Evolution and biomineralization of pteropod shells

Journal of Structural Biology, vol. 213, pp. 107779

Abstract

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.

Authors 5

1. Paula Ramos‐Silva corresponding Aachen Plankton Diversity and Evolution Naturalis Biodiversity Center

   Naturalis Biodiversity Center

   Affiliation as printed

   Plankton Diversity and Evolution, Naturalis Biodiversity Center, the Netherlands. Electronic address: paula.srs@gmail.com

   Plankton Diversity and Evolution (Netherlands)

2. Deborah Wall-Palmer Aachen Plankton Diversity and Evolution Naturalis Biodiversity Center

   Naturalis Biodiversity Center

   Affiliation as printed

   Plankton Diversity and Evolution, Naturalis Biodiversity Center, the Netherlands

   Plankton Diversity and Evolution (Netherlands)

3. Ferdinand Marlétaz

   University College London

   Affiliation as printed

   Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, United Kingdom

   Centre for Life’s Origins and Evolution (University College London - United Kingdom)

4. Frédéric Marin

   Centre National de la Recherche Scientifique · Université de Bourgogne · Biogéosciences

   Affiliation as printed

   University of Burgundy-Franche-Comté, Laboratoire Biogéosciences UMR CNRS 6282, France

   BGS - Biogéosciences [UMR 6282] (Université de Bourgogne - 6 boulevard Gabriel - 21000 Dijon - France)

5. Katja T. C. A. Peijnenburg Aachen

   Naturalis Biodiversity Center · University of Amsterdam

   Affiliation as printed

   Plankton Diversity and Evolution, Naturalis Biodiversity Center, the Netherlands; Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, the Netherlands

   Department of Freshwater and Marine Ecology (Netherlands)

   Plankton Diversity and Evolution (Netherlands)