 (2004). 32. Patil, A. J., Li, M., Dujardin, E. & Mann, S. Novel bioinorganic nanostructures based on mesolamellar intercalation or single molecule wrapping of DNA using organoclay building blocks. Nano Lett. 7, 2660–2665 (2007). 33. Kim, J. & Grate, J. W. Single-enzyme nanoparticles armored by a nanometer- scale organic/inorganic network. Nano Lett. 3, 1219–1222 (2003). 34. Bromley, K. M., Patil, A. J., Perriman, A. W., Stubbs, G. & Mann, S. Preparation of high quality nanowires by tobacco mosaic virus templating of gold nanoparticles. J. Mater. Chem. 18, 4796–4801 (2008). nmat_2496_OCT09.indd 790 14/9/09 09:52:19 © 2009 Macmillan Publishers Limited. All rights reserved nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials 791 review articleNatUre materials doi: 10.1038/nmat2496 35. Lemon, B. I. & Crooks, R. M. Preparation and characterization of dendrimer- encapsulated CdS semiconductor quantum dots. J. Am. Chem. Soc. 122, 12886–12887 (2000). 36. Manson, C. F. & Wooley, A. T. DNA-templated construction of copper nanowires. Nano Lett. 3, 359–363 (2003). 37. Behrens, S. et al. Nanoscale particle arrays induced by highly ordered protein assemblies. Adv. Mater. 14, 1621–1625 (2002). 38. Dujardin, E., Peet, C., Stubbs, G., Culver, J. N. & Mann, S. Organization of metallic nanoparticles using tobacco mosaic virus templates. Nano Lett. 3, 413–417 (2003). 39. Tseng, R. J. et al. Digital memory device based on tobacco mosaic virus conjugated with nanoparticles. Nature Nanotech. 1, 72–77 (2006). 40. Górzny, M. L., Walton, A. S., Wnek, M., Stockley, P. G. & Evans, S. D. Four-probe electrical characterization of Pt-coated TMV-based nanostructures. Nanotechnology 19, 165704 (2008). 41. Seddon, A. M., Patel, H. M., Burkett, S. L. & Mann, S. Chiral templating of silica-lipid lamellar mesophase with helical tubular architecture. Angew. Chem. Int. Ed. 41, 2988–2991 (2002). 42. Chappel, J. S. & Yager, P. Formation of mineral microstructures with a high aspect ratio from phospholipid bilayer tubules. J. Mater. Sci. Lett. 11, 633–636 (1992). 43. Yuwono, V. M. & Hartgerink, J. D. Peptide amphiphile nanofibres template and catalyse silica nanotube formation. Langmuir 23, 5033–5038 (2007). 44. Hartgerink, J. D., Beniash, E. & Stupp, S. I. Self-assembly and mineralization of peptide-amphiphile nanofibres. Science 294, 1684–1688 (2001). 45. Wang, H. et al. Cylindrical block co-micelles with spatially selective functionalization by nanoparticles. J. Am. Chem. Soc. 129, 12924–12925 (2007). 46. Wang, H. et al. Fabrication of continuous and segmented polymer/metal oxide nanowires using cylindrical micelles and block co-micelles as templates. Adv. Mater. 21, 1805–1808 (2009). 47. Sone, E. D., Zubarev, E. R. & Stupp, S. I. Semiconductor nanohelices templated by supramolecular ribbons. Angew. Chem. Int. Ed. 41, 1705–1709 (2002). 48. Sone, E. D., Zubarev, E. R. & Stupp, S. I. Supramolecular templating of single and double nanohelices of cadmium sulphide. Small 5, 694–697 (2005). 49. Perkin, K. K., Hirsch, A., Böttcher, C. & Mann, S. Nanoscale organization and patterning of cadmium sulphide quantum dots on structurally persistent dendro-calixarene micelles. Small 3, 2057–2060 (2007). 50. Yu, L. T., Banerjee, I. A., Shima, M., Rajan, K. & Matsui, H. Size-controlled Ni nanocrystal growth on peptide nanotubes and their magnetic properties. Adv. Mater. 