Local Light-Controlled Generation of Calcium Carbonate and Barium Carbonate Biomorphs via Photochemical Stimulation.

Photochemical activation is proposed as a general method for controlling the crystallization of sparingly soluble carbonates in space and time. The photogeneration of carbonate in an alkaline environment is achieved upon photo-decarboxylation of an organic precursor by using a conventional 365 nm UV LED. Local irradiation was conducted focusing the LED light on a 300 µm radius spot on a closed glass crystallization cell. The precursor solution was optimized to avoid the precipitation of the photoreaction organic byproducts and prevent photo-induced pH changes to achieve the formation of calcium carbonate only in the corresponding irradiated area. The crystallization was monitored in real-time by time-lapse imaging. The method is also shown to work in gels. Similarly, it was also shown to photo-activate locally the formation of barium carbonate biomorphs. In the last case, the morphology of these biomimetic structures was tuned by changing the irradiation intensity.

Prebiotic Organic Chemistry of Formamide and the Origin of Life in Planetary Conditions: What We Know and What Is the Future.

The goal of prebiotic chemistry is the depiction of molecular evolution events preceding the emergence of life on Earth or elsewhere in the cosmos. Plausible experimental models require geochemical scenarios and robust chemistry. Today we know that the chemical and physical conditions for life to flourish on Earth were at work much earlier than thought, i.e., earlier than 4.4 billion years ago. In recent years, a geochemical model for the first five hundred million years of the history of our planet has been devised that would work as a cradle for life. Serpentinization processes in the Hadean eon affording self-assembled structures and vesicles provides the link between the catalytic properties of the inorganic environment and the impressive chemical potential of formamide to produce complete panels of organic molecules relevant in pre-genetic and pre-metabolic processes. Based on an interdisciplinary approach, we propose basic transformations connecting geochemistry to the chemistry of formamide, and we hint at the possible extension of this perspective to other worlds.

Complex Morphogenesis by a Model Intrinsically Disordered Protein.

The development of intricate and complex self-assembling structures in the micrometer range, such as biomorphs, is a major challenge in materials science. Although complex structures can be obtained from self-assembling materials as they segregate from solution, their size is usually in the nanometer range or requires accessory techniques. Previous studies with intrinsically disordered proteins (IDPs) have shown that the active interplay of different molecular interactions provides access to new and more complex nanostructures. As such, it is hypothesized that enriching the variety of intra- and intermolecular interactions in a model IDP will widen the landscape of sophisticated intermediate structures that can be accessed. In this study, a model silk-elastin-like recombinamer capable of interacting via three non-covalent interactions, namely hydrophobic, ion-pairing, and H-bonding is built. This model material is shown to self-assemble into complex stable micrometer-sized biomorphs. Variation of the block composition, pH, and temperature demonstrates the necessary interplay of all three interactions for the formation of such complex structures.

Chasing Synthetic Life: A Tale of Forms, Chemical Fossils, and Biomorphs.

This Essay focuses briefly on early studies elaborated by natural and chemical philosophers, and the once-called synthetic biologists, who postulated the transition from inanimate to animate matter and even foresaw the possibility of creating artificial life on the basis of physical and chemical principles only. Such ideas and speculations, ranging from soundness to weirdness, paved however the way to current developments in areas like abiotic pattern formation, cell compartmentalization, biomineralization, or the origin of life itself. In particular, the generation of biomorphs and their relationship to microfossils represents an active research domain and seems to be the logical way to bring the historical work up to the future, as some scientists are trying to make artificial cells. The last sections of this essay will also highlight modern science aimed at understanding what life is and, whether or not, it can be redefined in chemical terms.

Earth's earliest and deepest purported fossils may be iron-mineralized chemical gardens.

