Unraveling the atomic structure of biogenic silica: evidence of the structural association of Al and Si in diatom frustules

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Abstract

We used X-ray absorption spectroscopy at the Al K-edge to investigate the atomic structure of biogenic silica and to assess the effect of Al on its crystal chemistry. Our study provides the first direct evidence for a structural association of Al and Si in biogenic silica. In samples of cultured diatoms, Al is present exclusively in fourfold coordination. The location and relative intensity of X-ray absorption near-edge structure (XANES) features suggests the structural insertion of tetrahedral Al inside the silica framework synthesized by the organism. In diatom samples collected in the marine environment, Al is present in mixed six- and fourfold coordination. The relative intensity of XANES structures indicates the coexistence of structural Al with a clay component, which most likely reflects sample contamination by adhering mineral particles. Extended X-ray absorption fine structure spectroscopy has been used to get Al-O distances in biogenic silica of cultured diatoms, confirming a tetrahedral coordination. Because of its effect on solubility and reaction kinetics of biogenic silica, the structural association between Al and biogenic silica at the stage of biosynthesis has consequences for the use of sedimentary biogenic silica as an indicator of past environmental conditions.

Introduction

Biogenic siliceous particles, made of amorphous, hydrated SiO2, are produced in the upper water column as skeletal elements by diatoms, radiolaria, and silicoflagellates. Ocean waters are undersaturated (<100 μmol/L) with respect to biogenic Si, for which a solubility of 1000 μmol/L (2°C) has been reported (Tréguer et al., 1995). Despite its thermodynamic tendency to dissolve, a fraction of biogenic Si survives transfer through the water column and accumulates in abyssal sediments. Biogenic silica (BSi) is a major constituent of marine sediments, and its sedimentary record provides potentially valuable information of past ocean productivity and ecosystem structure. Our capability to interpret the sedimentary record of BSi in terms of past environmental conditions is presently limited by our lack of understanding of the processes controlling its preservation Archer et al 1993, McManus et al 1995, Nelson et al 1995.

The preservation of BSi is controlled by a competition between dissolution and removal from the undersaturated waters by burial. In surface sediments, the ongoing dissolution is revealed by the buildup of silicic acid (Si[OH]4) in pore waters to quasi-constant levels below 5 to 30 cm deep. Reported asymptotic Si(OH)4 levels range from 100 to 850 μmol/L Hurd 1973, Fanning and Pilson 1974, Archer et al 1993, McManus et al 1995, Sayles et al 1996, Rabouille et al 1997 and are in general below the solubility of fresh plankton assemblages (Lawson et al., 1978) or diatom cultures (Kamatani et al., 1980). Several hypotheses have been proposed to account for the lowered apparent solubility in sediments. Instead of reflecting a thermodynamic equilibrium between pore waters and the dissolving phase, asymptotic Si(OH)4 might result from the kinetic competition between release of Si(OH)4 from dissolving BSi and its uptake by the formation of aluminosilicate minerals (reverse weathering; Mackenzie and Garrels 1966, Garrels and Mackenzie 1971, Ristvet 1978, Mackenzie et al 1981). While Michalopoulos and Aller (1995) documented the importance of reverse weathering reactions for sediments of the Amazon river continental shelf, clay neoformation driven by dissolved Al was verified experimentally by Dixit et al. (2001).

Alternatively, the solubility of BSi in marine sediments, after correction for pressure and temperature effects, might differ from estimates obtained for fresh plankton assemblages. Preferential dissolution of species with higher specific surface areas or fragile structures such as spines during the settling of diatom frustules through the water column results in a reduction of specific surface area of siliceous assemblages Hurd et al 1981, Hurd and Birdwhistell 1983, Barker et al 1994, Van Cappellen 1996, Dixit et al 2001. This process alone, however, cannot account for the apparent low solubilities of BSi in marine sediments (Dixit et al., 2001). After removal of the organic matrix, Al is the most important factor regulating the solubility of BSi Lewin 1961, Iler 1973. The solubility is decreased significantly by only minor amounts of Al, >0.1% Van Bennekom et al 1989, Van Bennekom et al 1991, compared to an average diatom Al/Si ratio of 1/1000 (Martin and Knauer, 1973). The interaction between BSi and dissolved Al produced by the dissolution of detrital minerals has been readdressed recently Van Cappellen 1996, Van Cappellen 1997a, Van Cappellen 1997b, Dixit et al 2001. The authors demonstrated the importance of diagenetic Al uptake by diatom frustules in modifying BSi solubility relative to that of fresh plankton assemblages.

