Oriented Crystallization of Barium Sulfate Confined ... - ACS Publications

Subscriber access provided by University of Newcastle, Australia

Article

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

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Crystal Growth & Design is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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

1


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 40

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.


2

Page 3 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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.


3


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 4 of 40

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.


4

Page 5 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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


5


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 6 of 40

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.


6

Page 7 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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 ≈


7


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 8 of 40

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


8

Page 9 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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.


9


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 10 of 40

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.


10

Page 11 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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


11


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 12 of 40

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.


12

Page 13 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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.


13


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 14 of 40

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.


14

Page 15 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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


15


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

according to the literature

47 48

Page 16 of 40

. 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).


16

Page 17 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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).


17


Page 18 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 ACS Paragon Plus Environment

18

Page 19 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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


19


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 20 of 40

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


20

Page 21 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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


21


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 22 of 40

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


22

Page 23 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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


23


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 24 of 40

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.


24

Page 25 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(15) Krejci, M. R.; Wasserman, B.; Finney, L.; McNulty, I.; Legnini, D.; Vogt, S.; Joester, D., Selectivity in biomineralization of barium and strontium. Journal of Structural Biology 2011, 176, (2), 192-202. (16) Benton, W. J.; Collins, I. R.; Grimsey, I. M.; Parkinson, G. M.; Rodger, S. A., Nucleation, growth and inhibition of barium sulfate-controlled modification with organic and inorganic additives. Faraday Discussions 1993, 95, (0), 281-297. (17) Pina, C. M.; Becker, U.; Risthaus, P.; Bosbach, D.; Putnis, A., Molecular-scale mechanisms of crystal growth in barite. Nature 1998, 395, (6701), 483-486. (18) Takiyama, K., Formation and Aging of Precipitates. X. An Electron Micro-Diffraction Study on Crystal Habit of Barium Sulfate Precipitates. Bulletin of the Chemical Society of Japan 1959, 32, (1), 68-70. (19) Liu, S. T.; Nancollas, G. H.; Gasiecki, E. A., Scanning electron microscopic and kinetic studies of the crystallization and dissolution of barium sulfate crystals. J. Cryst. Growth 1976, 33, (1), 11-20. (20) Rautaray, D.; Sainkar, S.; Sastry, M., Highly organized assembly of barite crystals grown within thermally evaporated AOT thin films. CrystEngComm 2003, 5, (70), 400-404. (21) Li, M.; Mann, S., Emergence of Morphological Complexity in BaSO4 Fibers Synthesized in AOT Microemulsions. Langmuir 2000, 16, (17), 7088-7094. (22) Heywood, B. R.; Mann, S., Organic template-directed inorganic crystallization: oriented nucleation of barium sulfate under compressed Langmuir monolayers. Journal of the American Chemical Society 1992, 114, (12), 4681-4686. (23) Qi, L.; Cölfen, H.; Antonietti, M.; Li, M.; Hopwood, J. D.; Ashley, A. J.; Mann, S., Formation of BaSO4 Fibres with Morphological Complexity in Aqueous Polymer Solutions. Chemistry – A European Journal 2001, 7, (16), 3526-3532. (24) Cölfen, H.; Qi, L.; Mastai, Y.; Börger, L., Formation of Unusual 10-Petal BaSO4 Structures in the Presence of a Polymeric Additive. Crystal Growth & Design 2002, 2, (3), 191196. (25) Yu, S.-H.; Antonietti, M.; Cölfen, H.; Hartmann, J., Growth and Self-Assembly of BaCrO4 and BaSO4 Nanofibers toward Hierarchical and Repetitive Superstructures by PolymerControlled Mineralization Reactions. Nano Letters 2003, 3, (3), 379-382. (26) Yu, S.-H.; Cölfen, H., Bio-inspired crystal morphogenesis by hydrophilic polymers. J. Mater. Chem. 2004, 14, (14), 2124-2147. (27) Wang, T.; Cölfen, H., In Situ Investigation of Complex BaSO4 Fiber Generation in the Presence of Sodium Polyacrylate. 1. Kinetics and Solution Analysis. Langmuir 2006, 22, (21), 8975-8985. (28) Wang, T.; Reinecke, A.; Cölfen, H., In Situ Investigation of Complex BaSO4 Fiber Generation in the Presence of Sodium Polyacrylate. 2. Crystallization Mechanisms. Langmuir 2006, 22, (21), 8986-8994. (29) Bromley, L. A.; Cottier, D.; Davey, R. J.; Dobbs, B.; Smith, S.; Heywood, B. R., Interactions at the organic/inorganic interface: molecular design of crystallization inhibitors for barite. Langmuir 1993, 9, (12), 3594-3599. (30) Ruiz-Agudo, C.; Ruiz-Agudo, E.; Putnis, C. V.; Putnis, A., Mechanistic Principles of Barite Formation: From Nanoparticles to Micron-Sized Crystals. Crystal Growth & Design 2015, 15, (8), 3724-3733. (31) Newman, R. H., Estimation of the relative proportions of cellulose I alpha and I beta in wood by carbon-13 NMR spectroscopy. Holzforschung 1999, 53, (4), 335-340.