Recognizing fossil microorganisms is essential to the study of life's origin and evolution and to the ongoing search for life on Mars. Purported fossil microbes in ancient rocks include common assemblages of iron-mineral filaments and tubes. Recently, such assemblages have been interpreted to represent Earth's oldest body fossils, Earth's oldest fossil fungi, and Earth's best analogues for fossils that might form in the basaltic Martian subsurface. Many of these putative fossils exhibit hollow circular cross-sections, lifelike (non-crystallographic, constant-thickness, and bifurcate) branching, anastomosis, nestedness within 'sheaths', and other features interpreted as strong evidence for a biological origin, since no abiotic process consistent with the composition of the filaments has been shown to produce these specific lifelike features either in nature or in the laboratory. Here, I show experimentally that abiotic chemical gardening can mimic such purported fossils in both morphology and composition. In particular, chemical gardens meet morphological criteria previously proposed to establish biogenicity, while also producing the precursors to the iron minerals most commonly constitutive of filaments in the rock record. Chemical gardening is likely to occur in nature. Such microstructures should therefore not be assumed to represent fossil microbes without independent corroborating evidence.

A Universal Geochemical Scenario for Formamide Condensation and Prebiotic Chemistry.

The condensation of formamide has been shown to be a robust chemical pathway affording molecules necessary for the origin of life. It has been experimentally demonstrated that condensation reactions of formamide are catalyzed by a number of minerals, including silicates, phosphates, sulfides, zirconia, and borates, and by cosmic dusts and meteorites. However, a critical discussion of the catalytic power of the tested minerals, and the geochemical conditions under which the condensation would occur, is still missing. We show here that mineral self-assembled structures forming under alkaline silica-rich solutions are excellent catalysts for the condensation of formamide with respect to other minerals. We also propose that these structures were likely forming as early as 4.4 billion years ago when the whole earth surface was a reactor, a global scale factory, releasing large amounts of organic compounds. Our experimental results suggest that the conditions required for the synthesis of the molecular bricks from which life self-assembles, rather than being local and bizarre, appears to be universal and geologically rather conventional.

Influence of Intramineral Proteins on the Growth of Carbonate Crystals Using as a Scaffold Membranes of Ratite Birds and Crocodiles Eggshells.

The lack of information on structural basis where proteins are involved, as well as the biomineralization processes of different systems such as bones, diatom frustules, and eggshells, have intrigued scientists from different fields for decades. This scientific curiosity has led to the use of methodologies that help understand the mechanism involved in the formation of these complex structures. Therefore, this work focuses on the use of eggshell membranes from different species of ratites (emu and ostrich) and reptiles (two species of crocodiles) as a model to differentiate biocalcification and biosilicification by introducing calcium phosphate or silica inside the membrane fiber mantles. We performed this to obtain information about the process of eggshell formation as well as the changes that occur in the membrane during crystal formation. In order to identify and understand the early processes leading to the formation of the microstructures present in the eggshell, we decided to carry out the synthesis of silica-carbonate of calcium, barium, and strontium called biomorph in the presence of intramineral proteins. This was carried out to evaluate the influence of these proteins on the formation of specific structures. We found that the proteins on untreated membranes, present a structural growth similar to those observed in the inner part of the eggshell, while in treated membranes, the structures formed present a high similarity with those observed in the outer and intermediate part of the eggshell. Finally, a topographic and molecular analysis of the biomorphs and membranes was performed by scanning electron microscopy (SEM), Raman and Fourier-transform Infrared (FTIR) spectroscopies.

Chemical Gardens Mimic Electron Paramagnetic Resonance Spectra and Morphology of Biogenic Mn Oxides.

Manganese (Mn) oxides are ubiquitous in nature and occur as both biological and abiotic minerals, but empirically distinguishing between the two remains a problem. Recently, electron paramagnetic resonance (EPR) spectroscopy has been proposed for this purpose. It has been reported that biogenic Mn oxides display a characteristic narrow linewidth in contrast to their pure abiotic counterparts, which is explained in part by the large number of cation vacancies that form within the layers of biogenic Mn oxides. It was, therefore, proposed that natural samples that display a narrow EPR linewidth, ΔHpp < 580G, could be assigned to a biogenic origin. However, in poorly crystalline or amorphous solids, both dipolar broadening and exchange narrowing simultaneously determine the linewidth. Considering that the spectral linewidth is governed by several mechanisms, this approach might be questioned. In this study, we report synthetic chemical garden Mn oxide biomorphs that exhibit both morphologically life-like structures and narrow EPR linewidths, suggesting that a narrow EPR line may be unsuitable as reliable evidence in assessment of biogenicity.

