Bivalve molluscs are descendants of an early-Cambrian lineage superbly adapted to benthic filter feeding. Adaptations in form and behavior are well recognized, but the underlying molecular mechanisms are largely unknown. Here, we investigate the genome, various transcriptomes, and proteomes of the scallop Chlamys farreri, a semi-sessile bivalve with well-developed adductor muscle, sophisticated eyes, and remarkable neurotoxin resistance. The scallop's large striated muscle is energy-dynamic but not fully differentiated from smooth muscle. Its eyes are supported by highly diverse, intronless opsins expanded by retroposition for broadened spectral sensitivity. Rapid byssal secretion is enabled by a specialized foot and multiple proteins including expanded tyrosinases. The scallop uses hepatopancreas to accumulate neurotoxins and kidney to transform to high-toxicity forms through expanded sulfotransferases, probably as deterrence against predation, while it achieves neurotoxin resistance through point mutations in sodium channels. These findings suggest that expansion and mutation of those genes may have profound effects on scallop's phenotype and adaptation.

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Scallop genome reveals molecular adaptations to semi-sessile life and neurotoxins

Molluscs are extremely diverse invertebrate animals with a rich fossil record, highly divergent life cycles, and considerable economical and ecological importance. Key representatives include worm-like aplacophorans, armoured groups (e.g. polyplacophorans, gastropods, bivalves) and the highly complex cephalopods. Molluscan origins and evolution of their different phenotypes have largely remained unresolved, but significant progress has been made over recent years. Phylogenomic studies revealed a dichotomy of the phylum, resulting in Aculifera (shell-less aplacophorans and multi-shelled polyplacophorans) and Conchifera (all other, primarily uni-shelled groups). This challenged traditional hypotheses that proposed that molluscs gradually evolved complex phenotypes from simple, worm-like animals, a view that is corroborated by developmental studies that showed that aplacophorans are secondarily simplified. Gene expression data indicate that key regulators involved in anterior-posterior patterning (the homeobox-containing Hox genes) lost this function and were co-opted into the evolution of taxon-specific novelties in conchiferans. While the bone morphogenetic protein (BMP)/decapentaplegic (Dpp) signalling pathway, that mediates dorso-ventral axis formation, and molecular components that establish chirality appear to be more conserved between molluscs and other metazoans, variations from the common scheme occur within molluscan sublineages. The deviation of various molluscs from developmental pathways that otherwise appear widely conserved among metazoans provides novel hypotheses on molluscan evolution that can be tested with genome editing tools such as the CRISPR/Cas9 (clustered regularly interspaced short palindromic repeats/clustered regularly interspaced short palindromic repeats-associated protein9) system.

The evolution of molluscs

The Mediterranean mussel Mytilus galloprovincialis is an ecologically and economically relevant edible marine bivalve, highly invasive and resilient to biotic and abiotic stressors causing recurrent massive mortalities in other bivalves. Although these traits have been recently linked with the maintenance of a high genetic variation within natural populations, the factors underlying the evolutionary success of this species remain unclear. Here, after the assembly of a 1.28-Gb reference genome and the resequencing of 14 individuals from two independent populations, we reveal a complex pan-genomic architecture in M. galloprovincialis, with a core set of 45,000 genes plus a strikingly high number of dispensable genes (20,000) subject to presence-absence variation, which may be entirely missing in several individuals. We show that dispensable genes are associated with hemizygous genomic regions affected by structural variants, which overall account for nearly 580 Mb of DNA sequence not included in the reference genome assembly. As such, this is the first study to report the widespread occurrence of gene presence-absence variation at a whole-genome scale in the animal kingdom. Dispensable genes usually belong to young and recently expanded gene families enriched in survival functions, which might be the key to explain the resilience and invasiveness of this species. This unique pan-genome architecture is characterized by dispensable genes in accessory genomic regions that exceed by orders of magnitude those observed in other metazoans, including humans, and closely mirror the open pan-genomes found in prokaryotes and in a few non-metazoan eukaryotes.

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Massive gene presence-absence variation shapes an open pan-genome in the Mediterranean mussel.

