Oriented Crystallization of Barium Sulfate Confined in Hierarchical

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Oriented crystallization of barium sulfate confined in hierarchical cellular structures Vivian Merk, John K. Berg, Christina Krywka, and Ingo Burgert Cryst. Growth Des., Just Accepted Manuscript • DOI: 10.1021/acs.cgd.6b01517 • Publication Date (Web): 22 Dec 2016 Downloaded from http://pubs.acs.org on January 14, 2017

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Crystal Growth & Design

Oriented crystallization of barium sulfate confined in hierarchical cellular structures Vivian Merk1,2*, John K. Berg1,2, Christina Krywka3, Ingo Burgert1,2*

1

ETH Zurich, Institute for Building Materials (IfB), Wood Materials Science, 8093 Zurich,

Switzerland 2

EMPA (Swiss Federal Laboratories for Material Science and Technology), Applied Wood

Materials Laboratory, Überlandstrasse 129, 8600 Dübendorf, Switzerland 3

Helmholtz Zentrum Geesthacht (HZG), Institute for Materials Research, Max-Planck-Straße 1,

21502 Geesthacht, Germany

KEYWORDS Barite, crystallographic orientation, wood, mineral, crystal growth Raman spectroscopy, Scanning Electron Microscopy, Wide-Angle X-ray Scattering

ABSTRACT Biomineralization involves the controlled formation of inorganic matter within hierarchical biological scaffolds. Mimicking the crystallization of biominerals in such

ACS Paragon Plus Environment

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confinement is an important goal in the field of crystal engineering. Natural porous materials offer an interesting platform for studying mineral morphogenesis and texturing through templatedirected mineralization. In this paper, we precipitate barium sulfate from aqueous salt solutions in the constrained micro- and nano-environment of pristine wood cells and cell walls. By employing spatially resolved characterization techniques, such as scanning electron microscopy (SEM), Raman spectroscopic imaging, and scanning wide-angle X-ray scattering (WAXS), we gain important insights into the deposition pattern, morphology, and crystallographic orientation of barite crystals in the plant cell anatomy. The experimental findings suggest directed crystallization of BaSO4 at different hierarchical levels. SEM shows elongated, dendritic BaSO4 crystals growing inside the cell lumina, closely associated with the interfacial cell wall region. WAXS measurements acquired from mineralized cell walls show a crystallographic coorientation of barite and cellulose, suggesting epitaxial crystal growth.

INTRODUCTION One of the most exciting topics discussed in the field of biomineralization is oriented crystal alignment 1. The outstanding macroscopic properties of various complex biological materials, such as bone 2 3, crustacean cuticles 4 5 6, or mollusk shells 7, are based upon a directed assembly of inorganic building blocks in an organic matrix. Hydroxyapatite platelets in bone are cooriented with the c-axis along the collagen fiber axis 2. The excellent mechanical properties of nacre evolve from a stacked packing of aragonite platelets orthogonally to the organic sheet plane 1. In crustacean cuticles, the crystallite orientation follows the helicoidal arrangement of the protein/chitin fiber matrix 5 6. In a similar way, mineral accumulations in higher plants (e.g.


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rice, sugarcane) fulfil specific biological functions, such as mechanical stabilization 8. Biomacromolecules (e.g. proteins) are often involved in controlling these biomineralization processes 7 9 10, but the role of carbohydrates in mediating crystallization of mineral phases has not been fully understood, yet 11 12 13 14. In nature, biogenic barite is sequestered in green algae for gravitactic orientation 15. BaSO4 scale presents a major industrial problem in off-shore oil-fields 16. A large body of literature describes the morphology and formation mechanisms of barite crystals in aqueous media 16 17 18 19

. Templated crystallization of BaSO4 has been studied extensively under the influence of

organic molecules in aqueous media, such as anionic surfactants 20 21, fatty acids 22, or charged polymers 23 24 25 26 27 28. Under functionalized surfactant monolayers, barite nucleates in a specific crystallographic orientation relative to the surrounding matrix 22. Here, favorable interactions rely upon stereochemical recognition of the binding motif including geometrical and electrostatic factors 22. Under the influence of additives, a variety of unusual barite crystal shapes has been produced. One rationale is the site-specific binding of organic moieties to polar faces that stabilizes the resulting crystal nucleus through charge neutralization 22. A selective blocking of growth faces by adsorbed molecules eventually triggers changes in the crystal morphology 29. Recently, the oriented alignment and coalescence of BaSO4 primary nano-domains to higherorder assemblies has been suggested as alternative to classical crystallization pathways 25 26 27 28 30

. In the presence of copolymers, there has been strong evidence for an ion-rich liquid precursor

phase preceding filamentary BaSO4 crystals 21 30 23. For this reason, double hydrophilic blockcopolymers are highly effective in controlling the BaSO4 crystal morphology and modulating hierarchical mineral assemblies 23 24 25 26.


