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Spatial-temporal expression analysis of lineage-restricted shell matrix proteins in the slipper snail Crepidula atrasolea reveals shell field regionalization and distinct cell populations

Lopez-Anido, Rebecca1; Batzel, Grant1; Ramirez, Gabriela1; Wang, Yiqun1; Neal, Stephanie1; Lesoway, Maryna1; Goodheart, Jessica2; Lyons, Deirdre1

Published May 31, 2024 on Dryad. https://doi.org/10.5061/dryad.zpc866tf1

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Abstract

Mollusca is a morphologically diverse metazoan phylum, exhibiting an immense variety of calcium carbonate shells. Biomineralization of the shell involves shell matrix proteins (SMPs). While SMP diversity is hypothesized to drive molluscan shell diversity, we are just starting to unravel SMP evolutionary history and biology. Here we leveraged two complementary molluscan model systems, the marine slipper snails Crepidula fornicata and Crepidula atrasolea, to determine the evolutionary lineage of 185 Crepidula SMPs. We found that 95% of the adult C. fornicata shell proteome belongs to conserved metazoan and molluscan orthogroups, with molluscan-restricted orthogroups containing half of all SMPs in the shell proteome. The low number of C. fornicata-restricted SMPs contradicts the generally-held notion that an animal’s biomineralization toolkit is dominated by mostly novel genes. Next, we selected a subset of SMPs across evolutionary lineages for spatial-temporal analysis using in situ hybridization chain reaction (HCR) during shell development in C. atrasolea. We found that 12 out of the 18 SMPs we analyzed are expressed in the shell tissue. These transcripts are present in 5 expression patterns, which define at least three distinct cell populations within the shell field. These results represent the most comprehensive analysis of gastropod SMP evolutionary age and shell field expression patterns to date. Collectively, these data lay the foundation for future work to interrogate the molecular mechanisms and cell fate decisions underlying molluscan mantle specification and diversification.