scholarly journals Marine and freshwater micropearls: Biomineralization producing strontium-rich amorphous calcium carbonate inclusions is widespread in the genus <i>Tetraselmis</i> (Chlorophyta)

2018 ◽  
Author(s):  
Agathe Martignier ◽  
Montserrat Filella ◽  
Kilian Pollok ◽  
Michael Melkonian ◽  
Michael Bensimon ◽  
...  

Abstract. The genus Tetraselmis (Chlorophyta) includes more than 30 species of unicellular micro-algae that have been widely studied since the description of the first species in 1878. Tetraselmis cordiformis (presumably the only freshwater species of the genus) was discovered recently to form intracellular mineral inclusions, called micropearls, which had been previously overlooked. These non-skeletal intracellular inclusions of hydrated amorphous calcium carbonates (ACC) were first described in Lake Geneva (Switzerland) and are the result of a novel biomineralization process. The present study shows that many Tetraselmis species share this biomineralization capacity: 10 species out of the 12 tested contained micropearls, including T. chui, T. convolutae, T. levis, T. subcordiformis, T. suecica and T. tetrathele. Our results indicate that micropearls are not randomly distributed inside the Tetraselmis cells, but are located preferentially under the plasma membrane and seem to form a definite pattern, which differs between species. In Tetraselmis cells, the biomineralization process seems to systematically start with a rod-shaped nucleus and results in an enrichment of the micropearls in strontium over calcium (the Sr / Ca ratio is up to 219 times higher in the micropearls than in the surrounding water or growth medium). This concentrating capacity varies from one species to the other, which might be of interest for possible bioremediation techniques regarding radioactive 90Sr water pollution. The Tetraselmis species forming micropearls live in various habitats, indicating that this novel biomineralization process can take place in different environments (marine, brackish and freshwater) and is therefore a widespread phenomenon.

2018 ◽  
Vol 15 (21) ◽  
pp. 6591-6605 ◽  
Author(s):  
Agathe Martignier ◽  
Montserrat Filella ◽  
Kilian Pollok ◽  
Michael Melkonian ◽  
Michael Bensimon ◽  
...  

Abstract. Unicellular algae play important roles in the biogeochemical cycles of numerous elements, particularly through the biomineralization capacity of certain species (e.g., coccolithophores greatly contributing to the “organic carbon pump” of the oceans), and unidentified actors of these cycles are still being discovered. This is the case of the unicellular alga Tetraselmis cordiformis (Chlorophyta) that was recently discovered to form intracellular mineral inclusions, called micropearls, which had been previously overlooked. These intracellular inclusions of hydrated amorphous calcium carbonates (ACCs) were first described in Lake Geneva (Switzerland) and are the result of a novel biomineralization process. The genus Tetraselmis includes more than 30 species that have been widely studied since the description of the type species in 1878. The present study shows that many other Tetraselmis species share this biomineralization capacity: 10 species out of the 12 tested contained micropearls, including T. chui, T. convolutae, T. levis, T. subcordiformis, T. suecica and T. tetrathele. Our results indicate that micropearls are not randomly distributed inside the Tetraselmis cells but are located preferentially under the plasma membrane and seem to form a definite pattern, which differs among species. In Tetraselmis cells, the biomineralization process seems to systematically start with a rod-shaped nucleus and results in an enrichment of the micropearls in Sr over Ca (the Sr∕Ca ratio is more than 200 times higher in the micropearls than in the surrounding water or growth medium). This concentrating capacity varies among species and may be of interest for possible bioremediation techniques regarding radioactive 90Sr water pollution. The Tetraselmis species forming micropearls live in various habitats, indicating that this novel biomineralization process takes place in different environments (marine, brackish and freshwater) and is therefore a widespread phenomenon.


Geosciences ◽  
2022 ◽  
Vol 12 (1) ◽  
pp. 32
Author(s):  
Agathe Martignier ◽  
Montserrat Filella ◽  
Jean-Michel Jaquet ◽  
Mathieu Coster ◽  
Daniel Ariztegui

