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Aggregation-Based Crystal Growth and Microstructure Development in Natural Iron Oxyhydroxide Biomineralization Products

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Science  04 Aug 2000:
Vol. 289, Issue 5480, pp. 751-754
DOI: 10.1126/science.289.5480.751

Abstract

Crystals are generally considered to grow by attachment of ions to inorganic surfaces or organic templates. High-resolution transmission electron microscopy of biomineralization products of iron-oxidizing bacteria revealed an alternative coarsening mechanism in which adjacent 2- to 3-nanometer particles aggregate and rotate so their structures adopt parallel orientations in three dimensions. Crystal growth is accomplished by eliminating water molecules at interfaces and forming iron-oxygen bonds. Self-assembly occurs at multiple sites, leading to a coarser, polycrystalline material. Point defects (from surface-adsorbed impurities), dislocations, and slabs of structurally distinct material are created as a consequence of this growth mechanism and can dramatically impact subsequent reactivity.

In natural systems, growth of crystals has typically been thought to occur by atom-by-atom addition to an inorganic or organic template or by dissolution of unstable phases (small particles or metastable polymorphs) and reprecipitation of the more stable phase. However, a growing body of experimental work indicates that additional self-assembly–based coarsening mechanisms can operate in certain nanophase materials under some conditions (1–7). Here, we show that iron oxyhydroxide crystals can grow via an aggregation-based pathway under natural conditions and discuss the ways in which this mechanism can control the form and reactivity of nanophase materials in nature.

Microorganisms catalyze iron oxidation in acidic and near-neutral solutions, leading to accumulations of iron oxyhydroxides. This process may have been important in formation of Proterozoic banded iron formations (8). Nanophase iron oxyhydroxides can also form abiogenically (e.g., due to neutralization of acidic iron-rich solutions and as the result of chemical weathering of iron-rich minerals). Iron oxyhydroxides (and aluminum oxyhydroxides, which share similar crystal chemical characteristics) are common in surficial materials and may compose the bulk of their reactive surface area.

We examined samples from the flooded, carbonate-hosted Piquette Pb-Zn mine beneath Tennyson, Wisconsin (water pH, ∼8). Iron-oxidizing microorganisms congregate in redox transition zones within the water column in the tunnels. In the ∼30 years since the mine flooded, tens of centimeter-thick orange stalactites and stalagmites and slime layers have accumulated (Fig. 1).

Figure 1

Photograph taken underwater in the Piquette mine showing accumulations of orange, polymer-laden ferric iron oxyhydroxides. Tens of centimeter-wide clumps of suspended material were displaced by passage of the leading diver. Image courtesy of T. O'Connor.

Samples of the water and slime were collected by a SCUBA diving team (9). Optical and transmission electron microscopic (TEM) examination of the slime (with a 200-kV TEM) revealed that it consists of colloidal aggregates of nanoparticles, mineralized cell products, and cells (Fig. 2). The twisted stalks are characteristic of iron-oxidizing bacteria belonging to theGallionella genus. Sheathed elongate cells are typical of bacteria belonging to the iron-oxidizing Lepthothrix genus (10).

Figure 2

TEM image of Gallionella stalks (G) and aLeptothrix sheath (L). Contrast associated with the stalks and sheath is due to nanoparticulate iron oxyhydroxides. Colloidal aggregates of nanoparticles (c) are also present.

Colloids and coatings on organic cell, stalk, and sheath materials consist of ∼2- to 3-nm diameter Fe-rich particles (Fig. 3). Selected area electron diffraction (SAED) patterns typically showed rings with diffuse intensity at ∼0.25 and 0.15 nm, indicating the sample consists mostly of randomly oriented two-line ferrihydrite (11–14) (Fig. 3). In regions ranging from a few nanometers to hundreds of nanometers, however, the primary nanoparticles were not randomly oriented, but were ordered into clusters and chains (Fig. 4). This was most pronounced at the peripheries of mineralized organic material (stalks and sheaths) and in colloidal aggregates. Low contrast between crystalline (lattice-fringe–bearing) regions in higher resolution images indicated that space separated adjacent particles (Fig. 5). However, the parallelism of lattice fringes demonstrates that the crystallographic axes of all particles in this area are parallel. We interpret these regions as consisting of aggregates of particles that share the same three-dimensional (3D) orientation (a defective single crystal).

Figure 3

HRTEM images of ∼ 2 to 3 nm diameter iron oxyhydroxide particles. Insets are Fourier transforms (FT) of image regions showing diagnostic interplanar spacings (in nanometers), and selected area electron diffraction pattern (left) is typical of two-line ferrihydrite.

Figure 4

TEM image of an area within a colloidal aggregate of ferrihydrite nanocrystals. Chains and aggregates indicate self-assembly of particles.

Figure 5

HRTEM image of an aggregate of ferrihydrite nanocrystals. Low contrast between crystalline regions (lattice fringes) indicates that space separates most particles. Lattice fringe orientations and FT (inset) demonstrate that particles have been assembled so they share a single crystallographic orientation (see Web fig. 1, A through F, for more examples) (24).

