Derk Joester

Crystallization by particle attachment in synthetic, biogenic, and geologic environments

Growing crystals by attaching particles Crystals grow in a number a ways, including pathways involving the assembly of other particles and multi-ion complexes. De Yoreo et al. review the mounting evidence for these nonclassical pathways from new observational and computational techniques, and the thermodynamic basis for these growth mechanisms. Developing predictive models for these crystal growth and nucleation pathways will improve materials synthesis strategies. These approaches will also improve fundamental understanding of natural processes such as biomineralization and trace element cycling in aquatic ecosystems. Science, this issue 10.1126/science.aaa6760 Materials nucleate and grow by the assembly of small particles and multi-ion complexes. BACKGROUND Numerous lines of evidence challenge the traditional interpretations of how crystals nucleate and grow in synthetic and natural systems. In contrast to the monomer-by-monomer addition described in classical models, crystallization by addition of particles, ranging from multi-ion complexes to fully formed nanocrystals, is now recognized as a common phenomenon. This diverse set of pathways results from the complexity of both the free-energy landscapes and the reaction dynamics that govern particle formation and interaction. Whereas experimental observations clearly demonstrate crystallization by particle attachment (CPA), many fundamental aspects remain unknown—particularly the interplay of solution structure, interfacial forces, and particle motion. Thus, a predictive description that connects molecular details to ensemble behavior is lacking. As that description develops, long-standing interpretations of crystal formation patterns in synthetic systems and natural environments must be revisited. Here, we describe the current understanding of CPA, examine some of the nonclassical thermodynamic and dynamic mechanisms known to give rise to experimentally observed pathways, and highlight the challenges to our understanding of these mechanisms. We also explore the factors determining when particle-attachment pathways dominate growth and discuss their implications for interpreting natural crystallization and controlling nanomaterials synthesis. ADVANCES CPA has been observed or inferred in a wide range of synthetic systems—including oxide, metallic, and semiconductor nanoparticles; and zeolites, organic systems, macromolecules, and common biomineral phases formed biomimetically. CPA in natural environments also occurs in geologic and biological minerals. The species identified as being responsible for growth vary widely and include multi-ion complexes, oligomeric clusters, crystalline or amorphous nanoparticles, and monomer-rich liquid droplets. Particle-based pathways exceed the scope of classical theories, which assume that a new phase appears via monomer-by-monomer addition to an isolated cluster. Theoretical studies have attempted to identify the forces that drive CPA, as well as the thermodynamic basis for appearance of the constituent particles. However, neither a qualitative consensus nor a comprehensive theory has emerged. Nonetheless, concepts from phase transition theory and colloidal physics provide many of the basic features needed for a qualitative framework. There is a free-energy landscape across which assembly takes place and that determines the thermodynamic preference for particle structure, shape, and size distribution. Dynamic processes, including particle diffusion and relaxation, determine whether the growth process follows this preference or another, kinetically controlled pathway. OUTLOOK Although observations of CPA in synthetic systems are reported for diverse mineral compositions, efforts to establish the scope of CPA in natural environments have only recently begun. Particle-based mineral formation may have particular importance for biogeochemical cycling of nutrients and metals in aquatic systems, as well as for environmental remediation. CPA is poised to provide a better understanding of biomineral formation with a physical basis for the origins of some compositions, isotopic signatures, and morphologies. It may also explain enigmatic textures and patterns found in carbonate mineral deposits that record Earth’s transition from an inorganic to a biological world. A predictive understanding of CPA, which is believed to dominate solution-based growth of important semiconductor, oxide, and metallic nanomaterials, promises advances in nanomaterials design and synthesis for diverse applications. With a mechanism-based understanding, CPA processes can be exploited to produce hierarchical structures that retain the size-dependent attributes of their nanoscale building blocks and create materials with enhanced or novel physical and chemical properties. Major gaps in our understanding of CPA. Particle attachment is influenced by the structure of solvent and ions at solid-solution interfaces and in confined regions of solution between solid surfaces. The details of solution and solid structure create the forces that drive particle motion. However, as the particles move, the local structure and corresponding forces change, taking the particles from a regime of long-range to short-range interactions and eventually leading to particle-attachment events. Field and laboratory observations show that crystals commonly form by the addition and attachment of particles that range from multi-ion complexes to fully formed nanoparticles. The particles involved in these nonclassical pathways to crystallization are diverse, in contrast to classical models that consider only the addition of monomeric chemical species. We review progress toward understanding crystal growth by particle-attachment processes and show that multiple pathways result from the interplay of free-energy landscapes and reaction dynamics. Much remains unknown about the fundamental aspects, particularly the relationships between solution structure, interfacial forces, and particle motion. Developing a predictive description that connects molecular details to ensemble behavior will require revisiting long-standing interpretations of crystal formation in synthetic systems, biominerals, and patterns of mineralization in natural environments.