In unicellular organisms, intracellular inclusions of amorphous calcium carbonate (ACC) were initially described in cyanobacteria and, later, in unicellular eukaryotes from Lake Geneva (Switzerland/France). Inclusions in unicellular eukaryotes, named micropearls, consist of hydrated ACCs, frequently enriched in Sr or Ba, and displaying internal oscillatory zonations, due to variations in the Ba:Ca or Sr:Ca ratios. An analysis of our database, consisting of 1597 micropearl analyses from Lake Geneva and 34 from Lake Titicaca (Bolivia/Peru), showed that a certain number of Sr- and Ba-enriched micropearls from these lakes contain As in amounts measurable by EDXS. A Q-mode statistical analysis confirmed the existence of five chemically distinct morpho-chemical groups of As-bearing micropearls, among which was a new category identified in Lake Geneva, where As is often associated with Mg. This new type of micropearl is possibly produced in a small (7–12 μm size) bi-flagellated organism. Micropearls from Lake Titicaca, which contain Sr, were found in an organism very similar to Tetraselmis cordiformis, which was observed earlier in Lake Geneva. Lake Titicaca micropearls contain larger As amounts, which can be explained by the high As concentration in the water of this lake. The ubiquity of this observed biomineralization process points to the need for a better understanding of the role of amorphous or crystalline calcium carbonates in As cycling in surface waters.


Author(s):  
Agathe Martignier ◽  
Montserrat Filella ◽  
Jean-Michel Jaquet ◽  
Mathieu Coster ◽  
Daniel Ariztegui

In unicellular organisms, intracellular inclusions of amorphous calcium carbonate (ACC) have been initially described in cyanobacteria and, later, in unicellular eukaryotes of Lake Geneva (Switzerland/France). Inclusions in unicellular eukaryotes ‒named micropearls‒ consist of hydrated ACCs, frequently enriched in Sr or Ba, displaying internal oscillatory zonations due to variations in the Ba:Ca or Sr:Ca ratios. The analysis of our database consisting of 1597 micropearl analyses from Lake Geneva and 34 from Lake Titicaca (Bolivia/Peru) has shown that a certain number of Sr and Ba-enriched micropearls from these lakes contain As in amounts measurable by EDXS. A Q-mode statistical analysis has confirmed the existence of five geochemically distinct morpho-chemical groups of As-bearing micropearls, among which a new category identified in Lake Geneva, where As is often associated with Mg. This new type of micropearl is possibly produced in a small (7-12 m size) bi-flagellated organism. Micropearls from Lake Titicaca, which contain Sr, are found in an organism very similar to Tetraselmis cordiformis, observed in Lake Geneva. Lake Titicaca micropearls contain higher As concentrations which can be explained by the high As concentration in the water of this lake. The ubiquity of the biomineralization process observed points to the need for better understanding of the role of amorphous or crystalline calcium carbonates in As cycling in surface waters.


2021 ◽  
Author(s):  
Inés Segovia Campos ◽  
Agathe Martignier ◽  
Montserrat Filella ◽  
Daniel Ariztegui

&lt;p&gt;Chlorodendrophyceae are a class of unicellular green algae widespread in the aquatic environment (seawater, brackish water, and freshwater) that have recently been discovered to form intracellular carbonates. These mineral inclusions, called &lt;em&gt;micropearls&lt;/em&gt;, are mainly composed of hydrated amorphous calcium carbonates (ACC) in which strontium can also accumulate at high concentrations. Under natural and culture conditions, the Sr/Ca ratio of micropearls can be 200 times higher than in their environment, suggesting that Chlorodendrophyceae species may be considered as potential candidates for new bioremediation methods regarding radioactive &lt;sup&gt;90&lt;/sup&gt;Sr water contamination. Because very little is known about this phenomenon, ongoing experiments with laboratory cultures are providing essential information about the cellular mechanisms involved in this newly discovered biomineralization process and its impact on the geochemical cycles of Ca and Sr.&lt;/p&gt;