25


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 26 of 40

(32) Krywka, C.; Keckes, J.; Storm, S.; Buffet, A.; Roth, S. V.; Döhrmann, R.; Müller, M., Nanodiffraction at MINAXS (P03) beamline of PETRA III. Journal of Physics: Conference Series 2013, 425, (7), 072021. (33) Storm, S.; Ogurreck, M.; Laipple, D.; Krywka, C.; Burghammer, M.; Di Cola, E.; Muller, M., On radiation damage in FIB-prepared softwood samples measured by scanning X-ray diffraction. Journal of Synchrotron Radiation 2015, 22, (2), 267-272. (34) Zabler, S.; Paris, O.; Burgert, I.; Fratzl, P., Moisture changes in the plant cell wall force cellulose crystallites to deform. Journal of Structural Biology 2010, 171, (2), 133-141. (35) Fernandes, A. N.; Thomas, L. H.; Altaner, C. M.; Callow, P.; Forsyth, V. T.; Apperley, D. C.; Kennedy, C. J.; Jarvis, M. C., Nanostructure of cellulose microfibrils in spruce wood. Proceedings of the National Academy of Sciences of the United States of America 2011, 108, (47), E1195-E1203. (36) Nishiyama, Y.; Langan, P.; Chanzy, H., Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction. Journal of the American Chemical Society 2002, 124, (31), 9074-9082. (37) Andersson, S.; Serimaa, R.; Paakkari, T.; SaranpÄÄ, P.; Pesonen, E., Crystallinity of wood and the size of cellulose crystallites in Norway spruce (Picea abies). J. Wood Sci. 2003, 49, (6), 531-537. (38) Fahlén, J.; Salmén, L., Pore and Matrix Distribution in the Fiber Wall Revealed by Atomic Force Microscopy and Image Analysis. Biomacromolecules 2005, 6, (1), 433-438. (39) Donaldson, L., Cellulose microfibril aggregates and their size variation with cell wall type. Wood Sci. Technol. 2007, 41, (5), 443-460. (40) Fritz-Popovski, G.; Van Opdenbosch, D.; Zollfrank, C.; Aichmayer, B.; Paris, O., Development of the Fibrillar and Microfibrillar Structure During Biomimetic Mineralization of Wood. Advanced Functional Materials 2013, 23, (10), 1265-1272. (41) Merk, V.; Chanana, M.; Keplinger, T.; Gaan, S.; Burgert, I., Hybrid wood materials with improved fire retardance by bio-inspired mineralisation on the nano- and submicron level. Green Chem. 2015, 17, (3), 1423-1428. (42) Merk, V.; Chanana, M.; Gaan, S.; Burgert, I., Mineralization of wood by calcium carbonate insertion for improved flame retardancy. Holzforschung 2016, 70, (9), 867-876. (43) Merk, V.; Chanana, M.; Gierlinger, N.; Hirt, A. M.; Burgert, I., Hybrid Wood Materials with Magnetic Anisotropy Dictated by the Hierarchical Cell Structure. ACS Appl. Mater. Interfaces 2014, 6, (12), 9760-9767. (44) Krywka, C.; Neubauer, H.; Priebe, M.; Salditt, T.; Keckes, J.; Buffet, A.; Roth, S. V.; Doehrmann, R.; Mueller, M., A two-dimensional waveguide beam for X-ray nanodiffraction. J. Appl. Cryst 2012, 45, 85-92. (45) Hammersley, A., FIT2D V12. 012 Reference Manual V6. 0. ESRF International Report No. ESRF98HA01T. Program available at http://www. esrf. eu/computing/scientific/FIT2D 2004. (46) Woodcock, C.; Sarko, A., Packing Analysis of Carbohydrates and Polysaccharides. 11. Molecular and Crystal Structure of Native Ramie Cellulose. Macromolecules 1980, 13, (5), 1183-1187. (47) Mineral powder diffraction file: Sets 1-42. ed.; International Centre for Diffraction Data: Swarthmore, Pennsylvania, 1993. (48) Colville, A. A.; Staudham.K, A Refinement of Structure of Barite. Am. Miner. 1967, 52, (11-1), 1877-1880.


