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A vacuole-like compartment concentrates a disordered calcium phase in a key coccolithophorid alga.

Sviben S, Gal A, Hood MA, Bertinetti L, Politi Y, Bennet M, Krishnamoorthy P, Schertel A, Wirth R, Sorrentino A, Pereiro E, Faivre D, Scheffel A - Nat Commun (2016)

Bottom Line: We identify a compartment, distinct from the coccolith-producing compartment, filled with high concentrations of a disordered form of calcium.The amounts of calcium stored in this reservoir seem to be dynamic and at a certain stage the compartment is in direct contact with the coccolith-producing vesicle, suggesting an active role in coccolith formation.Our findings provide insights into calcium accumulation in this important calcifying organism.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck Institute of Molecular Plant Physiology, Potsdam-Golm 14476, Germany.

ABSTRACT
Coccoliths are calcitic particles produced inside the cells of unicellular marine algae known as coccolithophores. They are abundant components of sea-floor carbonates, and the stoichiometry of calcium to other elements in fossil coccoliths is widely used to infer past environmental conditions. Here we study cryo-preserved cells of the dominant coccolithophore Emiliania huxleyi using state-of-the-art nanoscale imaging and spectroscopy. We identify a compartment, distinct from the coccolith-producing compartment, filled with high concentrations of a disordered form of calcium. Co-localized with calcium are high concentrations of phosphorus and minor concentrations of other cations. The amounts of calcium stored in this reservoir seem to be dynamic and at a certain stage the compartment is in direct contact with the coccolith-producing vesicle, suggesting an active role in coccolith formation. Our findings provide insights into calcium accumulation in this important calcifying organism.

No MeSH data available.


Related in: MedlinePlus

Conceptual model of the coccolith calcium pathway.Ca accumulation and calcite precipitation are spatially and temporallyseparated. Calcium uptake into cells involves Ca transporter. The Ca ionsare concentrated by polyphosphates into a disordered phase in a compartmentdistinct from the coccolith vesicle–reticular body system. Thedisordered Ca phase is a dynamic reservoir, concentrating and dispatching Caions. The released Ca ions are possibly transferred into the coccolithvesicle–reticular body system by Ca transporter and/or passivediffusion driven by a high-concentration gradient in free Ca ions. Insidethe coccolith vesicle the calcium is precipitated as calcite.
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f7: Conceptual model of the coccolith calcium pathway.Ca accumulation and calcite precipitation are spatially and temporallyseparated. Calcium uptake into cells involves Ca transporter. The Ca ionsare concentrated by polyphosphates into a disordered phase in a compartmentdistinct from the coccolith vesicle–reticular body system. Thedisordered Ca phase is a dynamic reservoir, concentrating and dispatching Caions. The released Ca ions are possibly transferred into the coccolithvesicle–reticular body system by Ca transporter and/or passivediffusion driven by a high-concentration gradient in free Ca ions. Insidethe coccolith vesicle the calcium is precipitated as calcite.

Mentions: Our results show that E. huxleyi cells concentrate large amounts of Ca into adense disordered phase in a vacuole-like compartment. Such a major internal storemust be a dominant player in the cellular Ca budget and will have a pivotal role inthe subcellular partitioning and allocation of Ca. The Ca phase stored in thehere-discovered compartment is likely not a direct precursor phase of coccolithcalcite, as (i) the Ca-rich body was never seen in direct contact with statusnascendi coccoliths, (ii) Ca and P were not detectable in the lumen of thecoccolith vesicle–reticular body system and the coccolith calcite is virtuallyfree of P, and (iii) the calcein stain was never observed in the coccolithvesicle–reticular body system or coccolith calcite, ruling out the possibilityof bulk transport from the Ca reservoir to the coccolith vesicle. The latterobservation is in contrast to the situation in many other calcifying organisms whereexogenously applied calcein becomes incorporated in the mineralized material143132. Considering all the above-reported observations, the mostplausible Ca transfer scenario is that Ca ions are released from their complex withpolyphosphate, likely by enzymatic degradation of the polyphosphate and/oracidification of the compartment, and these are transported by Ca transporter and/orpassive diffusion into the coccolith vesicle–reticular body system (Fig. 7). The large membrane surface of the reticular body hasbeen suggested to accommodate large numbers of calcium transporters33. The direct contact between the membranes of both compartment systems (Fig. 6c,d), and in particular between the Ca store and thereticular body, may be advantageous as it may enable direct transfer of Ca and sobypass the cytosol where a high concentration of calcium ions could be toxic.


