New insights into the molecular-level control of silica mineralization by diatoms

Marine diatoms are arguably the most important silica-mineralizing organisms in modern seas. They incorporate gigatons of Si into their siliceous cell walls annually, and control the concentration and bioavailability of silicon in marine environments. Although the roles that diatoms assume in regulating the global carbon cycle often go unrecognized, their ecological success places them alongside marine calcifiers as major players in the sequestration of organic carbon in the surface ocean. Consequently, most investigations have focused upon understanding how calcifying organisms mineralize their skeletons, and the silica biomineralization literature remains minimal. However, understanding how silicifying organisms control the deposition of silica is becoming increasingly important for a variety of forefront issues in science and technology. The increasing utilization of δO18 values obtained from biologically formed silica in paleoclimate research has recently raised questions about how the structural relationship between diatom silica and the macromolecular organic components of the cell wall might influence the quality of isotopic measurements. Biochemical investigations have begun to yield information about structural and chemical properties of organic macromolecules involved in biosilicification processes. Molecules that have been identified as part of the silicification mechanism either possess regions of locally concentrated positive and negative charge (silaffins), or require the presence of specific counter ions such as phosphate to control the assembly of the polycationic constituents (polyamines) of the organic matrix; however, the mechanisms by which these molecules control the spatial and temporal onset of biosilica formation remain unclear. As a first step towards quantifying the kinetic and thermodynamic drivers behind heterogeneous nucleation in biological systems, we have developed a new and novel approach that marries tapping mode atomic force microscopy with elements of modern materials chemistry, to directly measure the rate of amorphous silica nucleation on COOH, NH3+, and COOH / NH3+-terminated surfaces under controlled solution conditions. Our results provide new insights into the molecular-level control of silica mineralization in diatoms. We show that differences between substrate-specific nucleation rates are controlled largely by kinetic factors rather than thermodynamic drivers, and that amine-terminated surfaces are not capable of triggering the onset of silica deposition without the synergistic activity of neighboring negatively charged species on the surface or in solution (e.g. carboxyl or phosphoryl groups). In light of this result we conclude that sites on the organic matrix that have phosphate and amine moieties in close proximity serve not only as contact points between the constituent macromolecules in the matrix, but also as initial sites of silica deposition.