Calcium Carbonate Biomineralisation: Insights from Trace Elements

 1811-5209/25/0021-0105$2.50 DOI: 10.2138/gselements.21.2.105

Keywords: trace element; biomineralisation; calcification; calcite; aragonite; biomineral; calcium carbonate; foraminifera; coccolithophore; coral

INTRODUCTION

Numerous marine organisms produce skeletons or shells made of the calcium carbonate (CaCO3) minerals calcite and aragonite. In the open ocean, CaCO3 production is dominated by microscopic coccolithophores, foraminifera, and pteropods. Near the shore, communities of corals, mollusks, algae, echinoderms, foraminifera, brachiopods, and microbes produce massive CaCO3 structures that are a critical component of coastal morphology and ecosystems. Together, these organisms play an important role in the global cycling of carbon and impact alkalinity, which is a major determinant of atmospheric CO2 over long (i.e., geological) timescales (Ridgwell and Zeebe 2005).

The response of marine calcification to anthropogenic climate change, particularly ocean acidification, will have a major impact on future marine carbon cycling, which is central to both the trajectory of global climate change (Ridgwell and Zeebe 2005) and the efficacy of ocean based carbon dioxide removal technologies (Renforth and Henderson 2017). Despite the importance of calcification, we are not currently able to predict patterns of calcium carbonate production in the ocean. For example, basic chemistry tells us that ocean acidification driven by increased atmospheric partial pressure of CO2 (pCO2) will reduce the concentration of CO32−, reducing the CaCO3 saturation state (Ωc), potentially making it harder for organisms to calcify. However, studies of the response of biomineralising organisms to simulated ocean acidification do not always confirm this—some taxa appear to calcify less under ocean acidification, while others appear to calcify more (e.g., Leung et al. 2022). The cause of these counter-intuitive patterns lies in the mechanisms of biomineralisation: the cellular and physiological processes combining dissolved calcium and inorganic carbon to form crystalline CaCO3. We do not currently possess a complete mechanistic understanding of biomineralisation, yet under standing these mechanisms has never been more urgent.

The delicate, transitory nature of cellular biomineralisation mechanisms makes marine calcifying organisms challenging subjects. Intensive study of these processes in a few model organisms has yielded valuable insights into the ‘machinery’ of biomineralisation. For example, coccolithophores have been shown to actively transport Ca2+ across cellular membranes for calcification (Brownlee and Taylor 2004). In contrast, some corals have been shown to use seawater as a major source of ions for calcification (Gagnon et al. 2012). However, it is non-trivial to scale up such findings to predict global calcification patterns, which are determined by the response of diverse marine calcifiers with a wide gamut of biomineralisation mechanisms. Fortunately, the mechanisms of biomineralisation are also recorded in the trace element (TE) content of skeletal material, where each impurity incorporated into the mineral is affected in distinct ways by the processes of biomineralisation. The concentrations of TEs in biominerals therefore provide an indirect way to study biomineralisation mechanisms and thus address this issue.

TRACE ELEMENTS IN BIOMINERALS

The TE composition of carbonate biominerals has been intensely studied for the last century. This interest was fuelled by early observations that TE concentrations within biomineral carbonates commonly correlate with the environmental conditions at the time of their formation (see Lea 2014 for a consideration of temperature). The promise of using biomineral TEs as proxy recorders of past environmental conditions drove intense study into the systematics of numerous TEs in biominerals, both in controlled laboratory conditions to ‘calibrate’ proxies (e.g., Lea 2003), and in sedimentary settings to construct palaeo environmental records that together have transformed our understanding of Earth’s climate (e.g., Elderfield and Ganssen 2000).

Since the inception of these TE-based palaeoproxies, it was recognised that the concentrations of TEs in biominerals deviate from those in the same minerals grown synthetically from seawater in the laboratory (Fig. 1). These differences are driven by biological and mineralogical processes, collectively referred to as ‘vital effects’ (Erez 2003).

Historically, vital effects have been treated as a complication that must be accounted for when reconstructing palaeoenvironmental conditions. However, over the last few decades, an increasing body of research has sought to use the characteristic patterns of TE incorporation into biominerals as a tool to examine the underlying mechanisms of biomineralisation (e.g., Elderfield et al. 1996; Erez 2003; Gagnon et al. 2012; Evans et al. 2018; reviewed by Branson et al. 2024). With knowledge of the hypothesised biological, mineralogical, and dynamical processes that might affect TE incorporation, these studies seek to interpret differences between the TE content of biominerals and inorganic calcium carbonates to infer the mechanisms used by a biomineralising organism. For example, the much lower Mg/Ca of most foraminiferal calcite compared with inorganically grown CaCO3 indicated a biological mechanism that reduces Mg2+ incorporated within the mineral (Zeebe and Sanyal 2002), long before such mechanisms were directly investigated (e.g., Ujiié et al. 2023). Another example is the effect of crystal growth rate (or precipitation rate) on abiogenic TE/Ca, which can be a key mechanism that facilitates the environmental influence on biogenic element partitioning (see Stoll et al. 2002 for an evaluation of Sr/Ca in coccolithophores). These approaches offer an invaluable, indirect means of probing the mechanisms of biomineralisation that evade in-vivo measurement techniques.

