Dataset Information

Mantle transcriptome sequencing of Mytilus spp. and identification of putative biomineralization genes.

ABSTRACT: In molluscs, the shell secreted by mantle tissue during the biomineralization process is the first barrier against predators and mechanical damage. Changing environmental conditions, such as ocean acidification, influence shell strength and thus protection of the soft body within. Mussels are marine bivalves with important commercial and ecological value worldwide. Despite this importance, the proteins involved in the biomineralization and pigmentation processes in Mytilus spp. remain unclear, as does taxonomy of Mytilus taxa, though there have been many molecular studies. To further understanding in these areas, this study aimed to characterize and compare mantle transcriptomes of four mussel taxa using next generation sequencing. Mussels representing four taxa, were collected from several localities and RNA from mantle tissue was extracted. RNA sequences obtained were assembled, annotated and potential molecular markers, including simple sequence repeats (SSRs) and single nucleotide polymorphisms (SNPs) were identified. Candidate contigs putatively related to biomineralization and pigmentation processes were then selected and several transcripts were chosen for phylogenetic analyses from the Bivalvia class. Transcriptome comparisons between Mytilus taxa, including gene ontology (GO) enrichment analysis and orthologues identification were performed. Of assembled contigs, 46.57%, 37.28% and 17.53% were annotated using NCBI NR, GO and Kyoto Encyclopedia of Genes and Genomes databases, respectively. Potential SSRs (483) and SNPs (1,497) were identified. Results presented a total of 1,292 contigs putatively involved in biomineralization and melanogenesis. Phylogenetic analyses of ?-carbonic anhydrase, chitinase and tyrosinase revealed complex evolutionary history and diversity of these genes, which may be a result of duplication events or adaptation to different environments in mussels and other bivalves. Enrichment analyses revealed GO terms associated with pH and thermal response in Mytilus edulis from the North Sea and M. galloprovincialis from the Mediterranean Sea. The phylogenetic analysis within the genus Mytilus revealed M. californianus and M. coruscus to be genetically more distant from the other taxa: M. trossulus, M. edulis, M. chilensis and M. galloprovincialis. This work represents the first mantle transcriptome comparison between Mytilus taxa and provides contigs putatively involved in biomineralization.

SUBMITTER: Malachowicz M

PROVIDER: S-EPMC6359903 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Mantle transcriptome sequencing of <i>Mytilus</i> spp. and identification of putative biomineralization genes.

Malachowicz Magdalena M Wenne Roman R

PeerJ 20190114

In molluscs, the shell secreted by mantle tissue during the biomineralization process is the first barrier against predators and mechanical damage. Changing environmental conditions, such as ocean acidification, influence shell strength and thus protection of the soft body within. Mussels are marine bivalves with important commercial and ecological value worldwide. Despite this importance, the proteins involved in the biomineralization and pigmentation processes in <i>Mytilus</i> spp. remain unc ...[more]

PMID: 30723611

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Project description:The Yesso scallop Patinopecten yessoensis is an economically important marine bivalve species in aquaculture and fishery in Asian countries. However, limited genomic resources are available for this scallop, which hampers investigations into molecular mechanisms underlying their unique biological characteristics, such as shell formation and pigmentation. Mantle is the special tissue of P. yessoensis that secretes biomineralization proteins inducing shell deposition as well as pigmentation on the shells. However, a current deficiency of transcriptome information limits insight into mechanisms of shell formation and pigmentation in this species. In this study, the transcriptome of the mantle of P. yessoensis was deeply sequenced and characterized using Illumina RNA-seq technology. A total of 86,521 unique transcripts are assembled from 55,884,122 reads that passed quality filters, and annotated, using Gene Ontology classification. A total of 259 pathways are identified in the mantle transcriptome, including the calcium signaling and melanogenesis pathways. A total of 237 unigenes that are homologous to 102 reported biomineralization genes are identified, and 121 unigenes that are homologous to 93 known proteins related to melanin biosynthesis are found. Twenty-three annotated unigenes, which are mainly homologous to calmodulin and related proteins, Ca2+/calmodulin-dependent protein kinase, adenylate/guanylate cyclase, and tyrosinase family are potentially involved in both biomineralization and melanin biosynthesis. It is suggested that these genes are probably not limited in function to induce shell deposition by calcium metabolism, but may also be involved in pigmentation of the shells of the scallop. This potentially supports the idea that there might be a link between calcium metabolism and melanin biosynthesis, which was previously found in vertebrates. The findings presented here will notably advance the understanding of the sophisticated processes of shell formation as well as shell pigmentation in P. yessoensis and other bivalve species, and also provide new evidence on gene expression for the understanding of pigmentation and biomineralization not only in invertebrates but also probably in vertebrates.

Project description:BACKGROUND: The shell of the pearl-producing bivalve Pinctada margaritifera is composed of an organic cell-free matrix that plays a key role in the dynamic process of biologically-controlled biomineralization. In order to increase genomic resources and identify shell matrix proteins implicated in biomineralization in P. margaritifera, high-throughput Expressed Sequence Tag (EST) pyrosequencing was undertaken on the calcifying mantle, combined with a proteomic analysis of the shell. RESULTS: We report the functional analysis of 276 738 sequences, leading to the constitution of an unprecedented catalog of 82 P. margaritifera biomineralization-related mantle protein sequences. Components of the current "chitin-silk fibroin gel-acidic macromolecule" model of biomineralization processes were found, in particular a homolog of a biomineralization protein (Pif-177) recently discovered in P. fucata. Among these sequences, we could show the localization of two other biomineralization protein transcripts, pmarg-aspein and pmarg-pearlin, in two distinct areas of the outer mantle epithelium, suggesting their implication in calcite and aragonite formation. Finally, by combining the EST approach with a proteomic mass spectrometry analysis of proteins isolated from the P. margaritifera shell organic matrix, we demonstrated the presence of 30 sequences containing almost all of the shell proteins that have been previously described from shell matrix protein analyses of the Pinctada genus. The integration of these two methods allowed the global composition of biomineralizing tissue and calcified structures to be examined in tandem for the first time. CONCLUSIONS: This EST study made on the calcifying tissue of P. margaritifera is the first description of pyrosequencing on a pearl-producing bivalve species. Our results provide direct evidence that our EST data set covers most of the diversity of the matrix protein of P. margaritifera shell, but also that the mantle transcripts encode proteins present in P. margaritifera shell, hence demonstrating their implication in shell formation. Combining transcriptomic and proteomic approaches is therefore a powerful way to identify proteins involved in biomineralization. Data generated in this study supply the most comprehensive list of biomineralization-related sequences presently available among protostomian species, and represent a major breakthrough in the field of molluskan biomineralization.

Dataset Information

Mantle transcriptome sequencing of Mytilus spp. and identification of putative biomineralization genes.

Publications

Mantle transcriptome sequencing of <i>Mytilus</i> spp. and identification of putative biomineralization genes.

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