16, 709–712 (2004). 51. Banerjee, I. A., Yu, L. T. & Matsui, H. Cu nanocrystal growth on peptide nanotubes by biomineralization: size control of Cu nanocrystals by tuning peptide conformation. Proc. Natl Acad. Sci. USA 100, 14678–14682 (2003). 52. Reches, M. & Gazit, E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300, 625–627 (2003). 53. Meegan, J. E. et al. Designed self-assembled beta-sheet peptide fibrils as templates for silica nanotubes. Adv. Funct. Mater. 14, 31–37 (2004). 54. Holmström, S. C. et al. Templating silica nanostructures on rationally designed self-assembled peptide fibres. Langmuir 24, 11778–11783 (2008). 55. Schnur, J. M. Lipid tubules: A paradigm for molecularly engineered structures. Science 262, 1669–1676 (1993). 56. Yan, X. H., Liu, G. J., Haeussler, M. & Tang, B. Z. Water-dispersible polymer/ Pd/Ni hybrid magnetic nanofibres. Chem. Mater. 17, 6053–6059 (2005). 57. Duxin, N., Liu, F. T., Vali, H. & Eisenberg, A. Cadmium sulphide quantum dots in morphologically tunable triblock copolymer aggregates. J. Am. Chem. Soc. 127, 10063–10069 (2005). 58. Kellermann, M. et al. The first account of a structurally persistent micelle. Angew. Chem. Int. Ed. 43, 2959–2962 (2004). 59. Sadasivan, S., Dujardin, E., Li, M., Johnson, C. J. & Mann, S. DNA- driven assembly of mesoporous silica/gold satellite nanoparticles. Small 1, 103–106 (2005). 60. Mirkin, C. A., Letsinger, R. L., Mucic, R, C. & Storhoff, J. J. DNA-based method for rationally assembling nanoparticles into macroscopic materials. Nature 382, 607–609 (1996). 61. Niemeyer, C. M. Nanoparticles, proteins, and nucleic acids: Biotechnology meets materials science. Angew. Chem. Int. Ed. 40, 4128–4158 (2001). 62. Li, M., Dujardin, E. & Mann, S. Programmed assembly of multi-layered protein/nanoparticle-carbon nanotube conjugates. Chem. Commun. 4952–4954 (2005). 63. Ishii, D. et al. Chaperonin-mediated stabilization and ATP-triggered release of semiconductor nanoparticles. Nature 423, 628–632 (2003). 64. Scheibel, T. et al. Conducting nanowires built by controlled self-assembly of amyloid fibres and selective metal deposition. Proc. Natl Acad. Sci. USA 100, 4527–4532 (2003). 65. Medalsy, I et al. SP1 protein-based nanostructures and arrays. Nano Lett. 8, 473–477 (2008). 66. Gottlieb, D., Morin, S. A., Jin, S. & Raines, R. T. Self-assembled collagen- like peptide fibres as templates for metallic nanowires. J. Mater. Chem. 18, 3865–3870 (2008). 67. Wang, Q., Lin, T., Tang, L., Johnson, J. E. & Finn, M. G. Icosahedral virus particles as addressable nanoscale building blocks. Angew. Chem. Int. Ed. 41, 459–462 (2002). 68. McMillan, R. A. et al. Ordered nanoparticle arrays formed on engineered chaperonin protein templates. Nature Mater. 1, 247–252 (2002). 69. Patolsky, F., Weizmann, Y. & Willner, I. Actin-based metallic nanowires as bio-nanotransporters. Nature Mater. 3, 692–695 (2004). 70. Grybowski, B. A., Wilmer, C. E., Kim, J., Browne, K. P. & Bishop, K. J. M. Self-assembly: from crystals to cells. Soft Matter 5, 1110–1128 (2009). 71. Sun, J. et al. Core-controlled polymorphism in virus-like particles. Proc. Natl Acad. Sci. USA 104, 1354–1359 (2007). 72. Kalsin, A. M. et al. Electrostatic self-assembly of binary nanoparticle crystals with a diamond lattice. Science 312, 420–424 (2006). 