Distinguishing cellular from abiotic spheroidal microstructures in the ca. 3.4 Ga Strelley Pool Formation.

The morphogenesis of most carbonaceous microstructures that resemble microfossils in Archean (4-2.5 Ga old) rocks remains debated. The associated carbonaceous matter may even-in some cases-derive from abiotic organic molecules. Mineral growths associated with organic matter migration may mimic microbial cells, some anatomical features, and known microfossils-in particular those with simple spheroid shapes. Here, spheroid microstructures from a chert of the ca. 3.4 Ga Strelley Pool Formation (SPF) of the Pilbara Craton (Western Australia) were imaged and analyzed with a combination of high-resolution in situ techniques. This provides new insights into carbonaceous matter distributions and their relationships with the crystallographic textures of associated quartz. Thus, we describe five new types of spheroids and discuss their morphogenesis. In at least three types of microstructures, wall coalescence argues for migration of carbonaceous matter onto abiotic siliceous spherulites or diffusion in poorly crystalline silica. The nanoparticulate walls of these coalescent structures often cut across multiple quartz crystals, consistent with migration in/on silica prior to quartz recrystallization. Sub-continuous walls lying at quartz boundaries occur in some coalescent vesicles. This weakens the "continuous carbonaceous wall" criterion proposed to support cellular inferences. In contrast, some clustered spheroids display wrinkled sub-continuous double walls, and a large sphere shows a thick sub-continuous wall with pustules and depressions. These features appear consistent with post-mortem cell alteration, although abiotic morphogenesis remains difficult to rule out. We compared these siliceous and carbonaceous microstructures to coalescent pyritic spheroids from the same sample, which likely formed as "colloidal" structures in hydrothermal context. The pyrites display a smaller size and only limited carbonaceous coatings, arguing that they could not have acted as precursors to siliceous spheroids. This study revealed new textural features arguing for abiotic morphogenesis of some Archean spheroids. The absence of these features in distinct types of spheroids leaves open the microfossil hypothesis in the same rock. Distinction of such characteristics could help addressing further the origin of other candidate microfossils. This study calls for similar investigations of metamorphosed microfossiliferous rocks and of the products of in vitro growth of cell-mimicking structures in presence of organics and silica.

Strong mineralization ability of strontium zinc silicate: Formation of a continuous biomorphic mineralized layer with enhanced osteogenic activity.

Silica gel plays an important role in the formation of some biomorphic minerals (e.g. silica-carbonates) with morphologically complex micro/nanostructures in a pure inorganic system. Herein, we demonstrate the potential of strontium zinc silicate (Sr2ZnSi2O7, SZnS) bioceramics as a biomorphic mineral "garden" due to its incongruent dissolution behavior. Briefly, the preferential release of Sr ions from SZnS leaves behind a silica-rich gel on the ceramic surface and leads to an alkaline pH in the localized area close to the silica-rich gel, providing a growth condition similar to that for the conventional synthesis of biomorphic minerals. Based on this unique characteristic of SZnS, a continuous and integrated carbonated calcium-phosphate mineralized layer was formed on 3D porous SZnS scaffolds with the purpose of enhancing scaffold's bioactivity. The mineralized layer not only provides numerous nanotopographic cues for guiding cell behavior, but also avoids burst ion release, thus overcoming side effects caused by the overdose of bioactive ions and the over-high pH. In vitro cell culture experiments and in vivo animal studies demonstrate that the scaffold with nanostructured mineralized layers promotes osteogenic differentiation of osteoblasts and induce more new bone tissues compared to the non-mineralized scaffold.

A morphogram for silica-witherite biomorphs and its application to microfossil identification in the early earth rock record.

