Potential trade-offs between biomineralization and immunity revealed by shell properties and gene expression profiles of two closely related <i>Crassostrea</i> species

Ivanina, Anna V.; Borah, Ballav Moni; Vogts, Angela; Malik, Ifra; Wu, Jingyao; Chin, Adam R.; Almarza, Alejandro J.; Kumta, Prashant N.; Piontkivska, Helen; Beniash, Elia; Sokolova, Inna M.

doi:10.1242/jeb.183236

Cited by 16 publications

(30 citation statements)

References 72 publications

(109 reference statements)

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“…The calcium carbonate shell is predominantly laid down onto the periostracum by the epithelium of the outer mantle epithelium (Harper, 1997). We still have a poor knowledge of how calcium is mobilized within the animal to reach these specialized cells; however, in some species, such as Crassostrea, there is evidence to suggest that haemocytes may be involved, but this mechanism is not necessarily universal (Ivanina et al, 2018). Within outer mantle epithelial cells, experiments have demonstrated the active involvement of ion transporters in secreting calcium into the extra pallial space (Fig.…”

Section: Box 1 the Ecological And Socio-economic Benefits Of Calcifimentioning

confidence: 99%

Molecular mechanisms of biomineralization in marine invertebrates

Clark

2020

Journal of Experimental Biology

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Much recent marine research has been directed towards understanding the effects of anthropogenic-induced environmental change on marine biodiversity, particularly for those animals with heavily calcified exoskeletons, such as corals, molluscs and urchins. This is because life in our oceans is becoming more challenging for these animals with changes in temperature, pH and salinity. In the future, it will be more energetically expensive to make marine skeletons and the increasingly corrosive conditions in seawater are expected to result in the dissolution of these external skeletons. However, initial predictions of wide-scale sensitivity are changing as we understand more about the mechanisms underpinning skeletal production (biomineralization). These studies demonstrate the complexity of calcification pathways and the cellular responses of animals to these altered conditions. Factors including parental conditioning, phenotypic plasticity and epigenetics can significantly impact the production of skeletons and thus future population success. This understanding is paralleled by an increase in our knowledge of the genes and proteins involved in biomineralization, particularly in some phyla, such as urchins, molluscs and corals. This Review will provide a broad overview of our current understanding of the factors affecting skeletal production in marine invertebrates. It will focus on the molecular mechanisms underpinning biomineralization and how knowledge of these processes affects experimental design and our ability to predict responses to climate change. Understanding marine biomineralization has many tangible benefits in our changing world, including improvements in conservation and aquaculture and exploitation of natural calcified structure design using biomimicry approaches that are aimed at producing novel biocomposites.

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Section: Box 1 the Ecological And Socio-economic Benefits Of Calcifimentioning

confidence: 99%

Molecular mechanisms of biomineralization in marine invertebrates

Clark

2020

Journal of Experimental Biology

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“…Though the mantle tissue of mollusk is primarily responsible for shell biomineralization, it has also been reported that oyster hemocytes can mediate shell biomineralization by binding calcium ion as well as forming CaCO 3 crystals [101–103]. More recently, some studies also concluded that in addition to mineral transportation, hemocytes contribute to the secretion of the extracellular matrix required for shell biomineralization in bivalve [104, 105]. Therefore, the interaction between the epithelial cells of donor mantle and host hemocytes is very essential for the proper development of pearl sac and pearl [38].…”

Section: Discussionmentioning

confidence: 99%

Gene expression profiles at different stages for formation of pearl sac and pearl in the pearl oyster Pinctada fucata

