Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics

Melody S. Clark, Lloyd S. Peck, Jaison Arivalagan, Thierry Backeljau, Sophie Berland, Joao C. R. Cardoso, Carlos Caurcel, Gauthier Chapelle, Michele De Noia, Sam Dupont, Karim Gharbi, Joseph I. Hoffman, Kim S. Last, Arul Marie, Frank Melzner, Kati Michalek, James Morris, Deborah M. Power, Kirti Ramesh, Trystan SandersKirsikka Sillanpää, Victoria A. Sleight, Phoebe J. Stewart‐sinclair, Kristina Sundell, Luca Telesca, David L. J. Vendrami, Alexander Ventura, Thomas A. Wilding, Tejaswi Yarra, Elizabeth M. Harper

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Abstract

Most molluscs possess shells, constructed from a vast array of microstructures and architectures. The fully formed shell is composed of calcite or aragonite. These CaCO3 crystals form complex biocomposites with proteins, which although typically less than 5% of total shell mass, play significant roles in determining shell microstructure. Despite much research effort, large knowledge gaps remain in how molluscs construct and maintain their shells, and how they produce such a great diversity of forms. Here we synthesize results on how shell shape, microstructure, composition and organic content vary among, and within, species in response to numerous biotic and abiotic factors. At the local level, temperature, food supply and predation cues significantly affect shell morphology, whilst salinity has a much stronger influence across latitudes. Moreover, we emphasize how advances in genomic technologies [e.g. restriction site‐associated DNA sequencing (RAD‐Seq) and epigenetics] allow detailed examinations of whether morphological changes result from phenotypic plasticity or genetic adaptation, or a combination of these. RAD‐Seq has already identified single nucleotide polymorphisms associated with temperature and aquaculture practices, whilst epigenetic processes have been shown significantly to modify shell construction to local conditions in, for example, Antarctica and New Zealand. We also synthesize results on the costs of shell construction and explore how these affect energetic trade‐offs in animal metabolism. The cellular costs are still debated, with CaCO3 precipitation estimates ranging from 1–2 J/mg to 17–55 J/mg depending on experimental and environmental conditions. However, organic components are more expensive (~29 J/mg) and recent data indicate transmembrane calcium ion transporters can involve considerable costs. This review emphasizes the role that molecular analyses have played in demonstrating multiple evolutionary origins of biomineralization genes. Although these are characterized by lineage‐specific proteins and unique combinations of co‐opted genes, a small set of protein domains have been identified as a conserved biomineralization tool box. We further highlight the use of sequence data sets in providing candidate genes for in situ localization and protein function studies. The former has elucidated gene expression modularity in mantle tissue, improving understanding of the diversity of shell morphology synthesis. RNA interference (RNAi) and clustered regularly interspersed short palindromic repeats ‐ CRISPR‐associated protein 9 (CRISPR‐Cas9) experiments have provided proof of concept for use in the functional investigation of mollusc gene sequences, showing for example that Pif (aragonite‐binding) protein plays a significant role in structured nacre crystal growth and that the Lsdia1 gene sets shell chirality in Lymnaea stagnalis . Much research has focused on the impacts of ocean acidification on molluscs. Initial studies were predominantly pessimistic for future molluscan biodiversity. However, more sophisticated experiments incorporating selective breeding and multiple generations are identifying subtle effects and that variability within mollusc genomes has potential for adaption to future conditions. Furthermore, we highlight recent historical studies based on museum collections that demonstrate a greater resilience of molluscs to climate change compared with experimental data. The future of mollusc research lies not solely with ecological investigations into biodiversity, and this review synthesizes knowledge across disciplines to understand biomineralization. It spans research ranging from evolution and development, through predictions of biodiversity prospects and future‐proofing of aquaculture to identifying new biomimetic opportunities and societal benefits from recycling shell products.
Original languageEnglish
Number of pages26
JournalBiological Reviews
DOIs
Publication statusPublished - 31 Jul 2020

Keywords

  • intergrative biomineralization
  • calcification
  • calcium
  • skeleton
  • adaption
  • phenotypic plasticity
  • ion channels
  • Crassostrea
  • Pinctada
  • Mytilus

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    Clark, M. S., Peck, L. S., Arivalagan, J., Backeljau, T., Berland, S., Cardoso, J. C. R., Caurcel, C., Chapelle, G., De Noia, M., Dupont, S., Gharbi, K., Hoffman, J. I., Last, K. S., Marie, A., Melzner, F., Michalek, K., Morris, J., Power, D. M., Ramesh, K., ... Harper, E. M. (2020). Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics. Biological Reviews. https://doi.org/10.1111/brv.12640