Archean hydrothermal environments formed a likely site for the origin and early evolution of life. These are also the settings, however, were complex abiologic structures can form. Low-temperature serpentinization of ultramafic crust can generate alkaline, silica-saturated fluids in which carbonate-silica crystalline aggregates with life-like morphologies can self-assemble. These "biomorphs" could have adsorbed hydrocarbons from Fischer-Tropsch type synthesis processes, leading to metamorphosed structures that resemble carbonaceous microfossils. Although this abiogenic process has been extensively cited in the literature and has generated important controversy, so far only one specific biomorph type with a filamentous shape has been discussed for the interpretation of Archean microfossils. It is therefore critical to precisely determine the full distribution in morphology and size of these biomorphs, and to study the range of plausible geochemical conditions under which these microstructures can form. Here, a set of witherite-silica biomorph synthesis experiments in silica-saturated solutions is presented, for a range of pH values (from 9 to 11.5) and barium ion concentrations (from 0.6 to 40 mmol/L BaCl2 ). Under these varying conditions, a wide range of life-like structures is found, from fractal dendrites to complex shapes with continuous curvature. The size, spatial concentration, and morphology of the biomorphs are strongly controlled by environmental parameters, among which pH is the most important. This potentially limits the diversity of environments in which the growth of biomorphs could have occurred on Early Earth. Given the variety of the observed biomorph morphologies, our results show that the morphology of an individual microstructure is a poor criterion for biogenicity. However, biomorphs may be distinguished from actual populations of cellular microfossils by their wide, unimodal size distribution. Biomorphs grown by diffusion in silica gel can be differentiated by their continuous gradient in size, spatial density, and morphology along the direction of diffusion.

Biomimetic mineral self-organization from silica-rich spring waters.

Purely inorganic reactions of silica, metal carbonates, and metal hydroxides can produce self-organized complex structures that mimic the texture of biominerals, the morphology of primitive organisms, and that catalyze prebiotic reactions. To date, these fascinating structures have only been synthesized using model solutions. We report that mineral self-assembly can be also obtained from natural alkaline silica-rich water deriving from serpentinization. Specifically, we demonstrate three main types of mineral self-assembly: (i) nanocrystalline biomorphs of barium carbonate and silica, (ii) mesocrystals and crystal aggregates of calcium carbonate with complex biomimetic textures, and (iii) osmosis-driven metal silicate hydrate membranes that form compartmentalized, hollow structures. Our results suggest that silica-induced mineral self-assembly could have been a common phenomenon in alkaline environments of early Earth and Earth-like planets.

Self-organization in precipitation reactions far from the equilibrium.

Far from the thermodynamic equilibrium, many precipitation reactions create complex product structures with fascinating features caused by their unusual origins. Unlike the dissipative patterns in other self-organizing reactions, these features can be permanent, suggesting potential applications in materials science and engineering. We review four distinct classes of precipitation reactions, describe similarities and differences, and discuss related challenges for theoretical studies. These classes are hollow micro- and macrotubes in chemical gardens, polycrystalline silica carbonate aggregates (biomorphs), Liesegang bands, and propagating precipitation-dissolution fronts. In many cases, these systems show intricate structural hierarchies that span from the nanometer scale into the macroscopic world. We summarize recent experimental progress that often involves growth under tightly regulated conditions by means of wet stamping, holographic heating, and controlled electric, magnetic, or pH perturbations. In this research field, progress requires mechanistic insights that cannot be derived from experiments alone. We discuss how mesoscopic aspects of the product structures can be modeled by reaction-transport equations and suggest important targets for future studies that should also include materials features at the nanoscale.

Experimental techniques for the growth and characterization of silica biomorphs and silica gardens.

Silica biomorphs and silica gardens are canonical examples of precipitation phenomena yielding self-assembled nanocrystalline composite materials with outstanding properties in terms of morphology and texture. Both types of structures form spontaneously in alkaline environments and rely on simple, and essentially similar, chemistry. However, the underlying growth processes are very sensitive to a range of experimental parameters, distinct preparation procedures, and external conditions. In this chapter, we report detailed protocols for the synthesis of these extraordinary biomimetic materials and identify critical aspects as well as advantages and disadvantages of different approaches. Furthermore, modifications of established standard procedures are reviewed and discussed with respect to their benefit for the control over morphogenesis and the reproducibility of the experiments in both cases. Finally, we describe currently used techniques for the characterization of these fascinating structures and devise promising ways to analyze their growth behavior and formation mechanisms in situ and as a function of time.