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Although the emergence of complex biomineralized forms has been investigated for over a century, still little is known on how single cells control morphology of skeletal structures, such as frustules, shells, spicules, or scales. We have run experiments on the shell formation in foraminifera, unicellular, mainly marine organisms that can build shells by successive additions of chambers. We used live imaging to discover that all stages of chamber/shell formation are controlled by dedicated actin-driven pseudopodial structures. Successive reorganization of an F-actin meshwork, associated with microtubular structures, is actively involved in formation of protective envelope, followed by dynamic scaffolding of chamber morphology. Then lamellar dynamic templates create a confined space and control mineralization separated from seawater. These observations exclude extracellular calcification assumed in selected foraminiferal clades, and instead suggest a semiintracellular biomineralization pattern known from other unicellular calcifying and silicifying organisms. These results give a challenging prospect to decipher the vital effect on geochemical proxies applied to paleoceanographic reconstructions. They have further implications for understanding multiscale complexity of biomineralization and show a prospect for material science applications., Competing Interests: The authors declare no conflict of interest., (Copyright © 2019 the Author(s). Published by PNAS.)

Living organisms control the formation of mineral skeletons and other structures through biomineralization. Major phylogenetic groups usually consistently follow a single biomineralization pathway. Foraminifera, which are very efficient marine calcifiers, making a substantial contribution to global carbonate production and global carbon sequestration, are regarded as an exception. This phylum has been commonly thought to follow two contrasting models of either in situ ‘mineralization of extracellular matrix’ attributed to hyaline rotaliid shells, or ‘mineralization within intracellular vesicles’ attributed to porcelaneous miliolid shells. Our previous results on rotaliids along with those on miliolids in this paper question such a wide divergence of biomineralization pathways within the same phylum of Foraminifera. We have found under a high-resolution scanning electron microscopy (SEM) that precipitation of high-Mg calcitic mesocrystals in porcelaneous shells takes place in situ and form a dense, chaotic meshwork of needle-like crystallites. We have not observed calcified needles that already precipitated in the transported vesicles, what challenges the previous model of miliolid mineralization. Hence, Foraminifera probably utilize less divergent calcification pathways, following the recently discovered biomineralization principles. Mesocrystalline chamber walls in both models are therefore most likely created by intravesicular accumulation of pre-formed liquid amorphous mineral phase deposited and crystallized within the extracellular organic matrix enclosed in a biologically controlled privileged space by active pseudopodial structures. Both calcification pathways evolved independently in the Paleozoic and are well conserved in two clades that represent different chamber formation modes. [ABSTRACT FROM AUTHOR]

It has long since been noted that minor element (Me) partitioning into biogenic carbonates is sometimes different from Me partitioning into inorganically precipitated carbonates. The prime example is the partitioning coefficient, which might be lower or even higher than the one of inorganically precipitated carbonate. Such a difference is usually termed “vital effect” and is seen as indicative of a biologically modified minor element partitioning. Over the last three decades interest in conceptual biomineralization models compatible with minor element and isotope fractionation has been steadily increasing. However, inferring features of a biomineralization mechanism from Me partitioning is complicated, because not all partitioning coefficients show vital effects in every calcium carbonate producing organism. Moreover, the partitioning coefficient is not the only aspect of Me partitioning. Other aspects include polymorph specificity and rate dependence. Patellogastropod limpets are ideally suited for analysing Me partitioning in terms of biomineralization models, because they feature both aragonitic and calcitic shell parts, so that polymorph specificity can be tested. In this study, polymorph-specific partitioning of the minor elements Mg, Li, B, Sr, and U into shells of the patellogastropod limpet Patella caerulea from within and outside a CO 2 vent site at Ischia (Italy) was investigated by means of LA-ICP-MS. The partitioning coefficients of U, B, Mg, and Sr (in aragonite) differed from the respective inorganic ones, while the partitioning coefficients of Li and Sr (in calcite) fell within the range of published values for inorganically precipitated carbonates. Polymorph specificity of Me partitioning was explicable in terms of inorganic precipitation in the case of Sr and Mg, but not Li and B. Seawater carbon chemistry did not have the effect on B partitioning that was expected on the basis of data on inorganic precipitates and foraminifera. Carbon chemistry did affect Mg (in aragonite) and Li, but only the effect on Mg was explicable in terms of calcification rate. On the one hand, these results show that Me partitioning in P. caerulea is incompatible with a direct precipitation of shell calcium carbonate from the extrapallial fluid. On the other hand, our results are compatible with precipitation from a microenvironment formed by the mantle. Such a microenvironment was proposed based on data other than Me partitioning. This is the first study which systematically employs a multi-element, multi-aspect approach to test the compatibility of Me partitioning with different conceptual biomineralization models. [ABSTRACT FROM AUTHOR]