Nanoscale chemical tomography of buried organic–inorganic interfaces in the chiton tooth

Biological organisms possess an unparalleled ability to control the structure and properties of mineralized tissues. They are able, for example, to guide the formation of smoothly curving single crystals or tough, lightweight, self-repairing skeletal elements. In many biominerals, an organic matrix interacts with the mineral as it forms, controls its morphology and polymorph, and is occluded during mineralization. The remarkable functional properties of the resulting composites—such as outstanding fracture toughness and wear resistance—can be attributed to buried organic–inorganic interfaces at multiple hierarchical levels. Analysing and controlling such interfaces at the nanometre length scale is critical also in emerging organic electronic and photovoltaic hybrid materials. However, elucidating the structural and chemical complexity of buried organic–inorganic interfaces presents a challenge to state-of-the-art imaging techniques. Here we show that pulsed-laser atom-probe tomography reveals three-dimensional chemical maps of organic fibres with a diameter of 5–10 nm in the surrounding nano-crystalline magnetite (Fe3O4) mineral in the tooth of a marine mollusc, the chiton Chaetopleura apiculata. Remarkably, most fibres co-localize with either sodium or magnesium. Furthermore, clustering of these cations in the fibre indicates a structural level of hierarchy previously undetected. Our results demonstrate that in the chiton tooth, individual organic fibres have different chemical compositions, and therefore probably different functional roles in controlling fibre formation and matrix–mineral interactions. Atom-probe tomography is able to detect this chemical/structural heterogeneity by virtue of its high three-dimensional spatial resolution and sensitivity across the periodic table. We anticipate that the quantitative analysis and visualization of nanometre-scale interfaces by laser-pulsed atom-probe tomography will contribute greatly to our understanding not only of biominerals (such as bone, dentine and enamel), but also of synthetic organic–inorganic composites.

Spatial and Temporal Sequence of Events in Cell Adhesion: From Molecular Recognition to Focal Adhesion Assembly

A new concept that attributes a pivotal role to the pericellular coat in the regulation of the early stages of cell adhesion is presented. Quick, adaptable, and transient adhesion through multiple cooperative weak interactions provides the cell with an additional level of modulation in the decision‐making process that precedes the commitment to adhesion at a particular site. Hyaluronan emerges as a modulator of cell adhesion in certain cells, mediating binding or repulsion through its polyelectrolyte character, in addition to its chirality and molecular‐recognition properties. The biophysical properties of hyaluronan as well as its ultrastructural organization are analyzed in relation to this proposed function.

Amorphous intergranular phases control the properties of rodent tooth enamel

Key trace minerals greatly strengthen teeth The outer layers of teeth are made up of nanowires of enamel that are prone to decay. Gordon et al. analyzed the composition of tooth enamel from a variety of rodents at the nanometer scale (see the Perspective by Politi). In regular and pigmented enamel, which contain different trace elements at varying boundary regions, two intergranular phases—magnesium amorphous calcium phosphate or a mixed-phase iron oxide—control the rates of enamel demineralization. This suggests that there may be alternative options to fluoridation for strengthening teeth against decay. Science, this issue p. 746; see also p. 712 Differences in strength and stability of various tooth enamels may be due to trace minerals at boundary regions. [Also see Perspective by Politi] Dental enamel, a hierarchical material composed primarily of hydroxylapatite nanowires, is susceptible to degradation by plaque biofilm–derived acids. The solubility of enamel strongly depends on the presence of Mg2+, F−, and CO32–. However, determining the distribution of these minor ions is challenging. We show—using atom probe tomography, x-ray absorption spectroscopy, and correlative techniques—that in unpigmented rodent enamel, Mg2+ is predominantly present at grain boundaries as an intergranular phase of Mg-substituted amorphous calcium phosphate (Mg-ACP). In the pigmented enamel, a mixture of ferrihydrite and amorphous iron-calcium phosphate replaces the more soluble Mg-ACP, rendering it both harder and more resistant to acid attack. These results demonstrate the presence of enduring amorphous phases with a dramatic influence on the physical and chemical properties of the mature mineralized tissue.

In vitro synthesis and stabilization of amorphous calcium carbonate (ACC) nanoparticles within liposomes

We show that amorphous calcium carbonate (ACC) can be synthesized in phospholipid bilayer vesicles (liposomes). Liposome-encapsulated ACC nanoparticles are stable against aggregation, do not crystallize for at least 20 h, and are ideally suited to investigate the influence of lipid chemistry, particle size, and soluble additives on ACC in situ.

Atom Probe Tomography of Apatites and Bone-Type Mineralized Tissues

Nanocrystalline biological apatites constitute the mineral phase of vertebrate bone and teeth. Beyond their central importance to the mechanical function of our skeleton, their extraordinarily large surface acts as the most important ion exchanger for essential and toxic ions in our body. However, the nanoscale structural and chemical complexity of apatite-based mineralized tissues is a formidable challenge to quantitative imaging. For example, even energy-filtered electron microscopy is not suitable for detection of small quantities of low atomic number elements typical for biological materials. Herein we show that laser-pulsed atom probe tomography, a technique that combines subnanometer spatial resolution with unbiased chemical sensitivity, is uniquely suited to the task. Common apatite end members share a number of features, but can clearly be distinguished by their spectrometric fingerprint. This fingerprint and the formation of molecular ions during field evaporation can be explained based on the chemistry of the apatite channel ion. Using end members for reference, we are able to interpret the spectra of bone and dentin samples, and generate the first three-dimensional reconstruction of 1.2 × 10(7) atoms in a dentin sample. The fibrous nature of the collagenous organic matrix in dentin is clearly recognizable in the reconstruction. Surprisingly, some fibers show selectivity in binding for sodium ions over magnesium ions, implying that an additional, chemical level of hierarchy is necessary to describe dentin structure. Furthermore, segregation of inorganic ions or small organic molecules to homophase interfaces (grain boundaries) is not apparent. This has implications for the platelet model for apatite biominerals.

