Abstract
The rise of calcifying nannoplankton in the Late Triassic (237–201 Ma) had profound consequences for the carbonate buffering capacity of the ocean. Research on the appearance of calcification typically focuses on the reasons that made this process successful on a global scale. The underlying environmental and physiological conditions that led to its appearance, therefore, are still obscure. Here we show that the rise of intracellular calcification is intrinsically linked to cellular calcium metabolism and to the prevention of calcium accumulation in the cytoplasm. Using gene tree analysis, we present evidence that the physiological machinery for calcification was already present in non-calcifying ancestor cells. Additionally, by modelling the energy demands for calcium transport in calcifying and non-calcifying cells, we demonstrate that intracellular calcification does not require additional energy investments. Since all eukaryotic cells export calcium across the plasma membrane, our findings indicate that the onset of intracellular calcification in Earth’s history required only the activation of calcium transport proteins during their passage to the plasma membrane. Hence, intracellular calcification could have occurred at any time in the geological past because physiological preconditions were already present, but a combination of favourable environmental factors may have helped calcifying nannoplankton to spread at the beginning of the Mesozoic, a time of catastrophic climate changes and mass extinctions that reshuffled life on Earth.
1 Introduction
Pelagic nannoplankton calcifiers appeared in the Late Triassic (; ; ; Onoue and Yoshida, 2010; ; Preto et al., 2013b; a), Figure 1. The first were probably small calcareous dinoflagellates that produced simple calcispheres (on average about 10 μm in diameter) composed of sub-micron scale calcium carbonate crystals, which appeared during the Carnian, about 233 Ma, when modern marine fauna was rising in the aftermath of the most catastrophic mass extinction event of the entire Phanerozoic Eon at the Permian-Triassic boundary (; Onoue and Yoshida, 2010; Preto et al., 2013b; Preto et al., 2013a; ), Figure 1. Coccolithophores, which are haptophyte algae and secrete complex ornamented calcite plates (Young, 2003; Young et al., 2005), appeared in the middle-late Norian, about 215–210 Ma (; ), and spread after the Triassic-Jurassic mass extinction event (e.g.,: ), Figure 1. Before the emergence of pelagic nannoplankton calcification, the biological precipitation of calcium carbonate was dominated by metazoans and microbial mats that calcified extracellularly in a medium isolated from seawater (Lowenstam and Margulis, 1980; ; Knoll, 2003). In contrast, calcareous nannoplankton, such as calcareous dinoflagellates (calcispheres) and coccolithophores, calcify inside intracellular compartments called vesicles and extrude the accreted crystals via exocytosis (; Paasche, 2002; ; ). The emergence of intracellular calcification allowed biocalcification to expand into the surface waters of the open ocean, marking the transition from the so-called “Neritan” ocean to the “Cretan” ocean (Zeebe and Westbroek, 2003; Ridgwell, 2005; ), Figure 1. This expansion produced a much more efficient regulation of the global carbon cycle and changed the marine calcium carbonate saturation state, transforming the entire ocean carbonate chemistry (Zeebe and Westbroek, 2003; Ridgwell, 2005; Ridgwell and Zeebe, 2005). The production of intracellular platelets that are then extruded onto the outer cell surface led to a completely new phenotype with respect to non-calcifying nannoplankton. The emergence of pelagic calcareous nannoplankton is, thus, one of the most important evolutionary innovations in Earth’s history but how and why it originated is still unclear. The mechanisms driving evolutionary innovations are mutation and selection. Therefore, before identifying the benefits that could have selected intracellular calcification to make it a successful innovation at a global scale, it is important to understand the physiological characteristics (or mutations) required for its emergence.
FIGURE 1
While the evolution of extracellular calcification was likely an adaptive response to rising calcium concentrations in the ocean (; ), the appearance of intracellular calcification does not clearly correlate with changes in ocean chemistry (Figure 1). For example, a temporal coincidence between a Late Triassic drastic drop in atmospheric pCO2, resulting from global carbon-climate numerical modelling, and the primary radiation of calcareous nannoplankton, inferred from the fossil record, has been observed but a cause-and-effect link between the two events could not be proven ().
