Structural and functional analyses of calcium ion response factors in the mantle of Pinctada fucata

Matsuura, Akihiro; Yoshimura, Ko; Kintsu, Hiroyuki; Atsumi, Takashi; Tsuchihashi, Yasushi; Takeuchi, Takeshi; Satoh, Noriyuki; Negishi, Lumi; Sakuda, Shohei; Asakura, Tomiko; Imura, Yoshimi; Yoshimura, Etsuro; Suzuki, Michio

doi:10.1016/j.jsb.2018.08.014

Cited by 7 publications

(4 citation statements)

References 41 publications

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“…Although the ORF was only detected in the EcMPs of A. hians , a contig (DN73320_c0_g1_i1_fr4) matching the first half of the 123 amino acids (99%) and a contig (DN41781_c0_g1_i1_fr1) matching the second half of the 82 amino acids (98%) were obtained from the transcriptome of A. argo . Although in this study we only found homologous sequences with a similar domain structure in Pinctada fucata (Matsuura et al 2018), the presence of the Pif-like/Laminin G3 protein in the shell matrix were also reported from the nautilus (Setiamarga et al 2020), a pectinid bivalve Argopecten purpuratus (Li et al 2018), and the pond snail Lymnaea stagnalis (Ishikawa et al 2020).…”

Section: Resultsmentioning

confidence: 66%

Independent adoptions of a set of proteins found in the matrix of the mineralized shell-like eggcase of Argonaut octopuses

Setiamarga

Hirota

Ikai

et al. 2021

Preprint

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The Argonaut octopus, commonly called the paper nautilus, has a spiral-coiled shell-like eggcase. As the main characteristics, the eggcase has no internal septum, is composed entirely of calcite with chitosan being the main polycarbonate and is reportedly formed by organic materials secreted from the membranes of the arms. Meanwhile, the biomineralized external "true" shells of the Mollusks, which includes the Cephalopods, are secreted from the mantle tissue. Therefore, the histological origin of the two shells is completely different. The question of how the Argonauts, which phylogenetically diverged from the completely shell-less octopuses, could form a converging shell-like external structure has thus intrigued biologists for a long time. To answer this question, we performed a multi-omics analysis of the transcriptome and proteome of the two congeneric Argonaut species, Argonauta argo and A. hians. Our result indicates that the shell-like eggcase is not a homolog of the shell, even at the protein level, because the Argonauts apparently recruited a different set of protein repertoires to as eggcase matrix proteins (EcMPs). However, we also found the homologs of three shell matrix proteins (SMPs) of the Conchiferan Mollusks, Pif-like, SOD, and TRX, in the eggcase matrix. The proteins were also found in the only surviving shelled Cephalopods, the nautiloid Nautilus pompilius. Phylogenetic analysis revealed that homologous genes of the Conchiferan SMPs and EcMPs were found in the draft genome of shell-less octopuses. Our result reported here thus suggests that the SMP-coding genes are conserved in both shelled and shell-less Cephalopods. Meanwhile, the Argonauts adopted some of the SMP-coding genes and other non-SMP-coding genes, to form a convergent, non-homologous biomineralized external structure, the eggcase, which is autapomorphic to the group.

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Section: Resultsmentioning

confidence: 66%

Independent adoptions of a set of proteins found in the matrix of the mineralized shell-like eggcase of Argonaut octopuses

Setiamarga

Hirota

Ikai

et al. 2021

Preprint

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“…Cartilage matrix protein (CMP) is another predominant cartilage protein involved in calcium phosphate biomineralization in vertebrates [56]. Both dermatopontin (DPT) and filamin participate in nacre formation in molluscs, and are among the major components of shell matrix proteins [57]. Along with collagen, CMP, DPT and filamin were found to be specifically expanded in the genomes of shelled molluscs but not those of barnacles (figure 2 a ).…”

Section: Resultsmentioning

confidence: 99%

Convergent evolution of barnacles and molluscs sheds lights in origin and diversification of calcareous shell and sessile lifestyle

Yuan

Zhang

et al. 2022

Proc. R. Soc. B.

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The calcareous shell and sessile lifestyle are the representative phenotypes of many molluscs, which happen to be present in barnacles, a group of unique crustaceans. The origin of these phenotypes is unclear, but it may be embodied in the convergent genetics of such distant groups (interphylum). Herein, we perform comprehensive comparative genomics analysis in barnacles and molluscs, and reveal a genome-wide strong convergent molecular evolution between them, including coexpansion of biomineralization and organic matrix genes for shell formation, and origination of lineage-specific orphan genes for settlement. Notably, the expanded biomineralization gene encoding alkaline phosphatase evolves a novel, highly conserved motif that may trigger the origin of barnacle shell formation. Unlike molluscs, barnacles adopt novel organic matrices and cement proteins for shell formation and settlement, respectively, and their calcareous shells have potentially originated from the cuticle system of crustaceans. Therefore, our study corroborates the idea that selection pressures driving convergent evolution may strongly act in organisms inhabiting similar environments regardless of phylogenetic distance. The convergence signatures shed light on the origin of the shell and sessile lifestyle of barnacles and molluscs. In addition, notable non-convergence signatures are also present and may contribute to morphological and functional specificities.

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“…Recently, a filamin-like protein of P . fucata (pf-filamin-A) was reported as a calcium-sensing protein related to the synthesis and transportation of calcium-containing nanoparticles on the surface of the nacreous layer [63], indicating an important role for filamin in biomineralization. The presence of these abundant matrix proteins in both the nacre and myostracum layers of the P .…”

Section: Discussionmentioning

confidence: 99%

Microstructure and in-depth proteomic analysis of Perna viridis shell

et al. 2019

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For understanding the structural characteristics and the proteome of Perna shell, the microstructure, polymorph, and protein composition of the adult Perna viridis shell were investigated. The P . viridis shell have two distinct mineral layers, myostracum and nacre, with the same calcium carbonate polymorph of aragonite, determined by scanning electron microscope, Fourier transform infrared spectroscopy, and x-ray crystalline diffraction. Using Illumina sequencing, the mantle transcriptome of P . viridis was investigated and a total of 69,859 unigenes was generated. Using a combined proteomic/transcriptomic approach, a total of 378 shell proteins from P . viridis shell were identified, in which, 132 shell proteins identified with more than two matched unique peptides. Of the 132 shell proteins, 69 are exclusive to the nacre, 12 to the myostracum, and 51 are shared by both. The Myosin-tail domain containing proteins, Filament-like proteins, and Chitin-binding domain containing proteins represent the most abundant molecules. In addition, the shell matrix proteins (SMPs) containing biomineralization-related domains, such as Kunitz, A2M, WAP, EF-hand, PDZ, VWA, Collagen domain, and low complexity regions with abundant certain amino acids, were also identified from P . viridis shell. Collagenase and chitinase degradation can significantly change the morphology of the shell, indicating the important roles of collagen and chitin in the shell formation and the muscle-shell attachment. Our results present for the first time the proteome of P . viridis shell and increase the knowledge of SMPs in this genus.

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Structural and functional analyses of calcium ion response factors in the mantle of Pinctada fucata

Cited by 7 publications

References 41 publications

Independent adoptions of a set of proteins found in the matrix of the mineralized shell-like eggcase of Argonaut octopuses

Independent adoptions of a set of proteins found in the matrix of the mineralized shell-like eggcase of Argonaut octopuses

Convergent evolution of barnacles and molluscs sheds lights in origin and diversification of calcareous shell and sessile lifestyle

Microstructure and in-depth proteomic analysis of Perna viridis shell

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