Selective Sequestration of Strontium in Desmid Green Algae by Biogenic Co-precipitation with Barite

The generation of radioactive waste and/or environmental radioactive contamination is a common side effect of activities such as nuclear power generation, medical use of radioisotopes, nuclear weapons testing, and occasionally disasters such as Chernobyl. The subsequent decontamination of waste or the environment requires the nontrivial ability to selectively separate and remove harmful radioisotopes such as Sr, a product of nuclear fission with a half-life of approximately 30 years. In the case of Sr, the chemical similarity of Ca, Sr, and Ba presents a challenge for even the most advanced ion-exchange materials. While phytoremediation approaches utilizing the accumulation of environmental contaminants by green plants are becoming increasingly popular, the effectiveness of such approaches for Sr sequestration are drastically reduced in the presence of Ca, due to the indiscriminate transport of Ca, Sr, and Ba exhibited by most organisms. Surprisingly, there are a small number of organisms that selectively sequester Sr and/or Ba in biominerals. For example, the marine radiolarian acantharea builds an endoskeleton from celestite (SrSO4), and the desmid [5] and stonewort green algae deposit barite (BaSO4) in vacuoles. Accumulation of Sr and Ba in the presence of up to five orders of magnitude excess Ca emphasizes that to address the selectivity problem, there is much to be learned and possibly gained from the strategies these organisms have evolved. Here, we quantitatively demonstrate the incorporation of up to 45 mol % Sr in barite crystals deposited by desmid green algae. The unicellular desmid green algae are ubiquitous in fresh water habitats and robust in culture, and as such are particularly suitable as a model system for Sr/Ba biomineralization and as a potential candidate for phytoremediation. In the desmid Closterium moniliferum, BaSO4 crystals are found in small terminal vacuoles at the tips of the crescent-shaped cells (Figure 1). Scanning electron microscopy and energy dispersive spectroscopy (SEM/EDS) analysis of BaSO4 crystals in ashed cells reveals clusters of mixed rhombic and hexagonal crystals of 0.5–1 mm diameter with 0.1–0.5 mm thickness (Figure 1), which exhibit strong Ba and S signals and little Ca (Supporting Information), consistent with previous descriptions.

Controlling nucleation in giant liposomes

We introduce giant liposomes to investigate phase transformations in picoliter volumes. Precipitation of calcium carbonate in the confinement of DPPC liposomes leads to dramatic stabilization of amorphous calcium carbonate (ACC). In contrast, amorphous strontium carbonate (ASC) is a transient species, and BaCO3 precipitation leads directly to the formation of crystalline witherite.

Precipitation of ACC in liposomes—a model for biomineralization in confined volumes

Biomineralizing organisms frequently precipitate minerals in small phospholipid bilayer-delineated compartments. We have established an in vitro model system to investigate the effect of confinement in attoliter to femtoliter volumes on the precipitation of calcium carbonate. In particular, we analyze the growth and stabilization of liposome-encapsulated amorphous calcium carbonate (ACC) nanoparticles using a combination of in situ techniques, cryo-transmission electron microscopy (Cryo-TEM), and small angle X-ray scattering (SAXS). Herein, we discuss ACC nanoparticle growth rate as a function of liposome size, carbon dioxide flux across the liposome membrane, pH, and osmotic pressure. Based on these experiments, we argue that the stabilization of ACC nanoparticles in liposomes is a consequence of a low nucleation rate (high activation barrier) of crystalline polymorphs of calcium carbonate.

Organic Materials and Organic/Inorganic Heterostructures in Atom Probe Tomography

Nano-scale organic/inorganic interfaces are key to a wide range of materials. In many biominerals, for instance bone or teeth, outstanding fracture toughness and wear resistance can be attributed to buried organic/ inorganic interfaces. Organic/inorganic interfaces at very small length scales are becoming increasingly important also in nano and electronic materials. For example, functionalized inorganic nanomaterials have great potential in biomedicine or sensing applications. Thin organic films are used to increase the conductivity of LiFePO4 electrodes in lithium ion batteries, and solid electrode interphases (SEI) form by uncontrolled electrolyte decomposition. Organics play a key role in dye-sensitized solar cells, organic photovoltaics, and nano-dielectrics for organic field-effect transistors. The interface between oxide semiconductors and polymer substrates is critical in emergent applications, for example, flexible displays.