With this in mind, we introduce the key biological, mineralogical, and dynamical processes that may be important in biomineralisation and consider the impacts that these processes have on TE incorporation. We then offer an overview of patterns in biomineral TE content and highlight the key differences in biomineralisation processes that these patterns imply.

Describing Trace Element Incorporation: KTE vs. DTE

Before examining patterns in TE incorporation, it is important to consider how TE concentrations are described in solids. In the simplest case, we can consider a TE that exists in a solid solution with the host mineral:

CaCO3 + TE2+ ⇌ TECO3 + Ca2+

The concentration of TE in the solid will depend upon its concentration in the fluid relative to the ion that it is replacing (Ca2+ in this case), and the compatibility of the impurity within the solid structure, which is described by the partition coefficient, KTE, for that TE:

KTE = (TE/Ca)solid / (TE/Ca)fluid

The partition coefficient allows us to remove the effect of solution composition when considering TE incorporation, revealing the impact of the mineral growth processes on TE incorporation (KTE resembles an equilibrium constant familiar from chemical thermodynamics, but various processes can cause it to adopt non-equilibrium values). However, it cannot be directly applied to all TEs because it requires that the TE exists as a solid solution with a host ion, which is not necessarily the case. This is particularly relevant to biominerals where TEs may be incorporated in the solid in non-ideal ways (e.g., in association with organics; Branson et al. 2016), and the composition of the fluid from which a biomineral grows is unknown, which precludes the calculation of KTE.

Instead, the incorporation of non-solid-solution TEs in inorganic precipitates, and all TEs in biominerals, is commonly expressed as a distribution coefficient, DTE:

DTE = (TE/X)solid/(TE/X)environment

where X is the concentration of an abundant reference element in both the host mineral and the environment that the impurity does not necessarily substitute for and/ or compete with during incorporation. This quantity is conceptually similar to KTE, in that DTE > 1 indicates an enrichment in the solid phase (i.e., calcium carbonate) compared to the fluid, and DTE < 1 indicates a depletion.

However, DTE is crucially different from KTE in two key respects. First, by normalising the mineral composition to some composition of the environment (i.e., of ambient seawater rather than of the marine organism’s biomineralising fluid), this acknowledges that the composition of the fluid of mineral precipitation may not be known, and it implicitly includes all the biological processes that might cause the mineralizing fluid’s composition to deviate from seawater. Second, the use of DTE does not imply a specific substitution mechanism within the mineral, so the choice of the denominator in the fluid is therefore not dictated by the substitution mechanism inferred from inorganic precipitation processes and can be adapted to accommodate competition of TE with different solute ions. In inorganic minerals, KTE may be appropriate for some TEs, and DTE may be more appropriate for others. However, for the rest of this chapter, we use KTE when discussing the composition of inorganic precipitates relative to the solution from which they formed, and DTE when considering the composition of the biomineral relative to seawater (Fig. 2). Differences between inorganic KTE and biomineral DTE, when calculated with the same elements in the numerator and denominator, are driven by the mechanisms of biomineralisation and can, therefore be interpreted to infer those mechanisms.

WHAT CONTROLS TRACE ELEMENT INCORPORATION IN BIOMINERALS?

The observed DTE of a biomineral is the result of a combination of inorganic crystal growth processes governing the formation of the mineral at the site of calcification, and biological processes that separate the site of calcification from seawater and modify its chemical composition (Fig. 2). To understand how these mechanisms fit together, it is first necessary to consider this ‘inorganic’ side of the equation— how does KTE depend on crystal growth processes?

Changing KTE: Mineralogical Effects

The KTE of an inorganically formed mineral depends primarily on the chemistry of the element being incorporated and its compatibility with the host mineral phase (e.g., Mucci and Morse 1983). However, it is important to note that KTE is not necessarily constant for a given TE in a single mineral phase: it can also be affected by the solution’s ionic composition (e.g., Uchikawa et al. 2017), and the mineral’s precipitation rate (DePaolo 2011) and growth mechanism (Evans et al. 2020). All of these inorganic processes can therefore affect the DTE of a biomineral, without the intervention of any biological mechanisms.

