Evolution and biomineralization of pteropod shells.

12 pages International audience Shelled pteropods, known as sea butterflies, are a group of small gastropods that spend their entire lives swimming and drifting in the open ocean. They build thin shells of aragonite, a metastable polymorph of calcium carbonate. Pteropod shells have been shown to exp...

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Published in:Journal of Structural Biology
Main Authors: Ramos-Silva, Paula, Wall-Palmer, Deborah, Marlétaz, Ferdinand, Marin, Frédéric, Peijnenburg, Katja T.C.A.
Other Authors: Plankton Diversity and Evolution, Naturalis Biodiversity Center Leiden, Centre for Life’s Origins and Evolution, Biogéosciences UMR 6282 Dijon (BGS), Centre National de la Recherche Scientifique (CNRS)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement, Department of Freshwater and Marine Ecology, University of Amsterdam Amsterdam (UvA)-Institute for Biodiversity and Ecosystem Dynamics (IBED), Work funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreements No844345 project EPIC and No 746186 project POSEIDoN , by a Vidi grant (016.161351) from the Netherlands Organization for Scientific Research (NWO), and by additional support provided by internal funding from the Naturalis Biodiversity Center (Martin Fellowship), from the Malacological Society of London (Travel Award) and from recurrent annual funds of Biog´eosciences research unit (Dijon).
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2021
Subjects:
Online Access:https://hal.archives-ouvertes.fr/hal-03379758
https://hal.archives-ouvertes.fr/hal-03379758/document
https://hal.archives-ouvertes.fr/hal-03379758/file/Pteropods-JSB%20Paula.pdf
https://doi.org/10.1016/j.jsb.2021.107779
id ftccsdartic:oai:HAL:hal-03379758v1
record_format openpolar
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic Aragonite curved fibres
Biominerals
Helical microstructure
Mollusc
Pteropods
Shells
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials
spellingShingle Aragonite curved fibres
Biominerals
Helical microstructure
Mollusc
Pteropods
Shells
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials
Ramos-Silva, Paula
Wall-Palmer, Deborah
Marlétaz, Ferdinand
Marin, Frédéric
Peijnenburg, Katja T.C.A.
Evolution and biomineralization of pteropod shells.
topic_facet Aragonite curved fibres
Biominerals
Helical microstructure
Mollusc
Pteropods
Shells
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials
description 12 pages International audience Shelled pteropods, known as sea butterflies, are a group of small gastropods that spend their entire lives swimming and drifting in the open ocean. They build thin shells of aragonite, a metastable polymorph of calcium carbonate. Pteropod shells have been shown to experience dissolution and reduced thickness with a decrease in pH and therefore represent valuable bioindicators to monitor the impacts of ocean acidification. Over the past decades, several studies have highlighted the striking diversity of shell microstructures in pteropods, with exceptional mechanical properties, but their evolution and future in acidified waters remains uncertain. Here, we revisit the body-of-work on pteropod biomineralization, focusing on shell microstructures and their evolution. The evolutionary history of pteropods was recently resolved, and thus it is timely to examine their shell microstructures in such context. We analyse new images of shells from fossils and recent species providing a comprehensive overview of their structural diversity. Pteropod shells are made of the crossed lamellar and prismatic microstructures common in molluscs, but also of curved nanofibers which are proposed to form a helical three-dimensional structure. Our analyses suggest that the curved fibres emerged before the split between coiled and uncoiled pteropods and that they form incomplete to multiple helical turns. The curved fibres are seen as an important trait in the adaptation to a planktonic lifestyle, giving maximum strength and flexibility to the pteropod thin and lightweight shells. Finally, we also elucidate on the candidate biomineralization genes underpinning the shell diversity in these important indicators of ocean health.
author2 Plankton Diversity and Evolution
Naturalis Biodiversity Center Leiden
Centre for Life’s Origins and Evolution
Biogéosciences UMR 6282 Dijon (BGS)
Centre National de la Recherche Scientifique (CNRS)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement
Department of Freshwater and Marine Ecology
University of Amsterdam Amsterdam (UvA)-Institute for Biodiversity and Ecosystem Dynamics (IBED)
Work funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreements No844345 project EPIC and No 746186 project POSEIDoN , by a Vidi grant (016.161351) from the Netherlands Organization for Scientific Research (NWO), and by additional support provided by internal funding from the Naturalis Biodiversity Center (Martin Fellowship), from the Malacological Society of London (Travel Award) and from recurrent annual funds of Biog´eosciences research unit (Dijon).
format Article in Journal/Newspaper
author Ramos-Silva, Paula
Wall-Palmer, Deborah
Marlétaz, Ferdinand
Marin, Frédéric
Peijnenburg, Katja T.C.A.
author_facet Ramos-Silva, Paula
Wall-Palmer, Deborah
Marlétaz, Ferdinand
Marin, Frédéric
Peijnenburg, Katja T.C.A.
author_sort Ramos-Silva, Paula
title Evolution and biomineralization of pteropod shells.
title_short Evolution and biomineralization of pteropod shells.
title_full Evolution and biomineralization of pteropod shells.