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While providing fundamental insights into the nature of inorganic/organic interactions and mineral formation mechanisms, such controllable model systems (e.g. BaSO4 nucleated on Langmuir monolayers 22), do hardly reach the complexity of biological scaffolds. A major difference of many molecular templates is their well-defined two-dimensional organization. The relatively low cellulose crystallinity and complex multi-component chemistry compared to pure cellulose 31 render plant cell walls a complex reaction environment for inducing oriented BaSO4 crystallization. For understanding mineral formation inside a wood cell wall, it is important to know how wood is organized at the level of cells and cell walls. As schematically shown in Fig. 1, wood consists of hollow, tubular cells, which predominantly run parallel to the tree axis. In the cell walls, cellulose microfibrils wind helicoidally around the cell axis at a specific microfibril angle with respect to the cell axis. Numerous synchrotron experiments on pristine wood tissues using small-angle and wide-angle X-ray scattering have been performed by other authors 32 33 34. Depending on the cell wall layer, microfibrils vary in their texture (random or parallel) and helical angle. According to current models based on X-ray and neutron scattering, each microfibril in spruce softwood is ~3 nm in diameter and consists of 18 or 24 slightly twisted and partially disordered cellulose chains 35. The crystalline portion of the microfibrils conforms best to the (triclinic) cellulose Iα and the (monoclinic) cellulose Iβ allomorphs, with the latter dominating in vascular plant tissues 35 36. Together with the interstitial hemicelluloses (glucomannan), the microfibrils 37 are bundled to cellulose fibril aggregates of 15-25 nm 38 39, whose exact structure is still under debate. The surrounding matrix space of the cell wall is filled with amorphous hemicelluloses and lignin, and perforated with nanoscopic pores 38 39.


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Figure 1. Scheme of cellular ultrastructure and tracheid cell wall model. The cell wall layers can be distinguished by the texture and orientation of the cellulose microfibrils. Wood fibers consist of an amorphous lignin/hemicellulose matrix and cellulose fibril aggregates, which bundle elementary cellulose fibrils and associated hemicelluloses. Each elementary cellulose fibril contains amorphous and crystalline regions.

In this work, we precipitate barium sulfate (BaSO4) in a natural wood scaffold by alternating infiltration with concentrated electrolyte solutions. Similar artificial mineralization strategies of wood have been proposed for various biominerals, such as silica 40, calcium carbonate 41 42, or iron oxide 43. The objective of the present study is to provide a comprehensive picture of the local concentration, morphology, and orientation of crystalline BaSO4 deposits in the supramolecular wood structure at various length scales, from the nanometer to the millimeter range. Hence, we apply a combination of complementary spatially resolved characterization methods. SEM is an ideal tool for investigating the BaSO4 crystal morphology and spatial organization in the micron-sized cavities (lumina). Due to sample preparation constraints and sample-limited electron transmitivity, high-resolution imaging (e.g. by transmission electron


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microscopy) of mineralized cell walls is challenging. On the contrary, confocal Raman microscopy is ideal for non-destructive chemical imaging of crystalline barite in a complex cell wall environment. Wide-angle X-ray scattering (WAXS) provides even more detailed structural information, namely crystal lattice parameters and preferred grain orientations of the mineral. By recording scanning diffraction data using a micro-focused synchrotron X-ray beam, we obtain the distribution of crystalline barite within the nano-porous cell walls as compared to the cell lumina. This analysis is essential in understanding whether the chemistry of the cell walls or the confined porous structure affect the mineralization process, which to date is largely unknown.

EXPERIMENTAL SECTION Mineralization: Aqueous solutions of 1 M BaCl2 and 1 M Na2SO4 have been prepared from BaCl2 · 2H2O (Sigma Aldrich, ACS Reagent ≥ 99 %) and Na2SO4 (Merck, EMSURE ACS, ISO, Reag. PhEur) salts without further purification using deionized water. Wood cubes (1 cm3) from Norway spruce (Picea abies) have been mineralized in two successive vacuum-assisted reaction cycles (p ≤ 100 mbar) at room temperature using BaCl2 for 12h (first step), Na2SO4 for 12h (second step), BaCl2 for 12h (third step) and Na2SO4 for 12h (fourth step). After each step, samples were rinsed in deionized water. Mineralized wood samples were washed with absolute ethanol for 3 h to remove unreacted salt precursors and side products. Scanning electron microscopy: Environmental scanning electron microscopy (ESEM) was carried out on a FEI Quanta 600 in the low-vacuum mode (water vapour, 0.53 Torr) driven by 20 kV acceleration voltage using a SSD (solid-state) backscattered electron detector.


