Functional shell matrix proteins tentatively identified by asymmetric snail shell morphology

Ishikawa, Akito; Shimizu, Keisuke; Isowa, Yukinobu; Takeuchi, Takeshi; Zhao, Rongjun; Kito, Keiji; Fujie, Manabu; Satoh, Noriyuki; Endo, Kazuhiko

doi:10.1038/s41598-020-66021-w

“…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: 68%

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

Setiamarga

¹

,

Hirota

²

,

Ikai

³

et al. 2021

Preprint

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5

1

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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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“…8 A , Supplementary Material online, clade labeled PIF). The second homolog of Pif in the A. granulata genome, g24110, codes for a protein that is “PIF-like.” A “PIF-like” protein in Lymnaea stagnalis is associated with shell biomineralization ( Ishikawa et al. 2020 ).…”

Section: Resultsmentioning

confidence: 99%

The Iron-Responsive Genome of the Chiton Acanthopleura granulata

Varney

¹

,

Speiser

²

,

McDougall

³

et al. 2020

Genome Biology and Evolution

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Molluscs biomineralize structures that vary in composition, form, and function, prompting questions about the genetic mechanisms responsible for their production and the evolution of these mechanisms. Chitons (Mollusca, Polyplacophora) are a promising system for studies of biomineralization because they build a range of calcified structures including shell plates and spine- or scale-like sclerites. Chitons also harden the calcified teeth of their rasp-like radula with a coat of iron (as magnetite). Here we present the genome of the West Indian fuzzy chiton Acanthopleura granulata, the first from any aculiferan mollusc. The A. granulata genome contains homologs of many genes associated with biomineralization in conchiferan molluscs. We expected chitons to lack genes previously identified from pathways conchiferans use to make biominerals like calcite and nacre because chitons do not use these materials in their shells. Surprisingly, the A. granulata genome has homologs of many of these genes, suggesting that the ancestral mollusc may have had a more diverse biomineralization toolkit than expected. The A. granulata genome has features that may be specialized for iron biomineralization, including a higher proportion of genes regulated directly by iron than other molluscs. A. granulata also produces two isoforms of soma-like ferritin: one is regulated by iron and similar in sequence to the soma-like ferritins of other molluscs, and the other is constitutively translated and is not found in other molluscs. The A. granulata genome is a resource for future studies of molluscan evolution and biomineralization.

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“…These peptides have different roles in biomineralization: PIF80 binds nacre and aids in nacre formation (Suzuki et al 2009), whereas PIF97 binds to chitin and guides the growth of calcium carbonate crystals (Suzuki et al 2013). A recent study in the gastropod Lymnaea stagnalis identified a PIF-like protein that does not promote nacre production, but is expressed in tissues that suggest this PIF protein still plays a role in shell biomineralization (Ishikawa et al 2020). We found that A. granulata possesses a Pif homolog, but appears to only produce PIF97 rather than two separate peptides.…”

Section: Resultsmentioning

confidence: 99%

The iron-responsive genome of the chitonAcanthopleura granulata

Varney

¹

,

Speiser

²

,

McDougall

³

et al. 2020

Preprint

View full text Add to dashboard Cite

Molluscs biomineralize structures that vary in composition, form, and function, prompting questions about the genetic mechanisms responsible for their production and the evolution of these mechanisms. Chitons (Mollusca, Polyplacophora) are a promising system for studies of biomineralization because they build a range of calcified structures including shell plates and spine- or scale-like sclerites. Chitons also harden the teeth of their rasp-like radula with a coat of iron. Here we present the genome of the West Indian fuzzy chiton Acanthopleura granulata, the first from any aculiferan mollusc. The A. granulata genome has features that may be specialized for iron biomineralization, including a high proportion of genes regulated directly by iron and two isoforms of ferritin, one iron-regulated and the other constitutively translated. The A. granulata genome also contains homologs of many biomineralization genes identified previously in conchiferan molluscs, suggesting the ancestral mollusc had a diverse genetic toolkit for biomineralization.

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Functional shell matrix proteins tentatively identified by asymmetric snail shell morphology

Cited by 13 publications

References 55 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

The Iron-Responsive Genome of the Chiton Acanthopleura granulata

The iron-responsive genome of the chitonAcanthopleura granulata

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