Moreover, when intracellular calcification emerged, the concentration of calcium in the ocean was approximately 30 mM, dissolved inorganic carbon (DIC) was 5,000 μM, and ocean pH was about 7.8 (Figure 1). These conditions would have led to a carbonate concentration of 160 μM and a calcite saturation state of 10. Although such chemical conditions would be favourable to calcification and could therefore positively select for this innovation, they alone are not sufficient to explain the appearance of intracellular calcification because the ocean experienced similar conditions 80–100 million years before the first evidence of pelagic nannoplankton calcification appears in the geological record (Late Triassic-Jurassic). The ocean experienced even higher calcium concentrations (from 50 to almost 60 mM) from the Cambrian to the Carboniferous and calcite saturation reached almost 15 in the Carboniferous and Permian. Therefore, it is plausible to assume that the emergence of intracellular calcification was most likely a consequence of random changes in cellular physiology rather than a response to external environmental factors such as changes in ocean carbonate chemistry. Using new energy budget calculations and gene analyses, we investigate here the underlying mechanisms and prerequisites that allowed intracellular calcification to appear. More explicitly, we investigate if the proteins and ion transporters involved in intracellular calcification were present in non-calcifying ancestors or appeared coincidentally with the emergence of intracellular calcification. Furthermore, we explore if intracellular calcification is indeed energetically costly as proposed by Monteiro et al. (2016) so that secondary evolutionary benefits must compensate for the energy invested into calcification. This is done by calculating the amounts of energy required to pump calcium ions into the calcifying vesicles in comparison to maintaining calcium homeostasis in all (calcifying and non-calcifying) cells.
2 Materials and methods
2.1 Analysis of environmental data
We calculated the carbonate chemistry parameters from reconstructed historic ocean pH and DIC (Ridgwell, 2005) using the standard software CO2sys, version 1.01 (Lewis and Wallace, 1998). Calculated ocean carbonate concentrations and reconstructed calcium concentrations (Stanley and Hardie, 1998) were used to determine the calcite saturation state. Atmospheric pCO2 was obtained from previous reconstructions (). We compared the carbonate chemistry parameters with the fossil record of pelagic calcifying nannoplankton () to identify the environmental conditions under which intracellular calcification emerged (Figure 1). The primary objective of this analysis is to compare, in qualitative terms, the reconstructed carbonate chemistry of the ocean with the appearance of calcareous nannoplankton. A precise, quantitative reconstruction of the carbonate chemistry throughout the Phanerozoic goes beyond the scope of our study. However, from a visual inspection, the data we compiled using literature sources and CO2sys are consistent with recent reconstructions (Witkowski et al., 2018; Montañez et al., 2016).
2.2 Calcium-transporter gene tree analysis
To examine the evolutionary history of calcification-related proteins, we identified proteins across lineages and created gene trees of relevant protein families. We downloaded protein databases from the National Center for Biotechnology Information (NCBI) genome browser for taxa represented in the phylogeny of Read et al. (2013), Supplementary Table S1. To account for differences in annotation completeness in each protein database, we used BLAST to identify homologs of Gephyrocapsa huxleyi proteins in each taxon. We searched the G. huxleyi protein database for annotated sequences in each protein family implicated in calcification () to use as query sequences (Supplementary Table S2). We then used pBLAST to identify all sequences in the protein database that matched these query sequences with probabilities less than e-6. After discarding duplicates, we aligned the BLAST results for each protein family in Geneious 11.1.3, (Kearse et al., 2012), http://www.geneious.com, using the Geneious global alignment with cost matrix Blosum62, gap open penalty 12, and gap extension penalty 3. We created gene trees using Jukes-Cantor genetic distance module and the UPGMA tree building method in Geneious. We then inspected trees for phylogenetic representation and patterns of protein family expansion. Because the BLAST output results for calcium channels included both cation channels and calmodulin, we split these sequences into two subtrees for better visualization of the relationships among calmodulin-related proteins. Supplementary Figures S1 – S7 show the resulting gene trees.