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Raman microscopy: For the Raman measurements, 20 µm cross-sections were prepared with a rotary microtome (Leica Ultracut, Germany), placed on a microscopic slide with a few drops of D2O and sealed with a cover slip and nail polish to avoid evaporation. All Raman spectra were recorded with a confocal Raman-microscope (Renishaw InVia) equipped with a Nd-YAG laser (λ = 532 nm), a 1800 grooves/mm grating and a 100x oil immersion objective (Nikon, NA = 1.3), a step width of 300 nm and an integration time of 0.3 s. The data were processed with the software Wire 4.1 and single spectra were plotted with the program OriginPro 2016. Additionally, for the extraction of hyperspectral data, the spectral dataset was scanned for cosmic rays, and Vertex Component Analysis (VCA) was performed in the spectral range from 9001700 cm-1 with the MatLab-based software CytoSpec v. 2.00.01 assuming five endmembers. Scanning Wide-Angle X-Ray Scattering: For synchrotron experiments, 10 µm transverse sections and 10 µm radial sections were prepared using a rotary microtome (Leica Ultracut, Germany). Scanning WAXS measurements were carried out in the transmission geometry at the Nanofocus Endstation of the synchrotron beamline P03 (MINAXS) at PETRA III (DESY, Hamburg) 32 44. The X-ray beam (17 keV, 0.7293 Å) was collimated to a spot of 1x1 µm2 in diameter using a KB mirror system, as described elsewhere 32 33. The integrated flux in the micro-focused beam is 1010 ph s-1.The beam divergence corresponds to 2 mrad in the vertical and 1.3 mrad in the horizontal plane. Due to the relatively weak scattering intensity of wood cellulose, 2D diffraction patterns were recorded with a single-photon counting PILATUS 1M (981x1043 pixels, 172x172 µm²) detector. Samples were mounted on a sample holder fixed on a hexapod to ensure accurate alignment with an optical microscope installed at the experimental end-station. The sample-detector distance was set to 17.7 cm to give a maximum Q-space ≈


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37.6 nm-1. A scanning step size of 1 µm and an exposure time of 1 s helped avoiding X-ray radiation damage of the cellulose. Raw data analysis was automated using macros in the Fit2D software 45. A background reference frame was subtracted from all 2D patterns to account for atmosphere scattering. The sample-detector distance, beam center and detector tilt was calibrated against a LaB6 standard by the calibrant routine implemented in Fit2D. Full radial profiles give the scattering intensity depending on the length of the scattering vector, defined by Q = 4πλ-1sin(Θ), where 2Θ is the scattering angle. The XRD patterns were baseline-corrected and integrated using the OPUS 7.2 software (Bruker). Azimuthal integration over pronounced Bragg reflections of cellulose Iβ (200) (Q = 14.7-15.9 nm-1) 46 and barite (401) ≡ (113) and (122) ≡ (312) (Q = 29.3-30.2 nm-1) 47 reflects the distribution of these components. Single spectra and color-coded mappings were created with OriginPro 2016 (OriginLab Corporation). BaSO4 crystal grain texture was visualized by plotting the scattering intensity as function of the scattering vector (Q-space) and the azimuthal angle (χ = 0-360°). Unit cell projections of barite 48 and cellulose Iβ 36 were generated by the visualization software VESTA 49 from crystallographic database files downloaded from the supporting information of references 36 48. Fig. S1 (supporting information) displays ball-and-stick models of the cellulose Iβ 36 and barite 48 lattices projected along the [100], [010], and [001] directions. RESULTS AND DISCUSSION Barium sulfate was mineralized inside the hierarchical cell architecture of wood by sequential infiltration using BaCl2 and Na2SO4 solutions. High concentrations of precursor salts were used to ensure a detectable degree of mineralization of the wood cell walls, as concentrations that


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generate a low supersaturation would only result in the precipitation of a fraction of a percent by mass of mineral in the wood structure. SEM was used for morphological investigations of BaSO4 crystals in transverse and longitudinal block-faces (Fig. 2, Figure S2 (supporting information)). Mineralization produces elongated BaSO4 crystals of up to ~30 µm in length at the cell wall interface. Judging from the backscattered electron contrast, the inner part of the cell wall (S3 and partially S2 cell wall, see white arrow in Fig. 2) is also highly mineralized, likely due to ion diffusion from the lumen side. BaSO4 crystals seem to emanate from these interfacial regions and grow into the center of the void space, suggesting heterogeneous nucleation at the cell wall interface. Although we employed an extremely high level of initial supersaturation in the electrolyte solutions, the local ion concentration inside the wood anatomy is completely unknown. At high degrees of supersaturation, more than 1000 times over the saturation limit 50, crystallization is controlled by bulk ion-diffusion, whereas surface growth processes dominate under conditions close to equilibrium 19 51 52. In the SEM micrographs, we observe a broad variety of crystal habits, amongst them spicules and feathers. Dendritic crystal shapes often originate from diffusion-limited crystal growth 19 51 52. Similar dendritic morphologies have been reported by other authors for BaSO4 crystals precipitated from supersaturated solutions 16 19 18. Consequently, we presume the ion concentration in the lumina to be sufficiently high to enable dendrite formation, but not low enough to favor surface growth.


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Figure 2. Scanning electron micrographs of spruce cross-section (a) and radial section (b) collected in the backscattered electron mode. Scale-bars correspond to 20 µm. White arrows indicate high degree of mineralization in the inner parts of the cell wall.