73. Nykypanchuk, D., Maye, M. M., van der Lelie, D. & Gang, O. DNA-guided crystallization of colloidal nanoparticles. Nature 451, 549–552 (2008). 74. Park, S. Y. et al. DNA-programmable nanoparticle crystallization. Nature 451, 553–556 (2008). 75. Tlusty, T. & Safran, S. A. Defect-induced phase separation in dipolar fluids. Science 290, 1328–1331 (2000). 76. Tang, Z. Y., Kotov, N. A. & Giersig, M. Spontaneous organization of single CdTe nanoparticles into luminescent nanowires. Science 297, 237–240 (2002). 77. Lin, S., Li, M., Dujardin, E., Girard, C. & Mann, S. One-dimensional plasmon coupling by facile self-assembly of gold nanoparticles into branched chain networks. Adv. Mater. 17, 2553–2559 (2005). 78. DeVries, G. A. et al. Divalent metal nanoparticles. Science 315, 358–361 (2007). 79. Adams, M., Dogic, Z., Keller, S. L. & Fraden, S. Entropically driven microphase transitions in mixtures of colloidal rods and spheres. Nature 393, 349–352 (1998). 80. Nikoobakht, B., Wang, Z. L. & El-Sayed, M. A. Self-assembly of gold nanorods. J. Phys. Chem. B 104, 8635–8640 (2000). 81. Puntes, V. F., Krishnan, K. M. & Alivisatos, A. P. Colloidal nanocrystal shape and size control: the case of cobalt. Science 291, 2115–2117 (2001). 82. Li, M., Schnablegger, H. & Mann, S. Coupled synthesis and self-assembly of nanoparticles to give structures with controlled organization. Nature 402, 393–395 (1999). 83. Nie, Z. et al. Self-assembly of metal–polymer analogues of amphiphilic triblock copolymers. Nature Mater. 6, 609–614 (2007). 84. Stankovich, S. et al. Stable aqueous dispersions of graphitic nanoplatelets via the reduction of exfoliated graphite oxide in the presence of poly(sodium 4-styrenesulfonate). J. Mater. Chem. 16, 155–158 (2006). 85. Patil, A. J., Vickery, J. L., Scott, T. B. & Mann, S. Aqueous stabilization and self-assembly of graphene sheets into layered bio-nanocomposites using DNA. Adv. Mater. 21, 3159–3164 (2009). 86. Penn, R. L. & Banfield, J. F. Morphology development and crystal growth in nanocrystalline aggregates under hydrothermal conditions: insights from titania. Geochim. Cosmochim. Acta 63, 1549–1557 (1999). 87. Coelfen, H. & Antonietti, M. Mesocrystals: inorganic superstructures made by highly parallel crystallization and controlled alignment. Angew. Chem. Int. Ed. 44, 5576–5591 (2005). 88. Coelfen, H. & Mann, S. Higher-order organization by mesoscale self- assembly and transformation of hybrid nanostructures. Angew. Chem. Int. Ed. 42, 2350–2365 (2003). 89. Mann, S. The chemistry of form. Angew. Chem. Int. Ed. 39, 3392–3406 (2000). 90. Simon, P. et al. On the real-structure of biomimetically grown hexagonal prismatic seeds of fluorapatite-gelatine-composites: TEM investigations along [001]. J. Mater. Chem. 14, 2218–2224 (2004). 91. Yu, S.-H., Coelfen, H., Tauer, K. & Antonietti, M. Tectonic arrangement of BaCO3 nanocrystals into helices induced by a racemic block copolymer. Nature Mater. 4, 51–55 (2005). 92. Wang, T. X., Coelfen, H. & Antonietti, M. Nonclassical crystallization: mesocrystals and morphology change of CaCO3 crystals in the presence of a polyelectrolyte additive. J. Am. Chem. Soc. 127, 3246–3247 (2005). 93. Busch, S. et al. Biomimetic morphogenesis of fluorapatite-gelatin composites: fractal growth, the question of intrinsic electric fields, core/shell assemblies, hollow spheres and reorganization of denatured collagen. Eur. J. Inorg. Chem. 1643–1653 (1999). 