The present study focuses on the association of Al with BSi. The underlying questions are, is Al incorporated into the frustules, or is it bound to the surface? If it is incorporated, can we identify a structural effect of its presence? While the structural incorporation of Al has been demonstrated for synthetic Si gels (Stone et al., 1993) and nonbiogenic low-temperature opals (Ildefonse and Calas, 1997), there is to date no conclusive evidence for the opal synthesized by diatoms. A straightforward analogy between synthetic gels, nonbiogenic mineral formation, and biomineralization might be misleading. We have used X-ray absorption spectroscopy (XAS) Calas et al 1984, Brown et al 1988 to unravel the crystal chemistry of BSi and provide the first results on the structural association of Al with Si in diatom frustules. While Al K-edge X-ray absorption near-edge structure (XANES) spectra indicate the insertion of Al in the BSi framework of cultured diatoms in tetrahedral coordination, they reveal the coexistence of structural Al with smectite- and illite-type clay phases in natural marine diatom frustules. Extended X-ray fine structure (EXAFS) spectroscopy has been used to get Al-O distances in BSi of cultured diatoms, confirming a tetrahedral coordination.

Section snippets

Material

We compared diatom samples derived from cultures and the marine environment. Cultured diatoms were chosen to provide an end-member of known particle history on which the feasibility of our approach could be tested. Diatom samples used in this study are listed in Table 1 along with the corresponding atomic Al-to-Si ratios. Samples from diatom cultures Porosira glacialis (LV1) and Thalassiosira nordenskjiöldii (86) cover the low end of frustule Al-to-Si ratios. These ratios (Table 1) were too

Analytical methods

Al K-edge XANES and EXAFS spectra were collected on the SA 32 line (E range 0.8 to 3.5 keV) at the LURE/Super-ACO synchrotron radiation facility (Orsay, France). The storage ring was operating at 800 MeV positron energy and 100 to 300 mA positron current. The X-ray beam was monochromatized using a Yb66 double-crystal monochromator. Samples were powdered onto pure indium and mounted on a copper slide. Spectra were calibrated with a pure Al foil at the inflexion point of the K-edge (1559 eV) and

XANES spectroscopy: reference compounds

Al K-edge XANES spectra of Al-bearing reference compounds are presented in Figure 1. Al K-edge XANES spectra of albite (tetrahedral Al), kaolinite (octahedral Al), and nonbiogenic opal-A (tetrahedral Al) are plotted in Figure 1a. Spectra of muscovite (mixed coordination), smectite (mixed coordination), and illite (mixed coordination) are shown in Figure 1b. The energy positions of main Al K-edge structures are summarized in Table 3.

Al K-edge XANES spectra of tetrahedral Al-bearing minerals,

Structural interpretation of spectra of cultured diatoms

Aluminum may enter the framework of amorphous silica by two distinct structural processes (Narshneyer, 1994). It may enter as a network former, preserving the three-dimensional structure built by the corner sharing SiO4 tetrahedra, provided there is charge compensation by alkalis or alkaline earths located in a nearby position. Alternatively, a nonbridging oxygen is created by the presence of two octahedral Al atoms linked to an oxygen belonging to a SiO4 tetrahedron. At low temperature, Al is

Conclusions

Al K-edge XANES and EXAFS spectra collected for diatoms underline the structural association between Al and Si in diatom frustules. In samples of cultured diatoms, Al is present exclusively in fourfold coordination. The location and relative intensities of XANES features suggest the structural insertion of tetrahedral Al inside the silica framework synthesized by the organism. The peculiar structural position of Al within the BSi framework is invoked to explain the inhibiting effect of Al on

Acknowledgments

The first author dedicates this study to Prof. R. Wollast (Laboratoire d’Océanographie Chimique, Université Libre de Bruxelles) for initiating her to the silica problem during her Ph.D. work. She thanks F. T. Mackenzie for many fruitful discussions during the past years. This manuscript benefited from constructive comments by P. Anschutz, P. Van Cappellen, and P. N. Froelich. This study was carried out at the Laboratoire d’Utilisation du Rayonnement Electromagnétique (LURE), Orsay, France (LURE

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