As a result of vacuum-assisted solute transport by advection of the electrolyte followed by solute diffusion through the lumina of softwood tracheids, feather-like BaSO4 dendrites are predominantely developed (Fig. 2). The diffusion of solute ions from the bulk solution into the cell wall leads to crystal growth at the cellular interface. Even though equimolar precursor solutions have been employed, local ion ratios could vary considerably due to the higher diffusion coefficient of Ba2+ compared to SO42- ions 53 54. Furthermore, the wood samples were incubated with precursor salt solutions in sequential infiltration steps. The Ba2+/SO42- ratio has implications for the crystal size and morphology 55 56. A local excess of Ba2+ at a constant level of supersaturation, for instance, leads to faster nucleation and crystal growth than for SO42- 56. Here, an accumulation of Ba2+ in outer cell wall layers seems to enhance crystal growth into the bulk solution where the SO42- concentration is higher.


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As previously stated, the lighter grey values in the backscattered SEM images indicate the incorporation of electron-dense matter in the cell wall but it does not allow us to discern between BaSO4 and Ba2+ ions. Raman microscopy (Fig. 3) is suitable for detecting BaSO4 spectroscopically with sub-micron resolution. The vibrational spectrum of barite contains the ν2 = 458.4 cm-1 (E, doubly degenerate bend), ν3 = 1084.1-1168 cm-1 (F2, triply degenerate stretch) and ν4 = 618.2 cm-1; 647 cm-1 57 (F2, triply degenerate bend) bands (data not shown). The intense ν1 band at 988.7 cm-1 corresponds to the totally symmetric stretch of the sulfate ion (A1) in the barite lattice 57 and is suitable for tracking BaSO4 in the wood anatomy. Through the application of a multivariate analysis method (Vertex Component Analysis, VCA), a simultaneous monitoring of cell wall polymers and embedded BaSO4 mineral is possible, yielding a detailed picture of the presence and penetration depth in the cell walls. VCA has been used in previous papers for analyzing hyperspectral datasets of pristine 58 or chemically modified wood 41 to identify so-called endmember spectra with distinctly-different spectral features. The resulting endmember mappings of mineralized cells allow for imaging the chemical distribution of prominent cell wall components and the incorporated mineral. Figure 3a,d show the high abundance of lignin, an aromatic cell wall polymer, in the middle lamella and cell corners of tracheid cells. In the cell wall (Figure b,e), characteristic bands around 1550-1640 cm-1 and 1090-1105 cm-1 arise from lignin and cellulose, respectively 59. In addition, finely dispersed BaSO4 precipitates in the S2 cell wall, as evident from the simultaneous detection of the ν1 band of barite, polysaccharide and lignin bands (Fig. 3h). A striking feature of the endmember mappings (Fig. 3c,f) is the formation of a continuous layer of pure BaSO4 mineral at the lumen/cell wall interface of spruce tracheids, which is in accordance with the SEM results. We


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suppose that the extremely low solubility of BaSO4 (Ksp = 9.82 · 10-11 mol2L-2 60) likely accounts for the deposition of an interfacial mineral layer. Such a deposition pattern goes in line with ion diffusion from the lumen into the cell wall. Additional endmember spectra represent other components, e.g. the lumina (Supporting information, Fig. S3).

Figure 3. Vertex Component Analysis (VCA) of spruce mineralized with BaSO4. Hyperspectral Raman imaging showing endmember distribution and corresponding endmember spectra of lignin (a, d, g), cell wall with BaSO4 inclusions (b, e, h) and pure BaSO4 mineral at the cellular interface (c, f, i). Each scale-bar corresponds to 10 µm.


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Wide-angle X-ray scattering (Fig. 4-6) yields further information on the mineral distribution pattern in distinct anatomical regions of mineralized wood, complementary to Raman spectroscopic mapping. By scanning over a small sample volume with a finely collimated synchrotron X-ray beam, localized 2D diffraction patterns are produced. Debye-Scherrer rings related to reflecting lattice planes (hkl) reveal not only the character of the mineral phase, but also the crystallinity and preferential grain orientation, as reflected in peak broadening and angledependent intensity variations, correspondingly. The X-ray diffraction pattern of cellulose in wood is characterized by broad Bragg peaks, the (1-10) (110) doublet at Q ≈ 11 nm-1 and the (200) reflection at Q ≈ 16 nm-1 (Fig. 4d,5,6b). For the sake of simplicity, cellulose reflections are continuously indexed on the monoclinic Iβ lattice (space group P21, a = 7.784 Å, b = 8.201 Å, c = 10.380 Å, α = β = 90°, γ = 96.550° 36). Sharp scattering peaks at higher Q-space are consistent with standard d-spacings of orthorhombic barite (space group Pbnm, lattice constants a = 8.884 Å, b = 5.458 Å, c = 7.153 Å, α = β = γ = 90°) 47 48

. No additional reflections from any other possible component were observed in the 2D WAXS

patterns.


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Figure 4. Synchrotron X-ray scattering mappings of mineralized spruce cross-section (30 x 30 µm2). Scattering intensity mappings of (200) cellulose (orange, a) and (401) (122) barite (blue, b) and overlay (c). Radial 1D profiles (d) from exemplary positions marked by colored squares (c).