2.3 Calculation of energy invested into intracellular calcification
We calculated the energy required for calcium transport into Golgi-derived vesicles as part of the energy invested to maintain calcium homeostasis. In our calculations, we neglect the costs associated to the transport of golgi vesicles because these vesicles are transported by both calcifying and non-calcifying cells. We also neglect the costs required for the production of polysaccharides and for exocytosis, the process for the secretion of polysaccharides by haptophytes, because also these costs are inccurred by non-calcifying cells and, thus, do not constitute and additional energy requirement for calcifying cells. In order to achieve intracellular calcium homeostasis, total calcium transport out of the cytoplasm has to equal the passive influx via calcium channels. The passive, diffusive uptake via the calcium channels is driven by the difference between the calcium concentration at the cell surface (Casurf) and the calcium concentration in the cytoplasm (Cacyt). Thus, knowing the calcium gradient across the plasma membrane, the energy required to achieve calcium homeostasis (EATP) can be calculated by
where PCa is the apparent membrane permeability per cell surface area (Acell) and is the amount of ATP required per calcium ion transported. The consumption of one ATP molecule for transporting two calcium ions through the membrane is a functional property of the reaction loop of the Ca-ATPase (Toyoshima and Inesi, 2004; Winther et al., 2013) and is independent if transport is over the vesicle or plasma membrane. Without net calcium influx into the cell, Casurf is equal to the calcium concentration in the bulk medium (Caout). However, fluxes of calcium into intracellular compartments, such as vesicles, create a concentration gradient across the cell membrane with Casurf < Caout. With the total flux of calcium into the vesicles (Qvesicle), and thus into the cell, the integration of the spherical diffusion equation in the cell environment gives the following concentration at the cell surface:
where DCa is the diffusion coefficient of calcium in seawater and rcell is the cell radius. Here, we assume that the transport of calcium into vesicles represents a fixed fraction of total calcium transport (fv) as compared to the transport over the plasma membrane (1 − fv), i.e.,:
In other words, we assume that while calcium is rushing in through the ion channels, ATPases pump calcium back through the cell membrane into the extracellular medium but at the same time also into the vesicles. The volume inside the vesicle, however, can be regarded as outside of the cytoplasm from a thermodynamical point of view. In order to maintain calcium homeostasis, the flux into the cytoplasm has to be balanced by the fluxes out of the cytoplasm. Inserting the expression for Qvesicle into Eq. 2 and subtracting Cacyt from both sides of Eq. 2 results in an implicit equation for the concentration difference Casurf - Cacyt, which has the solution:
Replacing in Eq. 1 the concentration difference Casurf − Cacyt with Eq. 4 gives EATP as a function of the relative fraction of calcium transport into the calcifying vesicles:
This equation shows that the higher fv, the lower the absolute requirements for cellular energy. In order to quantify how much the cellular energy consumption can potentially be reduced by intracellular calcification, we calculate the energy requirements to maintain calcium homeostasis as a function of fv from 0 (non-calcifying cell) to 1 (Supplementary Figure S8). The coccolithophore Gephyrocapsa huxleyi produces approximately 1 coccolith per hour (Paasche, 1962) and one coccolith contains around 22 fmol of CaCO3 (Young and Ziveri, 2000). This results in a calcification flux (Qvesicle) of about 6.11 ⋅ 10–18 mol s−1 (see: ). Since the permeability of the plasma membrane for calcium ions is not known in coccolithophores, we estimate a permeability that is based on the conductance of calcium channels (Lux and Nagy, 1981) and measured densities of calcium channels in cell membranes of snail axons (Krishtal et al., 1981; Tsien, 1983). All the parameter values used to calculate the extra energy required by intracellular calcification are reported in Supplementary Table S3. We provide the numerical code for calculating the energy required to maintain calcium homeostasis by single-celled calcifying nannoplankton as open-source software (https://github.com/systemsecologygroup/Calcisphere) so that it can be used, modified, and redistributed freely.