et al. 2019

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BackgroundThe most critical step in the pearl formation during aquaculture is issued to the proliferation and differentiation of outer epithelial cells of mantle graft into pearl sac. This pearl sac secretes various matrix proteins to produce pearls by a complex physiological process which has not been well-understood yet. Here, we aimed to unravel the genes involved in the development of pearl sac and pearl, and the sequential expression patterns of different shell matrix proteins secreted from the pearl sac during pearl formation by pearl oyster Pinctada fucata using high-throughput transcriptome profiling.ResultsPrincipal component analysis (PCA) showed clearly different gene expression profiles between earlier (before 1 week) and later stages (1 week to 3 months) of grafting. Immune-related genes were highly expressed between 0 h – 24 h (donor dependent) and 48 h – 1 w (host dependent), and in the course of wound healing process pearl sac was developed by two weeks of graft transplantation. Moreover, for the first time, we identified some stem cell marker genes including ABCG2, SOX2, MEF2A, HES1, MET, NRP1, ESR1, STAT6, PAX2, FZD1 and PROM1 that were expressed differentially during the formation of pearl sac. The expression profiling of 192 biomineralization-related genes demonstrated that most of the shell matrix proteins (SMPs) involved in prismatic layer formation were first up-regulated and then gradually down-regulated indicating their involvement in the development of pearl sac and the onset of pearl mineralization. Most of the nacreous layer forming SMPs were up-regulated at 2 weeks after the maturation of pearl sac. Nacrein, MSI7 and shematrin involved in both layer formation were highly expressed during 0 h – 24 h, down-regulated up to 1 week and then up-regulated again after accomplishment of pearl sac formation.ConclusionsUsing an RNA-seq approach we unraveled the expression pattern of the key genes involved in the development of pearl sac and pearl as a result of host immune response after grafting. These findings provide valuable information in understanding the molecular mechanism of pearl formation and immune response in P. fucata.Electronic supplementary materialThe online version of this article (10.1186/s12864-019-5579-3) contains supplementary material, which is available to authorized users.

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“…For example, it has been proposed that haemocytes, found in the open circulatory system of molluscs, may play an active role during shell formation by carrying amorphous calcium, calcium crystals or SMPs to the site of shell formation [ 11 – 13 ]. However, the involvement of haemocytes in mollusc biomineralization may be species-specific, as they were associated with immune processes in Crastostrea gigas , but with ion regulation and calcium transport in C. virginica [ 14 ]. While in vivo and in vitro experiments have identified SMPs as integral to shell production, the molecular players in other shell formation processes such as the uptake, mobilisation and storage of calcium and bicarbonate ions, are unclear [ 15 ].…”

Section: Backgroundkmentioning

confidence: 99%

Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis

et al. 2021

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Background Biomineralization by molluscs involves regulated deposition of calcium carbonate crystals within a protein framework to produce complex biocomposite structures. Effective biomineralization is a key trait for aquaculture, and animal resilience under future climate change. While many enzymes and structural proteins have been identified from the shell and in mantle tissue, understanding biomieralization is impeded by a lack of fundamental knowledge of the genes and pathways involved. In adult bivalves, shells are secreted by the mantle tissue during growth, maintenance and repair, with the repair process, in particular, amenable to experimental dissection at the transcriptomic level in individual animals. Results Gene expression dynamics were explored in the adult blue mussel, Mytilus edulis, during experimentally induced shell repair, using the two valves of each animal as a matched treatment-control pair. Gene expression was assessed using high-resolution RNA-Seq against a de novo assembled database of functionally annotated transcripts. A large number of differentially expressed transcripts were identified in the repair process. Analysis focused on genes encoding proteins and domains identified in shell biology, using a new database of proteins and domains previously implicated in biomineralization in mussels and other molluscs. The genes implicated in repair included many otherwise novel transcripts that encoded proteins with domains found in other shell matrix proteins, as well as genes previously associated with primary shell formation in larvae. Genes with roles in intracellular signalling and maintenance of membrane resting potential were among the loci implicated in the repair process. While haemocytes have been proposed to be actively involved in repair, no evidence was found for this in the M. edulis data. Conclusions The shell repair experimental model and a newly developed shell protein domain database efficiently identified transcripts involved in M. edulis shell production. In particular, the matched pair analysis allowed factoring out of much of the inherent high level of variability between individual mussels. This snapshot of the damage repair process identified a large number of genes putatively involved in biomineralization from initial signalling, through calcium mobilization to shell construction, providing many novel transcripts for future in-depth functional analyses.

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Potential trade-offs between biomineralization and immunity revealed by shell properties and gene expression profiles of two closely related Crassostrea species

Cited by 16 publications

References 72 publications

Molecular mechanisms of biomineralization in marine invertebrates

Molecular mechanisms of biomineralization in marine invertebrates

Gene expression profiles at different stages for formation of pearl sac and pearl in the pearl oyster Pinctada fucata

Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis

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