Precipitation Rate. At slow precipitation rates, a growing mineral can be close to compositional equilibrium with the fluid, where KTE for different impurities are primarily determined by each impurity’s influence on the thermodynamics of the solid phase (DePaolo 2011). At faster precipitation rates, the kinetics of the attachment and detachment of impurities from the solution are increasingly influential and affect KTE values (Fig. 3A; DePaolo 2011). For some TEs, KTE increases with precipitation rate (e.g., Sr in calcite, and Mg in both calcite and aragonite; AlKhatib and Eisenhauer 2017), while for others, it can decrease (e.g., Sr in aragonite; Brazier et al. 2023). The sensitivity of KTE to precipitation rate has been experimentally determined for multiple TEs in both calcite and aragonite (see Branson et al. 2024), and a key observation is that differences in inorganic precipitation rates produce relatively predict able patterns across a suite of trace elements. A change in precipitation rate therefore simultaneously impacts the KTE of multiple trace elements in distinct ways. For example, a change in calcite precipitation rate from 10−8 to 10−6 mol/m2/s increases KSr from ~0.04 to ~0.07, while it decreases KMn from approximately 20 to <10 under otherwise identical circumstances (DePaolo 2011).

Intermediate Phases/Non-Classical Growth. Most studies of inorganic precipitation have focused on crystals growing via ‘classical’ mechanisms, where a crystal grows by individual ions attaching to the growing crystal faces. However, at relatively high saturation states, calcification can proceed via non-classical pathways involving precipitation of amorphous calcium carbonate (ACC) phases that then transform to produce the final crystalline structure (De Yoreo et al. 2015). These metastable ACC phases have been observed in multiple groups of major marine calcifiers (see Jantschke and Scholz 2025 this issue) and the involvement of these phases is consistent with the fine-scale microstructure of numerous biominerals, and the rapid precipitation rates observed during calcification (Gilbert et al. 2022; Branson et al. 2024).

It is increasingly likely that many, if not the majority of, marine calcifying organisms precipitate CaCO3 via non-classical growth mechanisms. The formation and transformation of ACC is likely to have a significant effect on the DTE of the biomineral. Indeed, it has been suggested that ACC is a key determinant of biomineral DTE (Ulrich et al. 2021). However, we note that there is considerable uncertainty surrounding the impact of ACC on DTE. In particular, ACC can form and transform via a range of mechanisms, each of which distinctly influences the TEs incorporated into the final mineral, and it is not currently clear which mechanisms dominate for seawater-like solutions, and therefore for natural biomineralisation (Evans et al. 2020). The implications of ACC for biomineral composition is a rapidly developing frontier in scientific understanding, and we direct the reader elsewhere for a more complete discussion of this complex topic (e.g., Branson et al. 2024).

Changing DTE: Solution Composition and Transport Dynamics

On the more biological side of biomineralisation, a suite of processes can cause the composition of the fluid in the calcifying space to deviate from the surrounding seawater. Essentially, these are the processes of ion ‘supply’ and fuel the ‘demand’ of crystal growth at the site of calcification— these encompass all the biological mechanisms that import the ingredients for calcification (mainly Ca2+ and inorganic carbon; Fig. 2).

Ion Transport for Calcification: Seawater vs. Specific Transport. There is strong evidence that seawater is the ‘starting point’ for calcification in many, but not all, marine calcifiers. The primary evidence for this is the incorporation of both membrane-impermeable dyes (e.g., calcein in corals, Venn et al. 2020; and foraminifera, de Nooijer et al. 2014) and rare earth elements with no known biological function (e.g., Tb in corals; Gagnon et al. 2012). The only route for these impurities to reach the site of calcification is via direct transport of seawater. This is not the case in coccolithophores, which calcify in an intracellular space that is completely separated from seawater by biological membranes (Brownlee and Taylor 2004). This range of biomineralisation architecture highlights two end-member mechanisms that might supply ions for biomineralisation: seawater transport, or the movement of specific ions across biological membranes (Fig. 2).

The extent to which seawater directly supplies ions for calcification remains an open question. However, if this is the only source of ions for calcification, we would expect the DTE of the biomineral to exactly match the KTE for the equivalent phase grown in seawater (provided the denominator for calculating DTE and KTE is the same). The sole involvement of unmodified seawater is unlikely, because the presence of other ions (e.g., Mg2+; Davis et al. 2000) and organic molecules (e.g., Kladi et al. 2002) in seawater inhibit the formation of CaCO3 (see Stolarski et al. 2025 this issue). It is therefore commonly proposed that seawater may be the starting point for biomineralisation, but it is substantially modified by trans-membrane transport of specific ions before calcification can occur (e.g., Zeebe and Sanyal 2002).