A vacuole-like compartment concentrates a disordered calcium phase in a key coccolithophorid alga.

Sviben S, Gal A, Hood MA, Bertinetti L, Politi Y, Bennet M, Krishnamoorthy P, Schertel A, Wirth R, Sorrentino A, Pereiro E, Faivre D, Scheffel A - Nat Commun (2016)

Conceptual model of the coccolith calcium pathway.Ca accumulation and calcite precipitation are spatially and temporallyseparated. Calcium uptake into cells involves Ca transporter. The Ca ionsare concentrated by polyphosphates into a disordered phase in a compartmentdistinct from the coccolith vesicle–reticular body system. Thedisordered Ca phase is a dynamic reservoir, concentrating and dispatching Caions. The released Ca ions are possibly transferred into the coccolithvesicle–reticular body system by Ca transporter and/or passivediffusion driven by a high-concentration gradient in free Ca ions. Insidethe coccolith vesicle the calcium is precipitated as calcite.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4834641&req=5

f7: Conceptual model of the coccolith calcium pathway.Ca accumulation and calcite precipitation are spatially and temporallyseparated. Calcium uptake into cells involves Ca transporter. The Ca ionsare concentrated by polyphosphates into a disordered phase in a compartmentdistinct from the coccolith vesicle–reticular body system. Thedisordered Ca phase is a dynamic reservoir, concentrating and dispatching Caions. The released Ca ions are possibly transferred into the coccolithvesicle–reticular body system by Ca transporter and/or passivediffusion driven by a high-concentration gradient in free Ca ions. Insidethe coccolith vesicle the calcium is precipitated as calcite.
Mentions: Our results show that E. huxleyi cells concentrate large amounts of Ca into adense disordered phase in a vacuole-like compartment. Such a major internal storemust be a dominant player in the cellular Ca budget and will have a pivotal role inthe subcellular partitioning and allocation of Ca. The Ca phase stored in thehere-discovered compartment is likely not a direct precursor phase of coccolithcalcite, as (i) the Ca-rich body was never seen in direct contact with statusnascendi coccoliths, (ii) Ca and P were not detectable in the lumen of thecoccolith vesicle–reticular body system and the coccolith calcite is virtuallyfree of P, and (iii) the calcein stain was never observed in the coccolithvesicle–reticular body system or coccolith calcite, ruling out the possibilityof bulk transport from the Ca reservoir to the coccolith vesicle. The latterobservation is in contrast to the situation in many other calcifying organisms whereexogenously applied calcein becomes incorporated in the mineralized material143132. Considering all the above-reported observations, the mostplausible Ca transfer scenario is that Ca ions are released from their complex withpolyphosphate, likely by enzymatic degradation of the polyphosphate and/oracidification of the compartment, and these are transported by Ca transporter and/orpassive diffusion into the coccolith vesicle–reticular body system (Fig. 7). The large membrane surface of the reticular body hasbeen suggested to accommodate large numbers of calcium transporters33. The direct contact between the membranes of both compartment systems (Fig. 6c,d), and in particular between the Ca store and thereticular body, may be advantageous as it may enable direct transfer of Ca and sobypass the cytosol where a high concentration of calcium ions could be toxic.

Bottom Line: We identify a compartment, distinct from the coccolith-producing compartment, filled with high concentrations of a disordered form of calcium.The amounts of calcium stored in this reservoir seem to be dynamic and at a certain stage the compartment is in direct contact with the coccolith-producing vesicle, suggesting an active role in coccolith formation.Our findings provide insights into calcium accumulation in this important calcifying organism.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck Institute of Molecular Plant Physiology, Potsdam-Golm 14476, Germany.

ABSTRACT
Coccoliths are calcitic particles produced inside the cells of unicellular marine algae known as coccolithophores. They are abundant components of sea-floor carbonates, and the stoichiometry of calcium to other elements in fossil coccoliths is widely used to infer past environmental conditions. Here we study cryo-preserved cells of the dominant coccolithophore Emiliania huxleyi using state-of-the-art nanoscale imaging and spectroscopy. We identify a compartment, distinct from the coccolith-producing compartment, filled with high concentrations of a disordered form of calcium. Co-localized with calcium are high concentrations of phosphorus and minor concentrations of other cations. The amounts of calcium stored in this reservoir seem to be dynamic and at a certain stage the compartment is in direct contact with the coccolith-producing vesicle, suggesting an active role in coccolith formation. Our findings provide insights into calcium accumulation in this important calcifying organism.

No MeSH data available.


Related in: MedlinePlus