Mechanistic insight into biopolymer induced iron oxide mineralization through quantification of molecular bonding.

Microbial production of iron (oxyhydr)oxides on polysaccharide rich biopolymers occurs on such a vast scale that it impacts the global iron cycle and has been responsible for major biogeochemical events. Yet the physiochemical controls these biopolymers exert on iron (oxyhydr)oxide formation are poorly understood. Here we used dynamic force spectroscopy to directly probe binding between complex, model and natural microbial polysaccharides and common iron (oxyhydr)oxides. Applying nucleation theory to our results demonstrates that if there is a strong attractive interaction between biopolymers and iron (oxyhydr)oxides, the biopolymers decrease the nucleation barriers, thus promoting mineral nucleation. These results are also supported by nucleation studies and density functional theory. Spectroscopic and thermogravimetric data provide insight into the subsequent growth dynamics and show that the degree and strength of water association with the polymers can explain the influence on iron (oxyhydr)oxide transformation rates. Combined, our results provide a mechanistic basis for understanding how polymer-mineral-water interactions alter iron (oxyhydr)oxides nucleation and growth dynamics and pave the way for an improved understanding of the consequences of polymer induced mineralization in natural systems.

The mechanisms of crystal growth inhibition by organic and inorganic inhibitors.

Understanding mineral growth mechanism is a key to understanding biomineralisation, fossilisation and diagenesis. The presence of trace compounds affect the growth and dissolution rates and the form of the crystals produced. Organisms use ions and organic molecules to control the growth of hard parts by inhibition and enhancement. Calcite growth in the presence of Mg2+ is a good example. Its inhibiting role in biomineralisation is well known, but the controlling mechanisms are still debated. Here, we use a microkinetic model for a series of inorganic and organic inhibitors of calcite growth. With one, single, nonempirical parameter per inhibitor, i.e. its adsorption energy, we can quantitatively reproduce the experimental data and unambiguously establish the inhibition mechanism(s) for each inhibitor. Our results provide molecular scale insight into the processes of crystal growth and biomineralisation, and open the door for logical design of mineral growth inhibitors through computational methods.

Prebiotic RNA polymerisation: energetics of nucleotide adsorption and polymerisation on clay mineral surfaces.

We measured the binding energy and bonding parameters between model nucleotide functional groups and model clay mineral surfaces in solutions of acidic pH. We demonstrate that basal surfaces of clay minerals interact most strongly with nucleobases and show that the adsorption of the phosphate group to clay edges could facilitate polymerisation. Our results suggest that Al- and Fe-rich edge sites behave similarly in nucleotide polymerisation through change of the phosphodiester bond strength. We present an internally consistent set of thermodynamic parameters that represent the nucleotide-clay mineral system.

Quantifying the free energy landscape between polymers and minerals.

Higher organisms as well as medical and technological materials exploit mineral-polymer interactions, however, mechanistic understanding of these interactions is poorly constrained. Dynamic force spectroscopy can probe the free energy landscape of interacting bonds, but interpretations are challenged by the complex mechanical behavior of polymers. Here we restate the difficulties inherent to applying DFS to polymer-linked adhesion and present an approach to gain quantitative insight into polymer-mineral binding.

Controlling biomineralisation with cations.

The production of polymers for controlling calcite growth is a well-known approach in biomineralising organisms. Numerous studies have shown that polymers significantly influenced the growth rate and morphology of CaCO3 but little is known about how the polymers are actually controlled by the organisms. Here we show that cations control the effect of polysaccharides and that these processes have been in place for at least 60 million years. We studied the interaction between cleaved samples of pure calcite and ancient coccolith associated polysaccharides (aPS) that we had extracted from the samples of Cretaceous chalk, in solutions that contained one of the common seawater cations, K+, Ca2+, Mg2+ and Sr2+. With atomic and chemical force microscopy (AFM and CFM), we showed that K+, Ca2+ and Sr2+ complex aPS through a weak, outer sphere bonding, giving the aPS affinity to sites on steps and terraces. In contrast, Mg2+ enhanced the formation of stronger and longer aPS complexes, resulting in low affinity to calcite terraces and strong affinity to steps. It is known that adsorption is influenced by ionic potential and ionic strength. Our results show that cation-polysaccharide complexing can modify the effectiveness of the polymer. Thus, creating organic molecules with cation complexing ability is an effective strategy for regulating mineral growth, both now and in the past.