The shallow water benthic foraminifera Ammonia aomoriensis and Amphistegina lessonii were grown at different seawater Sr/Ca and the test Sr/Ca ratio was determined by Laser Ablation - Inductively Coupled Plasma - Mass Spectrometry. A. aomoriensis test Sr/Ca is positively correlated with seawater Sr/Ca. The linear regression has a slope of 0.17, representing the overall Sr partitioning coefficient K DSr . The slope remains unchanged, if seawater Ca concentration is changed in order to change the seawater Sr/Ca. In the case of A. lessonii , the slopes of the linear regressions representing K DSr differ from one another i.e., 0.16 if the Sr concentration is changed and 0.32 if the Ca level is changed. This difference in K DSr can be explained by the, relative to A. aomoriensis , high Mg content of A. lessonii (ca. 40 mmol/mol), distorting the calcite lattice and weakening the discrimination against Sr. The Mg content of A. aomoriensis is too low (ca. 4 mmol/mol) to observe the influence on Sr partitioning. All data are compatible with a recently developed model for minor element partitioning in foraminifera (Nehrke et al., 2013; Mewes et al., 2015a). On the whole, our data confirm the model (applicability of the model to Sr and dependence of the calcite Sr/Ca on seawater Sr/Ca, as opposed to seawater Sr concentration), and improve our understanding of the model (influence of calcite Mg/Ca on Sr partitioning). [ABSTRACT FROM AUTHOR]

The isotopic ratio and concentration of B in foraminiferal calcite appear to reflect the pH and bicarbonate concentration of seawater. The use of B as a chemical proxy tracer has the potential to transform our understanding of the global carbon cycle, and ocean acidification processes. However, discrepancies between the theory underpinning the B proxies, and mineralogical observations of B coordination in biomineral carbonates call the basis of these proxies into question. Here, we use synchrotron X-ray spectromicroscopy to show that B is hosted solely as trigonal BO 3 in the calcite test of Amphistegina lessonii , and that B concentration exhibits banding at the micron length scale. In contrast to previous results, our observation of trigonal B agrees with the predictions of the theoretical mechanism behind B palaeoproxies. These data strengthen the use of B for producing palaeo-pH records. The observation of systematic B heterogeneity, however, highlights the complexity of foraminiferal biomineralisation, implying that B incorporation is modulated by biological or crystal growth processes. [ABSTRACT FROM AUTHOR]

Magnesium, incorporated in foraminiferal calcite (Mg/Ca CC ), is used intensively to reconstruct past seawater temperatures but, in addition to temperature, the Mg/Ca CC of foraminiferal tests also depends on the ratio of Mg and Ca in seawater (Mg/Ca SW ). The physiological mechanisms responsible for these proxy relationships are still unknown. This culture study investigates the impact of different seawater [Mg 2 + ] on calcification in two benthic foraminiferal species precipitating contrasting Mg/Ca CC : Ammonia aomoriensis , producing low-Mg calcite and Amphistegina lessonii , producing intermediate-Mg calcite. Foraminiferal growth and test thickness were determined and, Mg/Ca was analyzed using Laser Ablation-Inductively Coupled Plasma-Mass Spectrometry (LA-ICP-MS). Results show that at present-day seawater Mg/Ca SW of ~ 5, both species have highest growth rates, reflecting their adaptation to modern seawater element concentrations. Test thickness is not significantly affected by different Mg/Ca SW . The relationship between Mg/Ca SW and Mg/Ca CC shows a distinct positive y-axis intercept, possibly reflecting at least two processes involved in foraminiferal biomineralization. The associated Mg partition (D Mg ) changes non-linearly with increasing Mg/Ca SW , hence suggesting that the D Mg is best described by an exponential function approaching an asymptote. [ABSTRACT FROM AUTHOR]