2.4 Calculation of intracellular calcium poisoning
The energy for the Ca2+ pumping ATPase is provided by the hydrolysis of ATP at a high ATP/ADPxPi ratio in the cytosol with a free energy gain, ΔG, of 15 kcal/mol (Meldolesi and Pozzan, 1998). Cooperative binding of 2 Ca2+ per ATPase implies a Ca2+/ATP coupling ratio of 2 (). We assume an electroneutral Ca2+/2H+ co-transport for the Ca2+ pump and a physiological pH at both sides of the Ca2+ pump. If all of the free energy available from ATP hydrolysis is stored in the concentration gradient of Ca2+ between the cytosol and its environment, i.e.,: ΔG = 2RT ⋅ ln (Casurf/Cacyt), the calcium gradient can be up to 105. If the Ca-ATPases work near this thermodynamic limit, the cytosolic Ca2+ concentration of 0.1 μmol L−1 and the gradient of 105 yields a Ca2+ concentration of 10 mM at the cell surface, which is, in fact, exactly the Ca2+ concentration in today’s ocean (Langer et al., 2006). Ca2+ transport near the thermodynamic limit would have the advantages that: 1) pumping Ca2+ from the cytosol to the environment proceeds with a minimum dissipation of energy in ATP consumption, and 2) a steep Ca2+ gradient provides fast influx in cell signaling. We therefore postulate that a constant Ca2+-gradient close to the thermodynamic limit represents a part of calcium homeostasis. Moreover, the Ca2+-gradient across the plasma membrane should be quite independent of the bulk Ca2+ concentration in seawater.
Assuming that the Ca2+-gradient across the plasma membrane is maintained at 105 by the Ca2+-ATPase, the intracellular calcium concentration will respond to variations in extracellular calcium concentration as experienced during Earth’s history (Stanley and Hardie, 1998), Figure 1. The intracellular concentration of calcium (Cacyt), however, generates a constraint on the intracellular phosphate concentration (POcyt) because calcium and phosphate precipitate to Ca3(PO4)2 when the ion product exceeds the solubility product . We can therefore calculate the maximum possible intracellular phosphate concentration for any intracellular calcium concentration as follows:
3 Results and discussion
3.1 Calcium metabolism
Calcium ions play important roles in the physiology of eukaryotic cells, including control of DNA synthesis, chromosomal configuration, and signal transduction (Marcum et al., 1978; ; Krishtal et al., 1981; Lux and Nagy, 1981; Tsien, 1983; Poenie et al., 1985; ; Steinhardt and Alderton, 1988; ; Sanders et al., 2002; Verret et al., 2010). Calcium ions enter the cell passively via channels (; Verret et al., 2010) that allow for a diffusive influx driven by a steep concentration gradient across the plasma membrane (Langer et al., 2006). Excess intracellular Ca2+ is then actively removed by calcium-binding proteins (e.g., calmodulin) and transport proteins (Ca2+-ATPase and Na+/Ca2+ exchanger) with different calcium affinities and maximum transport rates (). The Ca2+ concentration inside the cell has to be tightly regulated (calcium homeostasis) at around 0.1 μmol L−1 () for optimal cell functioning () and to avoid cell poisoning (Simkiss, 1977; Orrenius et al., 1989; Müller et al., 2015).
