Bioinorganic and bioinspired solid-state chemistry: from classical crystallization to nonclassical synthesis concepts

Mesocrystalline Architecture in Hyaline Foraminifer Shells Indicates a Non‐Classical Crystallisation Pathway

“…The presence of distinct crystals rather than one continuously aligned entity is indicated by randomly oriented a-axes (Figure 5), which suggests that foraminiferal test formation is a discontinuous process, that directs crystallisation into different compartments, possibly by the presence of separating organic sheets (Nagai, Uematsu, Chen, et al, 2018;Nakajima et al, 2016;Tyszka et al, 2019). A strict direction of the crystallographic c-axis perpendicular to the shell surface has also been observed in other biominerals and has been suggested to serve mechanical as well as optical purposes (Gim et al, 2019;Harding et al, 2014;Jacob et al, 2017;Merkel et al, 2009;Sommerdijk & de With, 2008;Towe & Cifelli, 1967;Wolf, 2021;Wolf et al, 2016).…”

“…Lattice distortions are likely introduced to the crystal lattice by occluded organic material, which has been observed for other biominerals and reproduced in experimentally precipitated carbonates (Borukhin et al., 2012; Kim et al., 2011; Kontrec et al., 2004; Lang et al., 2020; Pokroy et al., 2004, 2006; Rae Cho et al., 2016; Seknazi & Pokroy, 2018; Zolotoyabko, 2017). The generation of internal strain and stress due to the presence of impurities seems to be a widespread mechanism in biominerals, as the organism benefits from mechanical advantages such as enhanced toughness and fracture‐resistance (Pokroy et al., 2004; Polishchuk et al., 2017; Seknazi & Pokroy, 2018; Wolf et al., 2016; Wolf, 2021). Our observations indicate that this is the case in some foraminifer species as well, which should be confirmed by systematic high‐resolution synchrotron studies.…”

“…In biominerals as well as in experimental studies, mesocrystallisation has been proposed to be realized via a non‐classical crystal growth mechanism, that is, attachment of nanoparticles to a growing crystal surface, in contrast to classical growth by single ions (Bergström et al., 2015; Cölfen & Antonietti, 2005; De Yoreo et al., 2015; Floquet & Vielzeuf, 2012; Gal et al., 2014; Jehannin et al., 2019; Rao & Cölfen, 2017; Sturm & Cölfen, 2016). These nanoparticles can either be nanocrystals, which attach in an oriented manner (oriented attachment), or metastable (amorphous, colloidal or liquid) phases, which crystallize upon interaction with the mineral surface (Bergström et al., 2015; De Yoreo et al., 2015; Gal et al., 2014; Huang et al., 2018; Rao & Cölfen, 2018; Rodríguez‐Navarro et al., 2016; Seto et al., 2012; Sturm & Cölfen, 2016; Wolf, 2021). The presence of a non‐classical mechanism resulting in a mesocrystal can mean that the final average crystallite domain size does not exceed the size of the attaching unit, which we confirm for hyaline foraminiferal test calcite by XRD methods (crystallite domain sizes range nanometer dimensions, Table 1, Figures 2 and 3; as well as Berman et al., 1993).…”

“…Crystallographic orientation and/or formation of the nanoparticles within the mesocrystals has been suggested to be achieved (a) by epitaxial crystallisation through mineral bridging, (b) with the guidance of a meshwork of organics, (c) by nucleation of ACC within an organic network and in situ crystallisation, (d) by oriented attachment of a previously formed nanocrystal, (e) by interface‐driven nucleation, (f) via a polymer‐induced liquid precursor (PILP), or (g) by accretion and crystallisation of amorphous colloids (Bergström et al., 2015; Cölfen & Antonietti, 2005; De Yoreo et al., 2015; Jehannin et al., 2019; Oaki et al., 2006; Pouget et al., 2009; Rao & Cölfen, 2017; Rao et al., 2019; Rodríguez‐Navarro et al., 2016; Seto et al., 2012; Sommerdijk & de With, 2008; Sturm & Cölfen, 2016; Wolf, 2021; Wolf et al., 2016, 2012; Zhu et al., 2021). Either of these mechanisms may have different implications for the formation of geochemical signals in foraminiferal shell calcite, as they might employ transitional carbonate phases such as ACC and phase transformations to thermodynamically stable calcite, which have the potential to exert control over the evolution of element distributions during test formation (Dietzel et al., 2020; Evans et al., 2020; Mavromatis et al., 2017).…”

“…This is consistent with a spherical and irregular shape of the nanocrystals devoid of crystal facets observed in hyaline foraminiferal calcite (Figure 4), which suggests preservation of the initial nanoparticle dimension upon crystallisation. Further confinement of the nanocrystallite might be provided by the formation of a grain boundary of organic matter and/or inorganic impurities during propagation of a crystallisation front within the nanogranule, as observed or proposed for abiogenic and biogenic calcites in the presence and absence of organic matter (Cölfen & Antonietti, 2005;Huang et al, 2018;Jehannin et al, 2019;Oaki et al, 2006;Rao & Cölfen, 2017;Sommerdijk & de With, 2008;Wolf et al, 2016;Wolf, 2021). A distinct inter-crystallite amorphous phase has been observed at grain boundaries in different hyaline foraminifer species in TEM studies from focused ion beam milled wedges of foraminifer shells (Jacob et al, 2017), which could possibly be a stabilized amorphous carbonate-organic composite material (Seto et al, 2012;Wolf et al, 2012Wolf et al, , 2016.…”