WAXS mappings were generated by integrating over full Debye-Scherrer rings of cellulose (200) and barite (401), (122) in the assigned integration limits. The (401), (122) peaks centered around Q ≈ 29.7 nm-1 exhibit high relative intensities and do not overlap with cellulose reflections.


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Azimuthally-averaged scattering intensity values of cellulose and barite were translated into false-color images in orange and blue, respectively, whereby each pixel represents a sampling area of 1 x 1 µm2. An overlay of the color-coded contour-plots displays the spatial distribution of BaSO4 in the cell wall tissue (Fig. 4c). Fig. 6d gives 1D X-ray diffraction profiles from arbitrary positions in the lumen or the cell wall comprising reflections of cellulose and barite, as marked by squares in Fig. 4c. According to WAXS mappings collected from spruce cross-sections (Fig. 4c), barite mineral is highly accumulated at the lumen/cell wall interface and adjacent cell wall regions at 4 µm distance from the lumen.

Figure 5. a) Radial profile of 2D WAXS pattern from the lumen (grey line) and the cell wall region (black line) of a spruce cross-section. b) X-ray powder diffraction pattern of barite


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according to the literature

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. Bragg peaks are scaled to relative intensities and indexed with

the reference to Miller indices of barite.

Fig. 5 shows 1D XRD profiles acquired from a BaSO4 mineral deposit in the lumen (grey line) and a mineralized cell wall (black line). The relative peak intensities of some barite reflections, e.g. (200), (011), (002), and (020), clearly deviate from tabulated X-ray powder diffraction data 47 48

. Variations in relative peak intensities have often been associated with unusual crystal

morphologies. On the other hand, each 2D XRD pattern gives an average over the sampling volume and the beam diameter can even exceed the crystallite size. The measured Bragg peaks appear at slightly shifted d-spacings (∆Q ~0.1 nm-1), which can indicate a certain lattice distortion. In the mineralization experiments, we operate at a high degree of supersaturation, but the local ion concentration in the nanoscopic pores of the cell wall is expected to be considerably lower than in the void lumina. Small pores between individual cellulose fibril aggregates ranging in a size of few nanometers 38 are amenable to act as highly confined reaction cavities. In fact, organic matrices mediate nucleation by lowering the interfacial energy 1. Recent experimental studies ascertained the existence of primary BaSO4 nanocrystals of 2-10 nm 30 rendering the formation of single-domain crystals in the confined cell walls possible. Possibly due to confinement in the nanoscopic cell wall pores, a substantial peak broadening of the Bragg reflections was detected, as exemplified by the full width at half maximum (FWHM) of the (211) Bragg reflection (see Fig. S4, supporting information).


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Moreover, localized X-ray diffraction for analyzing preferential crystal grain orientations (Fig. 6) were employed. Figure 6a-c depicts a WAXS mapping from a radial section of a spruce tracheid cell. Spotty diffraction patterns acquired from the lumina indicate a random orientation of BaSO4 crystals (see Figure 6e,f). In 2D diffraction patterns collected from a cell wall region (Fig. 6g,h), the orientation of the cellulose unit cell is evident from the (200) reflection, two diffuse spots at azimuthal angles φ = 90° and φ = 270°. Symmetrical arcs of meridional (004) cellulose reflections are located at φ = 0/360° and φ = 180°. The crystallographic c-axis of cellulose Iβ coincides with the long axis of the cellulose chains (note unit cell projections in Fig. S1) 36 34. Intensity variations in the Debye-Scherrer rings of barite also disclose texture information. Here, partial rings and arcs suggest a crystallographic co-orientation relationship between barite and cellulose with a mosaic spread of ~15°. The (020) Bragg peak of barite is coplanar with the plane of the (004) face of cellulose. The crystal facets of the (210) and (211) planes are oriented approximately at a 45° angle with respect to (002).


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Figure 6. a) Synchrotron X-ray scattering mapping of spruce radial section mineralized with BaSO4 (20 x 20 µm2). Scattering intensity mappings of (200) cellulose (orange, a) and (401) (122) barite (blue, b) and overlay (c). Radial Q-profiles (d) from exemplary positions marked by colored squares (c) with indexing of cellulose and barite diffraction rings. e) Spotty 2D WAXS pattern indicating random barite orientation. f) Scattering intensity plot of c) as function of azimuthal angle φ and Q-space. g) 2D WAXS pattern from cell wall region h) Scattering intensity plot of e) as function of azimuthal angle φ and Q-space.

The (102) reflection occurs at the angular positions φ = 20°, 155°, 195° and 335°. The faint Bragg reflections (103), (221), and (303) appear at φ = 30°, 150°, 210°, and 330°. Notably, strong texturing of barite occurs over the whole cell wall area, as reflected by summed-up 2D diffraction patterns from the cell wall and interfacial regions (see supporting information, Fig. S5). To summarize, it can be concluded that scanning WAXS data are in strong agreement with SEM and Raman microscopy results, as these complementary methods show the deposition of barite in the S2 cell wall and at the S3 cell wall/lumen interface.