Transmembrane ion transport could supply Ca2+ or inorganic carbon (e.g., HCO3−) to enrich the site of calcification (e.g., Sevilgen et al. 2019), actively remove H+ to elevate internal pH and promote calcification (e.g., de Nooijer et al. 2014), or even to directly remove inhibitory ions from the site of calcification (Zeebe and Sanyal 2002; Erez 2003). In each case, the transport of a specific ion to or from the site of calcification would change the chemistry of the calcifying space from that of external seawater and thus strongly influence the DTE of the biomineral. For example, actively pumping in Ca2+ would reduce the TE/Ca of the calcifying fluid, and therefore reduce DTE (Fig. 3D; relative to the KTE of a mineral forming directly from seawater).

An additional layer of complexity arises from the imperfec tion of specific ion transport mechanisms. No biological transporter can perfectly discriminate against other ions that are chemically similar to their target ion. For example, voltage-gated Ca2+ channels, which allow Ca2+ to move across membranes down concentration or charge gradients, also transport other ions with the approximate specificity Ca2+ > Sr2+ > Ba2+ >>> Mg2+ (Hess et al. 1986). If all Ca2+ for calcification is supplied by these channels, we would expect the DTE of the biomineral to be entirely set by the specificity of the transporter (Fig. 3B). On the ‘export’ side of the equation, Na+/H+ exchangers, which are commonly proposed to be involved in removing H+ to promote calcification, are ‘leaky’ to Li+ (Poet et al. 2023). The action of this proton pump in biomineralisation would also specifically modify the concentration of Li in the calcifying space, and therefore DLi. Thus, the actions of specific ion transporters modify the DTE of specific subsets of trace elements.

Transport Dynamics: Steady-State and Rayleigh Fractionation. So far, we have considered the supply of ions for biomineralisation, but the ‘demand’ side of the process is just as important. Relative rates of ion supply and removal by precipitation can drive dynamic behaviour, modifying the DTE of biominerals by changing the composition of the calcifying fluid. The two end-member cases here are steady-state transport in a small reservoir, where the composition of the biomineral will match the composition of the imported ions regardless of mineral KTE (Fig. 3B), and Rayleigh fractionation (i.e., the continuous removal of ions in a proportion that differs from the proportion of those ions in the solution) from a large reservoir, which causes the TE/Ca ratio of the calcifying fluid to evolve in distinct ways depending on the KTE of each trace element (Fig. 3C).

In the case of steady-state transport, the chemistry at the site of calcification will diverge significantly from seawater (as a function of the KTE of each element), until the removal of impurities by calcification matches their replacement by ion transport (Fig. 3B). In this case, the composition of the biomineral will purely depend on transport processes supplying the ions. This can lead to substantial divergences in the chemistry at the site of calcification, which is not evident in the DTE of the biomineral. This scenario is likely to arise in organisms with relatively high and well-matched rates of ion supply and consumption for calcification (i.e.. fast turnover) in a small calcifying space, such as a coccolith vesicle (Fig. 2).

Alternatively, if the calcifying space is larger and/or ion supply does not keep up with removal by precipitation, the composition of both the calcifying space and the DTE of the biomineral can deviate following the principles of Rayleigh fractionation (Fig. 3C; Elderfield et al. 1996). In this case, a fluid reservoir with some starting composition (e.g., seawater) is progressively modified by the removal of both Ca2+ and TE by calcification. The evolution of fluid composition is determined by the KTE for each element. If KTE < 1, the TE will be concentrated in the fluid, gradually increasing the TE/Ca of the remaining reservoir, and vice versa. As Ca2+ depletion continues, this shift in fluid composition causes the DTE of the biomineral to diverge from the inorganic KTE (Fig. 3C).

Tracers of Biomineralisation

Equipped with an understanding of the key processes that cause the DTE of a biomineral to deviate from the KTE of an inorganic precipitate, we can interpret systematic differences in the composition of key calcifying taxa (Fig. 1) to infer which mechanisms may be important in their biomineralisation. We approach this by comparing the DTE observed in each taxa to the inorganic KTE (calculated using Ca as the denominator for both; Fig. 4). If an organism does not control the composition of the calcifying fluid in any way (i.e., calcifies directly from seawater), the DTE for all elements should equal that of inorganically precipitated CaCO3, i.e., DTE/KTE = 1 for all elements. Each of the processes outlined will cause specific elements, or groups of elements, to deviate from this DTE/KTE = 1 line in characteristic, predictable ways.