The study of molluscan immune systems, in particular those of bivalve molluscs (e.g., clams, oysters, scallops, mussels), has experienced great growth in recent decades, mainly due to the needs of a rapidly growing aquaculture industry to manage the impacts of disease and the wider application of -omic tools to this diverse group of invertebrate organisms. Several unique aspects of molluscan immune systems highlighted in this chapter include the importance of feeding behavior and mucosal immunity, the discovery of unique levels of diversity in immune genes, and experimental indication of transgenerational immune priming. The development of comparative functional studies using natural and selectively bred disease-resistant strains, together with the potential but yet to be fully developed application of gene-editing technologies, should provide exciting insights into the functional relevance of immune gene family expansion and molecular diversification in bivalves. Other areas of bivalve immunity that deserve further study include elucidation of the process of hematopoiesis, the full characterization of hemocyte subpopulations, and the genetic and molecular mechanisms underlying immune priming. While the most important aspects of the immune system of the largest group of molluscs, gastropods (e.g., snails and slugs), are discussed in detail in Chap. 12, we also briefly outline the most distinctive features of the immune system of another fascinating group of marine molluscs, cephalopods, which include invertebrate animals with extraordinary morphological and behavioral complexity.

/pdf/immunity-in-molluscs-recognition-and-effector-mechanisms-2kyp04l89s.pdf

Immunity in Molluscs: Recognition and Effector Mechanisms, with a Focus on Bivalvia

Research advances in the genomics and applications for molecular breeding of aquaculture animals

Nacre, the iridescent material found in pearls and shells of molluscs, is formed through an extraordinary process of matrix-assisted biomineralization. Despite recent advances, many aspects of the biomineralization process and its evolutionary origin remain unknown. The pearl oyster Pinctada fucata martensii is a well-known master of biomineralization, but the molecular mechanisms that underlie its production of shells and pearls are not fully understood. We sequenced the highly polymorphic genome of the pearl oyster and conducted multi-omic and biochemical studies to probe nacre formation. We identified a large set of novel proteins participating in matrix-framework formation, many in expanded families, including components similar to that found in vertebrate bones such as collagen-related VWA-containing proteins, chondroitin sulfotransferases, and regulatory elements. Considering that there are only collagen-based matrices in vertebrate bones and chitin-based matrices in most invertebrate skeletons, the presence of both chitin and elements of collagen-based matrices in nacre suggests that elements of chitin- and collagen-based matrices have deep roots and might be part of an ancient biomineralizing matrix. Our results expand the current shell matrix-framework model and provide new insights into the evolution of diverse biomineralization systems.

The pearl oyster Pinctada fucata martensii genome and multi-omic analyses provide insights into biomineralization.

This study investigated the capability for fin regeneration in zebrafish larvae with the mechanism of FCS isolated from green and purple sea cucumbers Apostichopus japonicus (G-FCS and P-FCS). HPGPC determined that mean molecular weight of purified G-FCS and P-FCS is 19.5 and 18.8 kDa, and the FT-IR spectrum displayed similar characteristic absorption peaks. AFM images presented that G-FCS was shown as a spherical polysaccharide, while P-FCS molecules exhibited elongated chains. For the regeneration examination, FCS increased the regrowth area of the larval fin at 48 hours postamputation with enhanced locomotor behaviors, and the transcription levels of regeneration-related genes (Wnt10a, msx1b, fgf20a, bmp2a, bmp4, and igf2b) were upregulated. Moreover, FCS promoted the mRNA expression of inflammatory factors (iNOS, TNF-α, IL-6, IL-10, and IFN-γ) and TLR/NF-κB pathway-related genes (TLR3, TLR4a, NF-κb, and MyD88). The Western blot analyses of TNF-α and IL-1β supported that FCS enhanced immune response. ELISA results indicated that FCSs increased the contents of NO, CAT, SOD, and G6PD. Summarily, the present results suggested that FCS was a potential regeneration enhancer by elevating immunomodulatory and antioxidative processes in zebrafish.

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The Fin-Improving Effects of Fucosylated Chondroitin Sulfate from Green and Purple Apostichopus japonicus on Caudal Fin Regeneration of Zebrafish Larvae

Jialiang Liu

Papers

The pearl oyster Pinctada fucata martensii genome and multi-omic analyses provide insights into biomineralization.

The Fin-Improving Effects of Fucosylated Chondroitin Sulfate from Green and Purple Apostichopus japonicus on Caudal Fin Regeneration of Zebrafish Larvae