Phylogenetic comparisons reveal mosaic histories of larval and adult shell matrix protein deployment in pteriomorph bivalves

Ran Zhao,Yuqi Che,Noriyuki Satoh,Shunsuke Iwanaga,Akito Ishikawa,Alejandro Villar-Briones,Kazuyoshi Endo,Ryo Koyanagi,Takeshi Takeuchi,Hitoshi Sawada,Lixy Yamada,Kiyohito Nagai

doi:10.1038/s41598-020-79330-x

Abstract

Molluscan shells are organo-mineral composites, in which the dominant calcium carbonate is intimately associated with an organic matrix comprised mainly of proteins and polysaccharides. However, whether the various shell matrix proteins (SMPs) date to the origin of hard skeletons in the Cambrian, or whether they represent later deployment through adaptive evolution, is still debated. In order to address this issue and to better understand the origins and evolution of biomineralization, phylogenetic analyses have been performed on the three SMP families, Von Willebrand factor type A (VWA) and chitin-binding domain-containing protein (VWA-CB dcp), chitobiase, and carbonic anhydrase (CA), which exist in both larval and adult shell proteomes in the bivalves, Crassostrea gigas and Pinctada fucata. In VWA-CB dcp and chitobiase, paralogs for larval and adult SMPs evolved before the divergence of these species. CA-SMPs have been taken as evidence for ancient origins of SMPs by their presumed indispensable function in biomineralization and ubiquitous distribution in molluscs. However, our results indicate gene duplications that gave rise to separate deployments as larval and adult CA-SMPs occurred independently in each lineage after their divergence, which is considerably more recent than hitherto assumed, supporting the “recent heritage and fast evolution” scenario for SMP evolution.

Highlights

Molluscan shells are organo-mineral composites, in which the dominant calcium carbonate is intimately associated with an organic matrix comprised mainly of proteins and polysaccharides
According to a genome-wide survey based on the InterProScan online database (Supplementary table S1), as well as our proteomic work, proteins possessing both Von Willebrand factor type A (VWA) and CB domains appeared in the common ancestor of Mollusca and closely-related lophotrochozoans including the Nemertea, Phoronida, and Brachiopoda
As molluscan shell matrix proteins (SMPs), VWA-CB dcps have been reported from the shells of Mytilus galloprovincialis[36], Lottia gigantea[9,37] and in both the larval and adult shells of Crassostrea gigas and Pinctada fucata[13,38,39]

Summary

Introduction

Molluscan shells are organo-mineral composites, in which the dominant calcium carbonate is intimately associated with an organic matrix comprised mainly of proteins and polysaccharides. Calcium carbonate shells of the Mollusca provide exceptional resources for studying the processes of biomineralization due to their tremendously varied morphologies[4], as well as a huge diversity of special microstructures, characteristic of each s pecies[5,6]. Despite this complexity, adult molluscan shells are secreted by an evolutionarily homologous organ known as the mantle[7,8], and different aspects of the shell formation processes are controlled by the organic molecules collectively known as the shell matrix. Carbonic anhydrase domains have been found in both bivalves and gastropods, so it is impossible that such a key function resulted from recent r ecruitment[14]

Methods

Results

Discussion

Conclusion