For example, in a calcifying space connected to seawater, the addition of Ca2+ would act to reduce TE/Ca in that space, and therefore DTE, for all TEs simultaneously (Fig. 3D). Alternatively, if that space is transport-limited and under goes some degree of Rayleigh fractionation, DTE would be elevated for elements where KTE < 1, and lowered where KTE > 1 (Fig. 3C). This effect would be accentuated as Rayleigh fractionation becomes more extensive. A combination of both these processes would produce the characteristic Rayleigh pattern as a function of KTE but offset below the DTE/KTE = 1 line.

Other processes might modify the DTE of only single, or subsets of TEs. For example, the specific removal of Mg from the site of calcification, as has been proposed for foraminifera, might only reduce the concentration of Mg in the calcifying fluid, thus causing dramatic changes in DMg with only minor associated modifications in the D of other elements, driven by the influence of Mg on crystal precipitation and KTE. Alternatively, elements like Li may be specifically enriched by incidental transport alongside HCO3-, which would increase only DLi, or Na could be increased if a Na+/H+ exchanger is responsible for removing H+ during calcification. Finally, in cases where the site of calcification has no exchange with seawater, we would expect the DTE to be entirely set by the fractionation during ion transport. In the case of Ca2+ channels, we would expect a strong depletion of Mg2+ and a lesser depletion of Sr2+ and Ba2+ due to differences in the transport-specificity of ions other than Ca2+ (Hess et al. 1986). However, compositions of coccolith calcite, which is formed in a closed, transport-limited environment supplied by Ca channels (Fig. 3B), are not consistent with this. Coccolith calcite has elevated DSr and DBa, implying that the Ca channels used by these organisms may preferentially take up Sr and Ba over Ca. It is worth noting that the specificity of Ca channels was measured by Hess et al. (1986) in human heart cells, and relatively little is known about Ca channels in marine organisms.

The DTE of each element can be modified by multiple processes, so it is impossible to determine which mechanism is active by looking at a single element in isolation. However, because the influence of each process on each element is distinct, we can gain insights into biomineralisation processes by considering multiple elements simultaneously (Fig. 4). For example, most trace elements in foraminifera exhibit consistently high DTE/KTE > 1, except for DMg/KMg, which is <<1. This could be interpreted as consistent with Rayleigh fractionation from a seawater like fluid where Mg has been specifically removed (e.g., to reduce its inhibitory influence on calcite formation).

Differences in DTE/KTE patterns between calcifying taxa reflect the variability in the importance of the different biomineralisation processes in these groups. Coccolithophores exhibit the lowest D/K for Mg of any group, while their D/K for Sr and Ba are elevated, which is consistent with the known specificity of the Ca channels they are thought to employ. In corals, the DTE of all elements is consistent with the precipitation of aragonite directly from seawater, implying a much stronger role of seawater transport in coral biomineralisation. Alternatively, this pattern could be produced by a combination of Rayleigh fractionation from a Ca-enriched seawater, which is more consistent with observation of a minor/modest Ca2+ elevation at the site of calcification in corals (e.g., Sevilgen et al. 2019). Other groups may similarly be interpreted as being produced by different combinations of the component processes of biomineralisation.

CONCLUDING REMARKS

The patterns described above hint at different characteristic pathways in these taxa, but these patterns are necessarily coarse and are presented here to illustrate the potential power of biomineral composition as a tool for exploring biomineralisation pathways. As presented in Fig. 4, shaded boxes represent the full range of observed compositions in biomineral and inorganic experiments. Variability in KTE arises from changes in physical and chemical conditions and precipitation rate, adding substantial uncertainties to this analysis. Variation within DTE is driven by responses of biomineralisation processes to the physical and chemical environment, and likely represents important differences in biomineralisation strategy within groups. More detailed analyses accounting for these factors can provide important insights into the nature and variability of biomineralisation mechanisms between and within groups.

Clues from Environmental Variability. Finally, it is important to note that both the processes of crystal precipitation and biological ion transport are all sensitive to changes in the physical and chemical environment. This drives changes in both KTE and DTE with environmental conditions, which form the basis of palaeo-environmental proxies (e.g., the sensitivity of Mg/Ca to temperature in inorganic and biomineral calcite). Fine differences in the sensitivity of KTE and DTE to environmental factors can provide a wealth of information to further diagnose the processes of biomineralisation, which is the current cutting-edge of this field.

ACKNOWLEDGMENTS

We would like to thank the editors for the opportunity to write this article, and two anonymous reviewers who helped us improve our manuscript. OB would like to acknowledge support from the Leverhulme Trust (RL-2022-005).

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