2020 ◽  
Author(s):  
Neha Mehta ◽  
Feriel-Skouri Panet ◽  
Karim Benzerara

&lt;p&gt;Cyanobacteria are an abundant and diverse group of photosynthetic bacteria that have shaped Earth&amp;#8217;s environment for billions of years and play a vital role in the cycling of numerous elements such as carbon, calcium, and phosphorus. In particular, their impact on the global carbon cycle is of significant interest in the context of carbon capture and climate change, as they sequester atmospheric CO&lt;sub&gt;2&lt;/sub&gt; into organic carbon and biogenic calcium carbonates (CaCO&lt;sub&gt;3&lt;/sub&gt;) through a process called calcification.&amp;#160; The process of calcification has long been considered as extracellular and non-biologically controlled. However, recently, several cyanobacterial species have been reported to form intracellular amorphous calcium carbonate (ACC) inclusions. These cyanobacteria were found in diverse&amp;#160;environments and accumulate high concentrations of AEE (Ca, Ba and Sr) from solutions&amp;#160;undersaturated with respect to AEE-carbonate phases.&amp;#160;Moreover, one of these cyanobacteria species, &lt;em&gt;G. lithophora&lt;/em&gt; was shown to selectively accumulate stable and radioactive alkaline earth elements (AEE) within the intracellular amorphous carbonates and/or polyp inclusions (Mehta et al., 2019). Recently, it was confirmed that cyanobacteria forming intracellular ACC contained a much higher content of alkaline earth elements (AEE) than all other cyanobacteria (DeWever et al., 2019). The high concentration of Ba and Sr within these intracellular inclusions was surprising because Ba and Sr have usually been considered as having no physiological role at all. The high concentration of Ca within these intracellular inclusions was directly in contrast with the traditional paradigm of cells maintaining a state of homeostasis with respect to Ca. Furthermore, Sr/Ca and Ba/Ca ratios in these ACC inclusions were very different from those expected from abiotic precipitation in the solution surrounding the cells (Cam et al. 2015). To understand the biological driver behind these observations, first, I will present a review of the above mentioned &amp;#8220;vital effects&amp;#8221; in the context of intracellular calcification in cyanobacteria. Second, using batch incubation experiments, I will show that high Ca concentrations are vital not only for the growth of &lt;em&gt;G. lithophora&lt;/em&gt;, but also for the uptake of Ba by &lt;em&gt;G. lithophora&lt;/em&gt;. Lastly, I will examine Ca homeostasis in ACC forming cyanobacterial strains by using an antagonist/inhibitor of a known channel/transporter involved in Ca transport. &amp;#160;Overall, these insights will shed some light on the role of cyanobacteria forming intracellular ACC on carbonate (bio)mineralization, in both modern and ancient Earth&amp;#8217;s environment.&amp;#160;&lt;/p&gt;&lt;p&gt;Reference:&lt;/p&gt;&lt;p&gt;N Mehta, K Benzerara, B Kocar, V Chapon, Sequestration of radionuclidesRadium-226 and Strontium-90 by cyanobacteria forming intracellular calcium carbonates, ES&amp;T 2019&lt;/p&gt;&lt;p&gt;De Wever, A.; Benzerara, K. et al. Evidence of High Ca Uptake by Cyanobacteria Forming Intracellular CaCO 3 and Impact on Their Growth. Geobiology 2019&lt;/p&gt;&lt;p&gt;Cam, N., Georgelin, T., Jaber, M., Lambert, J.-F., and Benzerara, K, In vitro synthesis of amorphous Mg-, Ca-, Sr- and Ba-carbonates: what do we learn about intracellular calcification by cyanobacteria? Geochim. Cosmochim. Acta 2015&lt;/p&gt;&lt;p&gt;&amp;#160;&lt;/p&gt;


2017 ◽  
Vol 89 (5) ◽  
pp. 645-652 ◽  
Author(s):  
Bruno Thien ◽  
Agathe Martignier ◽  
Jean-Michel Jaquet ◽  
Montserrat Filella

AbstractIntracellular inclusions of amorphous Ba- and Sr-rich calcium carbonates – referred to as “micropearls”– have recently been detected in Lake Geneva. These micropearls are formed under conditions of pronounced Ba and Sr undersaturation in the lake waters. Their formation can be explained by the ability of certain microorganisms to preconcentrate these trace elements in tandem with a non-equilibrium solid-solution growing mechanism.


Nanomaterials ◽  
2021 ◽  
Vol 11 (2) ◽  
pp. 264
Author(s):  
Francesca Cestari ◽  
Francesca Agostinacchio ◽  
Anna Galotta ◽  
Giovanni Chemello ◽  
Antonella Motta ◽  
...  

Biogenic calcium carbonates naturally contain ions that can be beneficial for bone regeneration and therefore are attractive resources for the production of bioactive calcium phosphates. In the present work, cuttlefish bones, mussel shells, chicken eggshells and bioinspired amorphous calcium carbonate were used to synthesize hydroxyapatite nano-powders which were consolidated into cylindrical pellets by uniaxial pressing and sintering 800–1100 °C. Mineralogical, structural and chemical composition were studied by SEM, XRD, inductively coupled plasma/optical emission spectroscopy (ICP/OES). The results show that the phase composition of the sintered materials depends on the Ca/P molar ratio and on the specific CaCO3 source, very likely associated with the presence of some doping elements like Mg2+ in eggshell and Sr2+ in cuttlebone. Different CaCO3 sources also resulted in variable densification and sintering temperature. Preliminary in vitro tests were carried out (by the LDH assay) and they did not reveal any cytotoxic effects, while good cell adhesion and proliferation was observed at day 1, 3 and 5 after seeding through confocal microscopy. Among the different tested materials, those derived from eggshells and sintered at 900 °C promoted the best cell adhesion pattern, while those from cuttlebone and amorphous calcium carbonate showed round-shaped cells and poorer cell-to-cell interconnection.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
J. Gautron ◽  
L. Stapane ◽  
N. Le Roy ◽  
Y. Nys ◽  
A. B. Rodriguez-Navarro ◽  
...  