title_fullStr Evolution and biomineralization of pteropod shells.
title_full_unstemmed Evolution and biomineralization of pteropod shells.
title_sort evolution and biomineralization of pteropod shells.
publisher HAL CCSD
publishDate 2021
url https://hal.archives-ouvertes.fr/hal-03379758
https://hal.archives-ouvertes.fr/hal-03379758/document
https://hal.archives-ouvertes.fr/hal-03379758/file/Pteropods-JSB%20Paula.pdf
https://doi.org/10.1016/j.jsb.2021.107779
genre Ocean acidification
genre_facet Ocean acidification
op_source ISSN: 1047-8477
EISSN: 1095-8657
Journal of Structural Biology
https://hal.archives-ouvertes.fr/hal-03379758
Journal of Structural Biology, Elsevier, 2021, 213 (4), pp.107779. ⟨10.1016/j.jsb.2021.107779⟩
https://www.sciencedirect.com/science/article/pii/S1047847721000848?via%3Dihub
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doi:10.1016/j.jsb.2021.107779
PUBMED: 34474158
op_rights info:eu-repo/semantics/OpenAccess
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container_title Journal of Structural Biology
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spelling ftccsdartic:oai:HAL:hal-03379758v1 2023-05-15T17:51:46+02:00 Evolution and biomineralization of pteropod shells. Ramos-Silva, Paula Wall-Palmer, Deborah Marlétaz, Ferdinand Marin, Frédéric Peijnenburg, Katja T.C.A. Plankton Diversity and Evolution Naturalis Biodiversity Center Leiden Centre for Life’s Origins and Evolution Biogéosciences UMR 6282 Dijon (BGS) Centre National de la Recherche Scientifique (CNRS)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement Department of Freshwater and Marine Ecology University of Amsterdam Amsterdam (UvA)-Institute for Biodiversity and Ecosystem Dynamics (IBED) Work funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreements No844345 project EPIC and No 746186 project POSEIDoN , by a Vidi grant (016.161351) from the Netherlands Organization for Scientific Research (NWO), and by additional support provided by internal funding from the Naturalis Biodiversity Center (Martin Fellowship), from the Malacological Society of London (Travel Award) and from recurrent annual funds of Biog´eosciences research unit (Dijon). 2021-12 https://hal.archives-ouvertes.fr/hal-03379758 https://hal.archives-ouvertes.fr/hal-03379758/document https://hal.archives-ouvertes.fr/hal-03379758/file/Pteropods-JSB%20Paula.pdf https://doi.org/10.1016/j.jsb.2021.107779 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.jsb.2021.107779 info:eu-repo/semantics/altIdentifier/pmid/34474158 hal-03379758 https://hal.archives-ouvertes.fr/hal-03379758 https://hal.archives-ouvertes.fr/hal-03379758/document https://hal.archives-ouvertes.fr/hal-03379758/file/Pteropods-JSB%20Paula.pdf doi:10.1016/j.jsb.2021.107779 PUBMED: 34474158 info:eu-repo/semantics/OpenAccess ISSN: 1047-8477 EISSN: 1095-8657 Journal of Structural Biology https://hal.archives-ouvertes.fr/hal-03379758 Journal of Structural Biology, Elsevier, 2021, 213 (4), pp.107779. ⟨10.1016/j.jsb.2021.107779⟩ https://www.sciencedirect.com/science/article/pii/S1047847721000848?via%3Dihub Aragonite curved fibres Biominerals Helical microstructure Mollusc Pteropods Shells [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials info:eu-repo/semantics/article Journal articles 2021 ftccsdartic https://doi.org/10.1016/j.jsb.2021.107779 2021-11-27T23:28:44Z 12 pages International audience Shelled pteropods, known as sea butterflies, are a group of small gastropods that spend their entire lives swimming and drifting in the open ocean. They build thin shells of aragonite, a metastable polymorph of calcium carbonate. Pteropod shells have been shown to experience dissolution and reduced thickness with a decrease in pH and therefore represent valuable bioindicators to monitor the impacts of ocean acidification. Over the past decades, several studies have highlighted the striking diversity of shell microstructures in pteropods, with exceptional mechanical properties, but their evolution and future in acidified waters remains uncertain. Here, we revisit the body-of-work on pteropod biomineralization, focusing on shell microstructures and their evolution. The evolutionary history of pteropods was recently resolved, and thus it is timely to examine their shell microstructures in such context. We analyse new images of shells from fossils and recent species providing a comprehensive overview of their structural diversity. Pteropod shells are made of the crossed lamellar and prismatic microstructures common in molluscs, but also of curved nanofibers which are proposed to form a helical three-dimensional structure. Our analyses suggest that the curved fibres emerged before the split between coiled and uncoiled pteropods and that they form incomplete to multiple helical turns. The curved fibres are seen as an important trait in the adaptation to a planktonic lifestyle, giving maximum strength and flexibility to the pteropod thin and lightweight shells. Finally, we also elucidate on the candidate biomineralization genes underpinning the shell diversity in these important indicators of ocean health. Article in Journal/Newspaper Ocean acidification Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Journal of Structural Biology 213 4 107779