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Form and function of F-actin during biomineralization revealed from live experiments on foraminifera

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, unicel...

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Autores principales: Tyszka, Jarosław, Bickmeyer, Ulf, Raitzsch, Markus, Bijma, Jelle, Kaczmarek, Karina, Mewes, Antje, Topa, Paweł, Janse, Max
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6410838/
https://www.ncbi.nlm.nih.gov/pubmed/30782789
http://dx.doi.org/10.1073/pnas.1810394116
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author Tyszka, Jarosław
Bickmeyer, Ulf
Raitzsch, Markus
Bijma, Jelle
Kaczmarek, Karina
Mewes, Antje
Topa, Paweł
Janse, Max
author_facet Tyszka, Jarosław
Bickmeyer, Ulf
Raitzsch, Markus
Bijma, Jelle
Kaczmarek, Karina
Mewes, Antje
Topa, Paweł
Janse, Max
author_sort Tyszka, Jarosław
collection PubMed
description 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.
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spelling pubmed-64108382019-03-13 Form and function of F-actin during biomineralization revealed from live experiments on foraminifera Tyszka, Jarosław Bickmeyer, Ulf Raitzsch, Markus Bijma, Jelle Kaczmarek, Karina Mewes, Antje Topa, Paweł Janse, Max Proc Natl Acad Sci U S A Physical Sciences 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. National Academy of Sciences 2019-03-05 2019-02-19 /pmc/articles/PMC6410838/ /pubmed/30782789 http://dx.doi.org/10.1073/pnas.1810394116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Tyszka, Jarosław
Bickmeyer, Ulf
Raitzsch, Markus
Bijma, Jelle
Kaczmarek, Karina
Mewes, Antje
Topa, Paweł
Janse, Max
Form and function of F-actin during biomineralization revealed from live experiments on foraminifera
title Form and function of F-actin during biomineralization revealed from live experiments on foraminifera
title_full Form and function of F-actin during biomineralization revealed from live experiments on foraminifera
title_fullStr Form and function of F-actin during biomineralization revealed from live experiments on foraminifera
title_full_unstemmed Form and function of F-actin during biomineralization revealed from live experiments on foraminifera
title_short Form and function of F-actin during biomineralization revealed from live experiments on foraminifera
title_sort form and function of f-actin during biomineralization revealed from live experiments on foraminifera
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6410838/
https://www.ncbi.nlm.nih.gov/pubmed/30782789
http://dx.doi.org/10.1073/pnas.1810394116
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