The same proteins that maintain intracellular calcium homeostasis in non-calcifying cells (Figure 2A) are implicated in intracellular calcification (Figure 2B). To determine whether an expansion of protein families coincides with the emergence of intracellular calcification, we compared all gene families involved in the precipitation of calcium carbonate (von Dassow et al., 2009) in a large number of eukaryotes (Read et al., 2013). These genes include Ca2+ transporting ATPases, transporters, Ca2+ channels, calmodulin, carbonic anhydrase, Ca2+/H+ exchangers, Na+/Ca2+ exchangers, and vacuolar H+-ATPases. The presence of calcium transport proteins in all eukaryotes clearly indicates that these genes are not unique to intracellular calcification. We found no evidence that diversification of these gene families could explain the appearance of nannoplankton calcification (Supplementary Figures S1 – S7).
FIGURE 2
The most significant difference between calcifying and non-calcifying cells is that calcium carbonate precipitates inside Golgi-derived vesicles. The vesicles fuse with the plasma membrane and the calcium carbonate is extruded outside the cell where it remains attached to the extracellular organic matrix. The same vesicular pathway is used in non-calcifying cells to produce new membrane material and to transport proteins to the plasma membrane (Figure 3). All ion transporters and channels that help establish calcium homeostasis in non-calcifying cells, therefore, reach the plasma membrane via Golgi-derived transport vesicles (Pfeffer and Rothmann, 1987). However, the Ca2+ transporting ATPase initially occurs in its auto-inhibited form and becomes activated by the presence of calmodulin (Tidow et al., 2012) at the plasma membrane. We thus argue that the emergence of intracellular calcification was triggered by the activation of calcium pumps during the passage of transport vesicles from the Golgi apparatus to the plasma membrane, following the accumulation of calcium in the transport vesicles. This explanation is consistent with the simple structure of sub-micron scaled calcite crystals of proto-calcispheres found in previous studies and attributed to calcareous dinoflagellates (; Preto et al., 2013b; ). The activation of the calcium transport inside the Golgi apparatus would later lead to the formation of more elaborated coccolith-like platelets due to the specific endomembranous structure of the Golgi apparatus (Figure 3). This is also in line with the finding that inhibition of the cytoskeleton and microtubule formation induces malformations in modern coccolith (Langer et al., 2010).
FIGURE 3
Such a change in timing of activation would not be detected in gene sequence comparison, as they require protein functional assays. We conclude, however, that all components necessary for the emergence of intracellular calcification were already present in non-calcifying ancestor cells and that no major modifications of cellular physiology and structure were required to induce intracellular calcification. An alternative and speculative hypothesis to the activation of calcium pumps could be that those pumps were already active and that the precipitation of calcium carbonate in the vesicles was prevented by inhibitors, which were subsequently lost thus leading to the emergence of intracellular calcification. But also in this alternative case, the emergence of intracellular calcification would not require major innovations in cellular structure, which is our main argument here.
3.2 Energy requirements
Since ion transport requires energy, a previous study (Monteiro et al., 2016) assumed that intracellular calcification is energetically costly, thus implying the presence of associated benefits to overcome natural selection. But because non-calcifying cells also export calcium from their cytoplasm, the energetic costs of calcification have to be quantified by comparing the costs required for ion transport into vesicles in calcifying cells versus those required by ion transport across the plasma membrane (to maintain calcium homeostasis) in both calcifying and non-calcifying cells. We therefore assessed the energetic costs of intracellular calcification by calculating the total energy required by cellular calcium transport to maintain calcium homeostasis. Our calculations indicate that the precipitation of CaCO3 inside the vesicle removes calcium from the solution and generates a sink that depletes calcium around the cell, Eq. 2. Consequently, the gradient across the plasma membrane that drives the diffusive calcium influx through the channel is reduced with respect to non-calcifying cells, Eq. 4, thus fewer ions have to be transported out of the cytoplasm in order to maintain calcium homeostasis, Eq. 5. Since the energy required for active calcium transport out of a calcifying cell is negligibly lower than that required in non-calcifying cells (Supplementary Figure S8), we conclude that extra energy is not needed to transport calcium for intracellular calcification.