A Microkinetic Model of Calcite Step Growth.

In spite of decades of research, mineral growth models based on ion attachment and detachment rates fail to predict behavior beyond a narrow range of conditions. Here we present a microkinetic model that accurately reproduces calcite growth over a very wide range of published experimental data for solution composition, saturation index, pH and impurities. We demonstrate that polynuclear complexes play a central role in mineral growth at high supersaturation and that a classical complexation model is sufficient to reproduce measured rates. Dehydration of the attaching species, not the mineral surface, is rate limiting. Density functional theory supports our conclusions. The model provides new insights into the molecular mechanisms of mineral growth that control biomineralization, mineral scaling and industrial material synthesis.

Infrared spectroscopy and density functional theory investigation of calcite, chalk, and coccoliths--do we observe the mineral surface?

We have measured infrared spectra from several types of calcite: chalk, freshly cultured coccoliths produced by three species of algae, natural calcite (Iceland Spar), and two types of synthetic calcite. The most intense infrared band, the asymmetric carbonate stretch vibration, is clearly asymmetric for the coccoliths and the synthetic calcite prepared using the carbonation method. It can be very well fitted by two peaks: a narrow Lorenzian at lower frequency and a broader Gaussian at higher frequency. These two samples both have a high specific surface area. Density functional theory for bulk calcite and several calcite surface systems allows for assignment of the infrared bands. The two peaks that make up the asymmetric carbonate stretch band come from the bulk (narrow Lorenzian) and from a combination of two effects (broad Gaussian): the surface or near surface of calcite and line broadening from macroscopic dielectric effects. We detect water adsorbed on the high surface area synthetic calcite, which permits observation of the chemistry of thin liquid films on calcite using transmission infrared spectroscopy. The combination of infrared spectroscopy and density functional theory also allowed us to quantify the amount of polysaccharides associated with the coccoliths. The amount of polysaccharides left in chalk, demonstrated to be present in other work, is below the IR detection limit, which is 0.5% by mass.

Binding of ethanol on calcite: the role of the OH bond and its relevance to biomineralization.

The interaction of OH-containing compounds with calcite, CaCO(3), such as is required for the processes that control biomineralization, has been investigated in a low-water solution. We used ethanol (EtOH) as a simple, model, OH-containing organic compound, and observed the strength of its adsorption on calcite relative to OH from water and the consequences of the differences in interaction on crystal growth and dissolution. A combination of atomic force microscopy (AFM) and molecular dynamics (MD) simulations showed that EtOH attachment on calcite is stronger than HOH binding and that the first adsorbed layer of ethanol is highly ordered. The strong ordering of the ethanol molecules has important implications for mineral growth and dissolution because it produces a hydrophobic layer. Ethanol ordering is disturbed along steps and at defect sites, providing a bridge from the bulk solution to the surface. The strong influence of calcite in structuring ethanol extends further into the liquid than expected from electrical double-layer theory. This suggests that in fluids where water activity is low, such as in biological systems optimized for biomineralization, organic molecules can control ion transport to and from the mineral surface, confining it to specific locations, thus providing the organism with control for biomineral morphology.

Interaction of ethanol and water with the {1014} surface of calcite.

Molecular dynamics simulations have been used to model the interaction between ethanol, water, and the {1014} surface of calcite. Our results demonstrate that a single ethanol molecule is able to form two interactions with the mineral surface (both Ca-O and O-H), resulting in a highly ordered, stable adsorption layer. In contrast, a single water molecule can only form one or other of these interactions and is thus less well bound, resulting in a more unstable adsorption layer. Consequently, when competitive adsorption is considered, ethanol dominates the adsorption layer that forms even when the starting configuration consists of a complete monolayer of water at the surface. The computational results are in good agreement with the results from atomic force microscopy experiments where it is observed that a layer of ethanol remains attached to the calcite surface, decreasing its ability to interact with water and for growth at the {1014} surface to occur. This observation, and its corresponding molecular explanation, may give some insight into the ability to control crystal form using mixtures of different organic solvents.