26

Page 27 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(49) Momma, K.; Izumi, F., VESTA 3 for three-dimensional visualization of crystal, volumetric and morphology data. Journal of Applied Crystallography 2011, 44, (6), 1272-1276. (50) Dunn, K.; Daniel, E.; Shuler, P. J.; Chen, H. J.; Tang, Y.; Yen, T. F., Mechanisms of Surface Precipitation and Dissolution of Barite: A Morphology Approach. Journal of Colloid and Interface Science 1999, 214, (2), 427-437. (51) Oaki, Y.; Imai, H., Experimental Demonstration for the Morphological Evolution of Crystals Grown in Gel Media. Crystal Growth & Design 2003, 3, (5), 711-716. (52) Imai, H., Self-organized formation of hierarchical structures. In Biomineralization I: Crystallization and Self-Organization Process, Naka, K., Ed. 2007; Vol. 270, pp 43-72. (53) Vitagliano, V.; Lyons, P., Diffusion coefficients for aqueous solutions of sodium chloride and barium chloride. Journal of the American Chemical Society 1956, 78, (8), 1549-1552. (54) Rard, J. A.; Miller, D. G., The mutual diffusion coefficients of Na2SO4−H2O and MgSO4−H2O at 25°C from Rayleigh interferometry. Journal of Solution Chemistry 1979, 8, (10), 755-766. (55) Kucher, M.; Babic, D.; Kind, M., Precipitation of barium sulfate: Experimental investigation about the influence of supersaturation and free lattice ion ratio on particle formation. Chemical Engineering and Processing: Process Intensification 2006, 45, (10), 900907. (56) Wong, D. C. Y.; Jaworski, Z.; Nienow, A. W., Effect of ion excess on particle size and morphology during barium sulphate precipitation: an experimental study. Chemical Engineering Science 2001, 56, (3), 727-734. (57) Haley, L. V.; Mattioli, T. A.; Wiles, D. R., Micro-Raman Study of Barium Sulphate Coprecipitated with Potassium Ions. Journal of Raman Spectroscopy 1987, 18, (2), 101-104. (58) Gierlinger, N., Revealing changes in molecular composition of plant cell walls on the micron-level by Raman mapping and vertex component analysis (VCA). Frontiers in Plant Science 2014, 5, (306). (59) Gierlinger, N.; Keplinger, T.; Harrington, M., Imaging of plant cell walls by confocal Raman microscopy. Nat. Protocols 2012, 7, (9), 1694-1708. (60) Monnin, C., A thermodynamic model for the solubility of barite and celestite in electrolyte solutions and seawater to 200°C and to 1 kbar. Chemical Geology 1999, 153, (1–4), 187-209. (61) Maréchal, Y.; Chanzy, H., The hydrogen bond network in Iβ cellulose as observed by infrared spectrometry. Journal of Molecular Structure 2000, 523, (1–3), 183-196. (62) Bergenstråhle, M.; Wohlert, J.; Himmel, M. E.; Brady, J. W., Simulation studies of the insolubility of cellulose. Carbohydr. Res. 2010, 345, (14), 2060-2066. (63) Altaner, C.; Apperley, D. C.; Jarvis, M. C., Spatial relationships between polymers in Sitka spruce: Proton spin-diffusion studies. Holzforschung 2006, 60, (6), 665-673. (64) Viëtor, R. J.; Newman, R. H.; Ha, M. A.; Apperley, D. C.; Jarvis, M. C., Conformational features of crystal‐surface cellulose from higher plants. The Plant Journal 2002, 30, (6), 721731. (65) Lee, C. M.; Kubicki, J. D.; Fan, B.; Zhong, L.; Jarvis, M. C.; Kim, S. H., HydrogenBonding Network and OH Stretch Vibration of Cellulose: Comparison of Computational Modeling with Polarized IR and SFG Spectra. The Journal of Physical Chemistry B 2015, 119, (49), 15138-15149.


27


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 28 of 40

(66) Altaner, C. M.; Thomas, L. H.; Fernandes, A. N.; Jarvis, M. C., How Cellulose Stretches: Synergism between Covalent and Hydrogen Bonding. Biomacromolecules 2014, 15, (3), 791798. (67) Åkerholm, M.; Salmén, L., Interactions between wood polymers studied by dynamic FTIR spectroscopy. Polymer 2001, 42, (3), 963-969.

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.


28

Page 29 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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)



1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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)


Page 30 of 40

Page 31 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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)



1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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)


Page 32 of 40

Page 33 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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)



1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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)


Page 34 of 40

Page 35 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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)



1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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)


Page 36 of 40

Page 37 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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)



1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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)


Page 38 of 40

Page 39 of 40

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


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)



1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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)


Page 40 of 40

Oriented Crystallization of Barium Sulfate Confined ... - ACS Publications

Recommend Documents