However, our energy calculations also show that the reduction in energy requirements is very small because the calcification flux is slow compared to extracellular calcium diffusion so that no significant diffusive boundary layer develops at the cell surface. If all calcium ions were transported into the vesicles and no calcium were exported through the plasma membrane, fv = 1.0 in Eq. 5, the energy requirements would only be 0.16 percent less than if no calcium were transported into vesicles and all ions were exported through the plasma membrane, fv = 0.0 in Eq. 5.
Besides calcium ions, also carbonate ions are needed in the vesicle to sustain calcification. The transport of carbon could thus be another process requiring energy. However, the transport of hydrogen ions that is coupled to calcium transport creates an alkaline medium inside the calcifying vesicle that shifts the equilibrium of the carbonate system towards carbonate ions and lowers the CO2 concentration (; ). CO2 can, therefore, passively diffuse through the vesicle membrane to replenish the carbonate ions consumed by calcification, thus sustaining calcification at moderate rates (see Figure 3 and Table 4 in ) without additional metabolic costs. Additional carbon transport into the vesicles may only be required to sustain higher calcification rates, as observed in some coccolithophore species (e.g., G. huxleyi) that appeared later in the geological records. Data in support of these arguments can be found in Paasche (1962) and in Young and Ziveri (2000). Since the bicarbonate concentration in the calcifying vesicle is higher than in the cytoplasm, bicarbonate would then need to be transported actively under consumption of metabolic energy (). However, the bicarbonate gradient across the vesicle membrane is much smaller than the calcium gradient and CO2 can freely diffuse across the membrane, thereby functioning as a major source of carbon to the calcifying vesicle () and, thus, preventing additional energetic requirements for bicarbonate transport.
3.3 Evolutionary success
Because of its low metabolic requirements, intracellular calcification does not require secondary evolutionary benefits to emerge. Yet, a number of hypotheses in relation to potential benefits of intracellular calcification have been proposed to explain both emergence and success of coccolithophores. These hypotheses include the potential enhancement of photosynthesis via the removal of carbonate ions (Nielsen, 1966; Paasche, 2002), protection against photoinhibition, advantages in hydrodynamic control, and protection against viruses, bacteria, and grazing (Monteiro et al., 2016). However, enhanced calcification does not enhance photosynthesis (; Trimborn et al., 2007) and non-calcifying coccolithophore cells can grow even faster than calcifying cells (Rost and Riebesell, 2004). Non-calcifying strains appear also not affected by photo-inhibition at high irradiances (Nanninga and Tyrrell, 1996). Additionally, coccolithophores use non-calcifying haploid stages to escape viral infections of calcified diploid cells (), also questioning the relevance of calcification for viral protection. All these cases cast doubts on the assumption that calcification presents relevant physiological advantages.
Previous experiments (Müller et al., 2015) showed that calcifying cells can grow faster than non-calcifying cells when exposed to elevated calcium concentrations, indicating that intracellular calcification may protect against calcium poisoning (Simkiss, 1977). Our calculations show that the Ca2+-ATPase can transport ions against a gradient of up to 105 (see Supplementary Material S1). In non-calcifying cells, an increase of extracellular Ca2+ concentrations yields an increase of intracellular Ca2+ (Figure 2C). Since intracellular phosphate concentrations are usually around 4–5 mM (), cells operate at calcium and phosphate concentrations just below the solubility product of Ca3(PO4)2 (). Increasing intracellular calcium concentrations, therefore, lead to precipitation with phosphate due to the low solubility of Ca3(PO4)2 (Pytkowicz and Kester, 1967; ). The decrease of cellular phosphate impedes cell growth in non-calcifying cells (Figure 2C). In calcifying cells, calcium transport into intracellular vesicles can still occur under elevated extracellular calcium concentrations because the calcium concentration inside the vesicle (ranging from 0.5 to 10 mM ; ) required for the precipitation of calcium carbonate is lower than outside the cell. The calcium gradient at the vesicle membrane therefore permits Ca2+-ATPase activity and allows maintenance of calcium homeostasis even under elevated extracellular calcium concentrations (Figure 2D). Cell division of calcifying cells remains unaffected (Müller et al., 2015).