The experimental findings presented above suggest oriented crystallization of BaSO4 in the wood cell wall, so that cellulose, as being the only crystalline polymer, or the spatial organization of the fibrillar units, template the directional BaSO4 crystallization. A possible explanation for BaSO4 texturing is that interfacial interactions between cellulose and barite crystal come into play. Interactions commensurate with geometric or stereochemical


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requirements of the respective crystal face 22 can lead to an orientation of crystal nuclei along a preferred crystallographic direction. Epitaxy in biomineralization is commonly related to a close crystal lattice match between the mineral and the underlying organic template 22. In case of barite and cellulose Iβ, the smallest lattice mismatch (~8 %) corresponds to a co-alignment of acellulose Iβ/cbarite and bcellulose Iβ/abarite. The FWHM of the cellulose (200) reflection conforms to the intersheet spacing of the Iβ lattice 35

(see Fig. S1, supporting information). Inside a cellulose microfibril, Ba2+ complexation

between glucan chains would be expected to undergo with a change in the crystal packing and a substantial peak broadening, which is contrary to our experimental findings. Due to limited accessibility to solutes, a crystallization of barite in bulk crystalline cellulose can be ruled out to the greatest extent. Based on current assumptions, water molecules are incapable of penetrating the core of a crystalline microfibril 61 62, while interdispersed, disordered regions are accessible to water 63. At the microfibril surface, though, the crystalline network is interrupted and β-Dglucopyranose units exhibit an angular distortion. As a consequence, surface cellulose chains form fewer intramolecular and more outward-directed hydrogen bonds 64. The large fraction of hydroxyl groups exposed at the microfibril surface 65 is available for molecular interactions with charged ions or crystal faces. It needs to be borne in mind that minerals precipitate in waterswollen cell walls wherein the spatial dimensions of the polymers, such as the equatorial spacing between cellulose molecules in the microfibrils 34, differ from the dry condition during ex situ WAXS measurements. In addition, intramolecular hydrogen bonding of water-accessible cellulose chains is disrupted in the wet state 62 66. Thus, the formation of barite seems to be more likely to take place at the microfibril surface, but it is yet unclear whether co-aligned barite crystals are located inside or outside a cellulose microfibril aggregate. In the latter case, only


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exterior microfibrils would be involved in such interactions. Glucomannan polysaccharides, in part furnished with acetyl groups, are closely associated with cellulose 38 67 63 and accessible to hydration, so they might also interact with as-formed barite crystals. Therefore, deriving an unequivocal mechanism for oriented barite crystallization is challenging, as the knowledge of the nano-porosity and the complex macromolecular organization inside the cell wall is yet limited. The previously published mineralization of wood by CaCO3 differs substantially from the present work in crystal morphology, crystal orientation or mineral distribution.42 Despite equally high precursor solutions, BaSO4 dendrites precipitated at the cellular interface, while complete lumen filling occurred in the mineralization with CaCO3. This might be due to the by a factor of 10 or 100 lower solubility of barite compared to calcite or vaterite, respectively. Furthermore, BaSO4 crystallizes in a single polymorph in contrast to CaCO3. Most importantly, BaSO4 shows a preferred crystallographic orientation with regard to the cellulose, which we have not observed in the CaCO3 mineral system. Based on striking structural analogies, we can draw parallels between BaSO4-mineralized wood and other hierarchical biomaterials. Crystallographic alignment is a wide-spread phenomenon in biomineralization 1. A common feature of many biological templates is the fact that acidic (glyco)proteins control inorganic morphogenesis, while carbohydrates (e.g. chitin) merely constitute a supportive framework 7 10. The experimental findings in this work suggest that carbohydrates in the mineralization of plant tissues do not only provide the macromolecular scaffold but can also direct the mineral deposition. The crystallization of barite occurs in the confinement of nano-pores in the presence of various cell wall polymers (cellulose, hemicellulose, lignin) and the mineralization of the native cell wall with BaSO4 seems to undergo with a crystallographic co-orientation of barite and cellulose. We propose that the


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structure-directing activity of the polysaccharides results from structural matching of inorganic and organic building blocks at the nano-scale, mimicking the biomineralization in various animal species. This supports the notion that the crystallization mechanisms valid in plant tissues are different from the ones in biotemplates of animal origin, since charged proteins or polysaccharides are less abundant.