94. Ball, P. The Self‑Made Tapestry: Pattern Formation in Nature (Oxford Univ. Press, 1999). 95. Li, M. & Mann, S. Emergent hybrid nanostructures based on non-equilibrium block copolymer self-assembly. Angew. Chem. Int. Ed. 47, 9476–9479 (2008). 96. Backov, R. Combining soft matter and soft chemistry: integrative chemistry towards designing novel and complex multiscale architectures. Soft Matter 2, 452–464 (2006). 97. Chandrappa, G. T., Steunou, N. & Livage, J. Macroporous crystalline vanadium oxide foam. Nature 416, 702 (2002). 98. Walsh, D. et al. Preparation of higher-order zeolite materials using dextran templating. Angew. Chem. Int. Ed. 43, 6691–6695 (2004). nmat_2496_OCT09.indd 791 14/9/09 09:52:19 © 2009 Macmillan Publishers Limited. All rights reserved 792 nature materials | VOL 8 | OCTOBER 2009 | www.nature.com/naturematerials review article NatUre materials doi: 10.1038/nmat2496 99. Grzybowski, B. A., Bishop, K. J. M., Campbell, C. J., Fialkowski, M. & Smoukov, S. K. Micro- and nanotechnology via reaction-diffusion. Soft Matter 1, 114–128 (2005). 100. Nicolis, G. & Prigogine, I. Self‑Organization in Nonequilibrium Systems ‑ From Dissipative Structures to Order Through Fluctuations (Wiley, 1977). 101. Haase, C. S., Chadam, J., Feinn, D. & Ortoleva, P. Oscillatory zoning in plagioclase feldspar. Science 209, 272–274 (1980). 102. Short, M. B. et al. Stalactite growth as a free-boundary problem: a geometric law and its platonic ideal. Phys. Rev. Lett. 94, 18501 (2005). 103. Tabor, Z., Rokita, E. & Cichocki, T. Origin of the pattern of trabecular bone: an experiment and a model. Phys. Rev. E 66, 51906 (2002). 104. Liesegang, R. E. Uber einige Eigenschaften von Gallerten. Naturwiss. Wochenschr. 11, 353–362 (1896). 105. Devon, R., RoseFigura, J., Douthat, D., Kudenov, J. & Maselko, J. Complex morphology in a simple chemical system. Chem. Commun. 1678–1680 (2005). 106. Collins, A. M., Carriazo, D., Davis, S. A & Mann, S. Spontaneous template-free assembly of ordered macroporous titania. Chem Commun. 568–569 (2004). 107. Leonard, A. & Su, B. L. A novel and template-free method for the spontaneous formation of aluminosilicate macro-channels with mesoporous walls. Chem. Commun. 1674–1675 (2004). 108. Deng, W. H. & Shanks, B. H. Synthesis of hierarchically structured aluminas under controlled hydrodynamic conditions. Chem. Mater. 17, 3092–3100 (2005). 109. Henisch, H. K. Crystals in Gels and Liesegang Rings (Cambridge Univ. Press, 1988). 110. Mueller, K. F. Periodic interfacial precipitation in polymer films. Science 225, 1021–1027 (1984). 111. Bitner, A., Fialkowski, M., Smoukov, S. K., Campbell, C. J. & Grzybowski, B. A. Amplification of changes of a thin film’s macromolecular structure into macroscopic reaction−diffusion patterns. J. Am. Chem. Soc. 127, 6936–6937 (2005). 112. Sugawara, A., Ishii, T. & Kato, T. Self-organized calcium carbonate with regular surface-relief structures. Angew. Chem. Int. Ed. 42, 5299–5303 (2003). 113. Imai, H., Tatar, S., Furuichi, K. & Oaki, Y. Formation of calcium phosphate having a hierarchically laminated architecture through periodic precipitation in organic gel. Chem. Commun. 1952–1953 (2003). 