Another benefit proposed for intracellular calcification is protection against zooplankton grazing (; Monteiro et al., 2016). However, coccolithophores are grazed by copepods without any significant sign of saturation of ingestion rates at increasing coccolithophore densities (). This indicates that calcification and thus mechanical stability does not necessarily protect against copepod grazing. Calcification can, however, have an indirect negative effect on zooplankton grazing. Culture experiments () showed that ingestion of calcifying cells reduces the growth rate of the grazers (Figure 2F), whereas ingestion of non-calcifying cells leads to an incrase in zooplankton growth rate (Figure 2E). A reduction of coccolithophore grazing mortality would thus provide calcifying cells with a competitive advantage against non-calcifying cells (Monteiro et al., 2016). Though not relevant for the emergence of pelagic nannoplankton calcification, the potential chemical protection against grazing may have contributed to its ecological success.
4 Conclusion
In summary, our analyses indicate that the first appearance of intracellular calcification is intrinsically linked to cellular calcium metabolism and to the prevention of calcium accumulation in the cytoplasm. This process did not require major physiological mutations or extra energy but only a very minor change, that is the activation of calcium transport proteins during their passage from the endoplasmic reticulum to the plasma membrane. Therefore, this innovation could have occurred at any time in the geologic past because preconditions were favourable, in line with evidence suggesting unrelated appearances in different lineages. A combination of environmental factors, such as chemical conditions and ecological interactions, may have subsequently helped calcifying nannoplankton to become abundant at a global scale. Therefore, nannoplankton calcifiers rose in pelagic environments during a time, the beginning of the Mesozoic, of profound changes in the structure of Earth’s ecosystems, marked by major climate changes and biological crises (i.e., the Permian–Triassic mass extinction, the Carnian Pluvial Episode and the Triassic-Jurassic mass extinction), which wiped out most of the Palaeozoic life and paved the way to the emergence of modern organisms. Within these new ecosystems, calcifying nannoplankton spread.
Statements
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.
Author contributions
SH, JDC, and AM conceived the idea of the study. SH and ST performed the energy budget calculations. KLH compiled the genetic information and performed the gene tree analysis. All authors contributed to the interpretation of the results. SH and AM wrote the manuscript with contributions from all authors. All authors contributed to the article and approved the submitted version.
Funding
Hanse-Wissenschaftskolleg (HWK) provided visiting fellowships to JDC and KLH.
Acknowledgments
We gratefully acknowledge the Hanse-Wissenschaftskolleg (HWK), Delmenhorst, Germany, for providing visiting fellowship to JDC and KLH and thus for creating the opportunity to bring together the multidisciplinary expertise necessary for this study.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/feart.2023.747059/full#supplementary-material
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Summary
Keywords
calcareous nannoplankton, unicellular eukaryotes, calcium homeostasis, ion transport, Carnian, coccolithophores
Citation
Hohn S, Dal Corso J, Hoke KL, Thoms S and Merico A (2023) Environmental and physiological conditions that led to the rise of calcifying nannoplankton in the Late Triassic. Front. Earth Sci. 11:747059. doi: 10.3389/feart.2023.747059
Received
25 July 2021
Accepted
17 July 2023
Published
31 July 2023
Volume
11 - 2023
Edited by
Ángel Puga-Bernabéu, University of Granada, Spain
Reviewed by
Annette Goetz, State Authority for Mining, Energy and Geology, Germany
Wolfram Michael Kürschner, University of Oslo, Norway
Updates
Copyright
© 2023 Hohn, Dal Corso, Hoke, Thoms and Merico.
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*Correspondence: Agostino Merico, agostino.merico@leibniz-zmt.de
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