CONCLUSIONS Our results show oriented growth of BaSO4 crystals confined in the complex and highlydirectional cell architecture of wood at various levels of hierarchy. In order to characterize the morphology and crystallinity of in situ formed barite, we combined spatially resolved characterization techniques, scanning electron microscopy, Raman mapping and scanning microfocused wide-angle X-ray scattering. Apparently, the driving force for mineral precipitation in the lumina is the high supersaturation of the electrolyte solutions, as indicated by dendritic crystals growing from mineralized cell walls towards the lumen center. As demonstrated by Raman microscopy and scanning wide-angle X-ray scattering, barite does not only form a layer at the lumen/cell wall interface, but it is also widely deposited inside the nanoporous cell wall. A texture analysis founded on diffraction of synchrotron X-ray radiation strongly indicates a crystallographic co-orientation of barite and cellulose crystals at the nanoscale, but the basic principle remains unclear. The implementation into a fibrous organic matrix seems to give rise to a structural and textural organization of barite reminiscent of other biomineralized tissues, such as bone, nacre, or crustacean cuticles. In contrast to these examples, the structure-directing mechanism invoked to explain barite crystallization in nano-porous cell


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walls is based exclusively on carbohydrates in confinement. We believe that our experimental findings enhance our general conception of biomineralization processes in the plant kingdom, in particular nucleation and growth of inorganic phases in natural, sub-microporous cell walls. A deeper understanding of the interaction between inorganic phases and organic macromolecules on the nanoscale is essential for templated crystal engineering and bio-inspired materials design.

ASSOCIATED CONTENT Supporting Information. Ball-and-stick models of crystal structures. Scanning electron micrographs. Raman endmember mappings. Wide-angle X-ray mappings. This material is available free of charge via the Internet at http://pubs.acs.org.”

AUTHOR INFORMATION Corresponding Author *Vivian Merk ([email protected]); Ingo Burgert ([email protected]) Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT


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The Bundesamt für Umwelt (BAFU) and Lignum, Switzerland are acknowledged for the financial support of the Wood Materials Science group. Thanks to Tobias Keplinger for writing a macro for baseline-correction in OPUS. REFERENCES (1) Mann, S., Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry. ed.; Oxford University Press: Oxford 2001; Vol. 5. (2) Fratzl, P.; Gupta, H. S.; Paschalis, E. P.; Roschger, P., Structure and mechanical quality of the collagen-mineral nano-composite in bone. J. Mater. Chem. 2004, 14, (14), 2115-2123. (3) Wagermaier, W.; Gupta, H. S.; Gourrier, A.; Paris, O.; Roschger, P.; Burghammer, M.; Riekel, C.; Fratzl, P., Scanning texture analysis of lamellar bone using microbeam synchrotron X-ray radiation. Journal of Applied Crystallography 2007, 40, (1), 115-120. (4) Huber, J.; Griesshaber, E.; Nindiyasari, F.; Schmahl, W. W.; Ziegler, A., Functionalization of biomineral reinforcement in crustacean cuticle: Calcite orientation in the partes incisivae of the mandibles of Porcellio scaber and the supralittoral species Tylos europaeus (Oniscidea, Isopoda). Journal of Structural Biology 2015, 190, (2), 173-191. (5) Al‐Sawalmih, A.; Li, C.; Siegel, S.; Fabritius, H.; Yi, S.; Raabe, D.; Fratzl, P.; Paris, O., Microtexture and chitin/calcite orientation relationship in the mineralized exoskeleton of the American lobster. Advanced Functional Materials 2008, 18, (20), 3307-3314. (6) Weaver, J. C.; Milliron, G. W.; Miserez, A.; Evans-Lutterodt, K.; Herrera, S.; Gallana, I.; Mershon, W. J.; Swanson, B.; Zavattieri, P.; DiMasi, E.; Kisailus, D., The Stomatopod Dactyl Club: A Formidable Damage-Tolerant Biological Hammer. Science 2012, 336, (6086), 12751280. (7) Gilow, C.; Zolotoyabko, E.; Paris, O.; Fratzl, P.; Aichmayer, B., Nanostructure of biogenic calcite crystals: a view by small-angle X-ray scattering. Crystal Growth & Design 2011, 11, (6), 2054-2058. (8) Müller, W. E. G., Silicon Biomineralization: Biology, Biochemistry, Molecular Biology, Biotechnology. ed.; Springer: Berlin, 2003; Vol. 33. (9) Mann, S., Molecular tectonics in biomineralization and biomimetic materials chemistry. Nature 1993, 365, (6446), 499-505. (10) Falini, G.; Albeck, S.; Weiner, S.; Addadi, L., Control of Aragonite or Calcite Polymorphism by Mollusk Shell Macromolecules. Science 1996, 271, (5245), 67-69. (11) Arias, J. L.; Fernandez, M. S., Polysaccharides and Proteoglycans in Calcium Carbonatebased Biomineralization. Chem. Rev. 2008, 108, (11), 4475-4482. (12) Rao, A.; Berg, J. K.; Kellermeier, M.; Gebauer, D., Sweet on biomineralization: effects of carbohydrates on the early stages of calcium carbonate crystallization. Eur. J. Mineral. 2014. (13) Henriksen, K.; Stipp, S. L. S.; Young, J. R.; Marsh, M. E., Biological control on calcite crystallization: AFM investigation of coccolith polysaccharide function. Am. Miner. 2004, 89, (11-12), 1709-1716. (14) Wise, E. R.; Maltsev, S.; Davies, M. E.; Duer, M. J.; Jaeger, C.; Loveridge, N.; Murray, R. C.; Reid, D. G., The organic-mineral interface in bone is predominantly polysaccharide. Chem. Mat. 2007, 19, (21), 5055-5057.