We suggest that these crystals formed as follows. It is well established that bacteria such as the Gallionella spp. and the Leptothrix spp. enzymatically oxidize dissolved ferrous iron. Due to the low solubility of ferric iron compounds at near-neutral pH, immediate solution supersaturation with respect to ferrihydrite solubility occurred. Most of the ∼2- to 3-nm diameter particles formed in solution and either attached to surrounding negatively charged polymers (e.g., Gallionella stalks) or flocculated to form colloidal aggregates. The double layers separating surfaces of adjacent particles may have been eliminated after repulsive interactions were overcome as the result of random, Brownian motion–driven particle collisions. These collisions may have been especially effective because the double layer of each particle contained very little net charge because the pH was close to the average isoelectric point of iron oxyhydroxide crystal surfaces. Jiggling of nanoparticles by Brownian motion may also allow adjacent particles to rotate to find the low-energy configuration represented by a coherent particle-particle interface. Rotation of particles within aggregates may also be driven by short-range interactions between adjacent surfaces (15). In aggregation-based growth, reduction in surface free energy is achieved by complete removal of pairs of surfaces.

TEM data showed oriented aggregates within spatially confined regions separated from other adjacent regions of oriented particles by areas that were dominated by particles in random orientations. This suggests that oriented aggregation was initiated at multiple sites within colloids. The orientation adopted within one region was unrelated to that in an adjacent region. Therefore, we predict that coarsening will lead to a polycrystalline material composed of larger particles. Oriented aggregation was most commonly detected in colloids and in particle aggregates at the peripheries of bacterial stalks and sheaths. We attribute the less extensive coarsening of ferrihydrite bound to stalks and cell sheaths to the inhibition of crystal rotation by interactions between the particles and the polymer substrate. It is possible that the distinctive stalk or cell morphologies (potential biosignatures) will be preserved by textural differences, including smaller particle size compared to surrounding materials.

Crystal growth by oriented attachment has important implications for subsequent materials reactivity. Phase stability can be particle size–dependent, so crystal growth can promote phase transformation (16–19). Phase transformation is also induced if initial precipitates are metastable. In our samples, laths of goethite (FeOOH) (Fig. 6A) are intergrown within regions of coarsened ferrihydrite. Observed crystal orientations (Fig. 6B) ensure the maximum continuity between the closest packed oxygen planes of goethite and ferrihydrite, which is presumed to be the goethite precursor. Goethite can form from ferrihydrite largely by relocation of a subset of iron atoms into adjacent face-sharing octahedral sites and small displacements of every fourth oxygen plane.

Figure 6

(A) HRTEM image of goethite containing three edge dislocations interpreted to have formed due to imperfectly oriented aggregation (see Web fig. 2, A and B, for more examples) (24). (B) HRTEM image showing the ferrihydrite-goethite interface, reactant, and product orientations. These are consistent with growth of goethite directly from ferrihydrite (see Web fig. 3) (24).

Surfaces of nanocrystalline iron oxyhydroxides in the environment are active adsorption sites (e.g., for arsenate or phosphate in acidic solutions and metals in alkaline solutions). If aggregation-based growth occurs, adsorbed ions at particle surfaces may be incorporated as point defects. This could decrease the bioavailability of these ions and could modify the thermodynamic properties and kinetic behavior of the material.

Previous experimental studies have shown that line defects (3) are introduced when growth occurs by oriented aggregation. Dislocations form at interfaces when surfaces of adjacent oriented particles are not atomically flat. Such dislocations are common at low-angle grain boundaries in arrays of ferrihydrite particles and are present in goethite (Fig. 6A). These defects can fundamentally impact subsequent coarsening (e.g., by spiral growth) and deformation.

Oriented attachment requires coherence in the two-dimensional (2D) plane of the interface. This can be achieved in a way that ensures perfect structural continuity across the interface, or new 3D structural units can be created (4, 5). These units may be characteristic of a more stable phase and provide nuclei for the phase transformation. Thus, planar defects introduced during growth by oriented attachment can increase rates of subsequent reactions by lowering the activation barrier. In the case of ferrrihydrite, incomplete double chains of Fe octahedra, similar to the double chains found parallel to [001] goethite, can be created at coherent interfaces (20). Schwertmann et al.(21) showed that recrystallization and transformation were enhanced by particle aggregation. Our results provide an atomistic explanation for these phenomena.

Aggregation may occur at finer scales than reported here. Assembly of multinuclear clusters (22) may be a very early crystallization step. Periodic, few-octahedra–wide vacancies characteristic of (six-line) ferrihydrite (14) are explained if ferrihydrite is constructed from subnanometer-scale clusters, which are also formed by aggregation of aqueous ions (23). Thus, crystals may grow by assembly of increasingly large units in a process analogous to the formation of hundred-nanometer–wide particles from few-nanometer-diameter particles (as in Fig. 5). This pathway may dominate over dissolution-recrystallization if the phase is relatively insoluble.

  • * To whom correspondence should be addressed. E-mail: jill{at}geology.wisc.edu

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