AbstractThe avian eggshell is a natural protective envelope that relies on the phenomenon of biomineralization for its formation. The shell is made of calcium carbonate in the form of calcite, which contains hundreds of proteins that interact with the mineral phase controlling its formation and structural organization, and thus determine the mechanical properties of the mature biomaterial. We describe its mineralogy, structure and the regulatory interactions that integrate the mineral and organic constituents. We underline recent evidence for vesicular transfer of amorphous calcium carbonate (ACC), as a new pathway to ensure the active and continuous supply of the ions necessary for shell mineralization. Currently more than 900 proteins and thousands of upregulated transcripts have been identified during chicken eggshell formation. Bioinformatic predictions address their functionality during the biomineralization process. In addition, we describe matrix protein quantification to understand their role during the key spatially- and temporally- regulated events of shell mineralization. Finally, we propose an updated scheme with a global scenario encompassing the mechanisms of avian eggshell mineralization. With this large dataset at hand, it should now be possible to determine specific motifs, domains or proteins and peptide sequences that perform a critical function during avian eggshell biomineralization. The integration of this insight with genomic data (non-synonymous single nucleotide polymorphisms) and precise phenotyping (shell biomechanical parameters) on pure selected lines will lead to consistently better-quality eggshell characteristics for improved food safety. This information will also address the question of how the evolutionary-optimized chicken eggshell matrix proteins affect and regulate calcium carbonate mineralization as a good example of biomimetic and bio-inspired material design.


2021 ◽  
Author(s):  
Karim Benzerara ◽  
Elodie Duprat ◽  
Tristan Bitard-Feildel ◽  
Géraldine Caumes ◽  
Corinne Cassier-Chauvat ◽  
...  

Cyanobacteria have massively contributed to carbonate deposit formation over the geological history. They are traditionally thought to biomineralize CaCO3 extracellularly as an indirect byproduct of photosynthesis. However, the recent discovery of freshwater cyanobacteria forming intracellular amorphous calcium carbonates (iACC) challenges this view. Despite the geochemical interest of such a biomineralization process, its molecular mechanisms and evolutionary history remain elusive. Here, using comparative genomics, we identify a new gene (ccyA) and protein (calcyanin) family specifically associated with cyanobacterial iACC biomineralization. Calcyanin is composed of a conserved C-terminal domain, which likely adopts an original fold, and a variable N- terminal domain whose structure allows differentiating 4 major types among the 35 known calcyanin homologues. Calcyanin lacks detectable full-length homologs with known function. Yet, genetic and comparative genomic analyses suggest a possible involvement in Ca homeostasis, making this gene family a particularly interesting target for future functional studies. Whatever its function, this new gene family appears as a gene diagnostic of intracellular calcification in cyanobacteria. By searching for ccyA in publicly available genomes, we identified 13 additional cyanobacterial strains forming iACC. This significantly extends our knowledge about the phylogenetic and environmental distribution of cyanobacterial iACC biomineralization, especially with the detection of multicellular genera as well as a marine species. Phylogenetic analyses indicate that iACC biomineralization is ancient, with independent losses in various lineages and some HGT cases that resulted in the broad but patchy distribution of calcyanin across modern cyanobacteria. Overall, iACC biomineralization emerges as a new case of genetically controlled biomineralization in bacteria.


2019 ◽  
Vol 2019 ◽  
pp. 1-9
Author(s):  
Zeng-Qiong Huang ◽  
Gang-Sheng Zhang ◽  
Yuan Tan

Biomimetic synthesis of aragonite with various templates in vitro is an important way to understand the biomineralization process and synthesize nacre-like materials. Herein, we used the siphon sheath from the bivalve Lutraria sieboldii as the substrate for the formation of calcium carbonate. We found that the inner layer of the sheath, which is composed of approximately 40% protein and 60% β-chitin, induced the formation of nearly pure aragonite by the transformation of amorphous calcium carbonate (ACC). More surprisingly, unique starfruit-shaped aragonite aggregates were observed on the substrate and were constructed from many adhered, oriented aragonite tablets. We consider that the acid-rich protein from the inner layer of the siphon sheath triggers the formation of ACC, and the swollen β-chitin regulates the transformation of ACC into aragonite by lattice matching and stereochemical recognition. The various surface adhesion energies of the crystal, the change in growth rates on different crystallographic facets, and the hexagonal features of the aragonite tablets led to the formation of starfruit-shaped aragonite aggregates.


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