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Oriented nucleation and growth of barium sulfate minerals occurs at various length scales in hierarchical lignocellulosic materials. Dendritic crystals are deposited at the interface of the cellular macropores, while directed crystallization in the nano-scale compartments of natural cell walls shows an epitaxial growth of inorganic barite on organic cellulose.


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Scheme of cellular ultrastructure and tracheid cell wall model. The cell wall layers can be distinguished by the texture and orientation of the cellulose microfibrils. Wood fibers consist of an amorphous lignin/hemicellulose matrix and cellulose fibril aggregates, which bundle elementary cellulose fibrils and associated hemicelluloses. Each elementary cellulose fibril contains amorphous and crystalline regions. 1045x346mm (72 x 72 DPI)



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Scanning electron micrographs of spruce cross-section (a) and radial section (b) collected in the backscattered electron mode. Scale-bars correspond to 20 µm. White arrows indicate high degree of mineralization in the inner parts of the cell wall. 879x390mm (72 x 72 DPI)


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Vertex Component Analysis (VCA) of spruce mineralized with BaSO4. Hyperspectral Raman imaging showing endmember distribution and corresponding endmember spectra of lignin (a, d, g), cell wall with BaSO4 inclusions (b, e, h) and pure BaSO4 mineral at the cellular interface (c, f, i). Each scale-bar corresponds to 10 µm. 940x743mm (72 x 72 DPI)



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Synchrotron X-ray scattering mappings of mineralized spruce cross-section (30 x 30 µm2). Scattering intensity mappings of (200) cellulose (orange, a) and (401) (122) barite (blue, b) and overlay (c). Radial 1D profiles (d) from exemplary positions marked by colored squares (c). 721x690mm (72 x 72 DPI)


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a) Radial profile of 2D WAXS pattern from the lumen (grey line) and the cell wall region (black line) of a spruce cross-section. b) X-ray powder diffraction pattern of barite according to the literature 43 44. Bragg peaks are scaled to relative intensities and indexed with the reference to Miller indices of barite. 149x183mm (300 x 300 DPI)



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a) Synchrotron X-ray scattering mapping of spruce radial section mineralized with BaSO4 (20 x 20 µm2). Scattering intensity mappings of (200) cellulose (orange, a) and (401) (122) barite (blue, b) and overlay (c). Radial Q-profiles (d) from exemplary positions marked by colored squares (c) with indexing of cellulose and barite diffraction rings. e) Spotty 2D WAXS pattern indicating random barite orientation. f) Scattering intensity plot of c) as function of azimuthal angle φ and Q-space. g) 2D WAXS pattern from cell wall region h) Scattering intensity plot of e) as function of azimuthal angle φ and Q-space. 503x908mm (72 x 72 DPI)


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Unit cells of cellulose Iβ (upper row) and barite (lower row) projected along [100], [010] and [001] direction (from left to right). The balls represent carbon (brown), hydrogen (grey), oxygen (red), sulfur (yellow) and barium atoms (green). 2425x1402mm (72 x 72 DPI)



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Figure S2. Scanning electron micrograph of spruce cross-section (a, b) and radial section (c, d) at lower magnification. Scale-bar corresponds to 500 µm in a) and 200 µm in b-d. 303x264mm (96 x 96 DPI)


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Figure S3. Vertex Component Analysis (VCA) of spruce mineralized with BaSO4. Hyperspectral Raman imaging showing endmember distribution of cell wall components (a-d). a: Endmember mapping showing highly fluorescent pit membrane. C: Endmember mapping of S2 cell wall. b,f: Endmember mappings of lumina. The endmember spectra corresponding to these mappings are given in (e-f). Each scale-bar corresponds to 10 µm. 222x262mm (72 x 72 DPI)



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Figure S4. Color-coded FWHM mapping of (211) barite reflection fitted with a Pseudo-Voigt (PsdVoigt I) function. a) Mineralized spruce cross-section (Fig. 4). b) Mineralized spruce radial section (Fig. 6). 1524x596mm (72 x 72 DPI)


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Figure S5. Synchrotron X-ray scattering mapping of spruce radial section mineralized with BaSO4 (20 x 20 µm2, Fig. 6). a) Overlay of scattering intensity mappings of (200) cellulose (orange) and (401) (122) barite (blue). b) Summed-up 2D diffraction patterns from regions of interest marked by black frames. A: Nonmineralized cell wall (sum of 105 diffraction patterns). B: Interfacial region of mineralized cell wall (Sum of 63 diffraction patterns). C: Minerals in lumina (Sum of 105 diffraction patterns). D: Mineralized cell wall (Sum of 105 diffraction patterns). 1371x774mm (72 x 72 DPI)



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Oriented nucleation and growth of barium sulfate minerals occurs at various length scales in hierarchical lignocellulosic materials. Dendritic crystals are deposited at the interface of the cellular macropores, while directed crystallization in the nano-scale compartments of natural cell walls shows an epitaxial growth of inorganic barite on organic cellulose. 190x74mm (96 x 96 DPI)


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Oriented Crystallization of Barium Sulfate Confined in Hierarchical

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