114. Voinescu, A. E. et al. Inorganic self-organized silica aragonite biomorphic composites. Cryst. Growth Des. 8, 1515–1521 (2008). 115. Yu, J., Guo, H., Davis, S. A. & Mann, S. Fabrication of monodisperse calcium carbonate hollow microspheres by chemically induced self-transformation. Adv. Funct. Mater. 16, 2035–2041 (2006). 116. Zeng, H. C. Synthetic architecture of interior space for inorganic nanostructures. J. Mater. Chem. 16, 649–662 (2006). 117. Oaki, Y. & Imai, H. Hierarchically organized superstructure emerging from the exquisite association of inorganic crystals, organic polymers, and dyes: a model approach towards suprabiomineral materials. Adv. Funct. Mater. 15, 1407–1414 (2005). 118. Li, M., Coelfen, H. & Mann, S. Morphological control of BaSO4 microstructures by double hydrophilic block copolymer mixtures. J. Mater. Chem. 14, 2269–2276 (2004). 119. Viravaidya, C., Li, M. & Mann, S. Microemulsion-based synthesis of stacked calcium carbonate (calcite) superstructures. Chem Commun. 2182–2183 (2004). 120. Xing, Y., Li, M., Davis, S. A. & Mann, S. Synthesis and characterization of cerium phosphate nanowires in microemulsion reaction media. J. Phys. Chem. 110, 1111–1113 (2006). 121. Aisenberg, J., Miller, D. A., Grazul, J. L. & Hamann, D. R. Direct fabrication of large micropatterned single crystals. Science 299, 1205–1208 (2003). 122. Nakanishi, T. et al. Flower-shaped supramolecular assemblies: hierarchical organization of a fullerene bearing long aliphatic chains. Small 3, 2019–2023 (2007). 123. Garcia-Ruiz, J. M., Melero-Gracia, E. & Hyde, S. T. Morphogenesis of self- assembled nanocrystalline materials of barium carbonate and silica. Science 323, 362–365 (2009). 124. Escudero, C., Crusats, J., Diez-Perez, I., El-Hachemi, Z. & Ribó, J. Folding and hydrodynamic forces in J-aggregates of 5-phenyl-10,15,20-tris (4-sulphophenyl)porphyrin. Angew. Chem. Int. Ed. 45, 8032–8035 (2006). 125. Hopwood, J. D. & Mann, S. Synthesis of barium sulphate nanoparticles and nanofilaments in reverse micelles and microemulsions. Chem. Mater. 9, 1819–1828 (1997). 126. Klajn, R., Bishop, K. J. M. & Grzybowski, B. A. Light-controlled self- assembly of reversible and irreversible nanoparticle suprastructures. Proc. Natl Acad. Sci. USA 104, 10305–10309 (2007). 127. Bruinsma, R. F., Gelbart, W. M., Reguera, D., Rudnick, J. & Zandi, R. Viral self-assembly as a thermodynamic process. Phys. Rev. Lett. 90, 248101 (2003). 128. Israelachvili, J. Intermolecular & Surface Forces (Academic Press, 1991). 129. Mann, S. Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry (Oxford Univ. Press, 2001). 130. Lee, S. Y., Royston, E., Culver, J. & Harris, M. Improved metal cluster deposition on a genetically engineered tobacco mosaic virus template. Nanotechnology 16, S435–S441 (2005). 131. Douglas, T. et al. Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv. Mater. 14, 415–418 (2002). 132. Grzybowski, B. A. & Campbell, C. J. Complexity and dynamic self-assembly. Chem. Eng. Sci. 59, 1667–1676 (2004). 133. Cross, M. C. & Hohenberg, P. C. Pattern formation out of equilibrium. Rev. Mod. Phys. 65, 851–1112 (1993). 134. Kurin-Csorgei, K., Epstein, I. R. & Orban, M. Systematic design of chemical oscillators using complexation and precipitation equilibria. Nature 433, 139–142 (2005). nmat_2496_OCT09.indd 792 14/9/09 09:52:20 © 2009 Macmillan Publishers Limited. All rights reserved