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

Abstract

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.

Chromosome‐level genome assembly of the razor clam Sinonovacula constricta (Lamarck, 1818)

“…The consensus gene set was 43,795 by merging the gene sets from ab initio methods ( Augustus , GenScan, GlimmerHMM , snap and Geneid ), homologous prediction from other species and RNA‐seq data (Table S7, cufflinks and PASA) using EvidenceModeler (Table ). Next, the gene models were filtered according to the following criteria: coding region length less than 150 bp, supported only by the ab initio method, and with expression value < five for single‐exon genes and expression value < one for multi‐exon genes (Li et al, ). After gene filtering, 28,594 protein‐coding genes with a mean of 7.34 exons per gene were retained and constituted the final gene set for S. constricta genome (Table , Table S8).…”

The evolution of molluscs

“…Thereby, the release of the genomes of various gastropods including the Pacific abalone Haliotis discus hannai (Nam et al, ), the freshwater snail Biomphalaria glabrata (Adema et al, ), and the basally branching owl limpet Lottia gigantea (Simakov et al, ) together with several bivalves [e.g. Crassostrea gigas (Thunberg, 1793) (Zhang et al, ), Patinopecten yessoensis (Jay, 1857) (Wang et al, ), and other scallop, oyster, and mussel species (Takeuchi et al, ; Du et al, ; Li et al, , ; Sun et al, )] and the California two‐spot octopus Octopus bimaculoides Pickford & McConnaughey, 1949 (Albertin et al, ) provided an important framework for studies into key developmental regulators such as Hox and ParaHox genes as well as signalling molecules involved in dorso‐ventral axis patterning (bone morphogenetic protein (BMP)/decapentaplegic (Dpp) pathway) and left/right determination (Nodal pathway).…”

“…Quantitative expression analyses of Crassostrea gigas stages are in line with the split Hox cluster insofar as no temporal correlation was found between expression of a given Hox gene in a certain ontogenetic stage and its relative position to other Hox genes on the genome (Zhang et al, ). However, in two other bivalves, the scallops Patinopecten yessoensis and Chlamys farreri , the Hox genes do appear to form a true cluster (Li et al, ; Wang et al, ). While precise tempo‐spatial expression analyses of Hox genes spanning entire embryonic and larval development are still lacking, transcript localization in gastrulae of Patinopecten yessoensis suggests some degree of staggered expression of four Hox genes ( Hox1 , Hox4 , Lox5 , Post2 ) in this stage, and quantitative analyses revealed staggered temporal expression of individual Hox genes within four (virtual) Patinopecten yessoensis subclusters (Wang et al, ).…”

“…Recent advances in palaeontological, phylogenetic, developmental, and experimental approaches have revealed some of the mysteries revolving around the emergence of the large phenotypic diversity encountered in modern and fossil species. The recent establishment of genomic editing tools such as the CRISPR/Cas (clustered regularly interspaced short palindromic repeats/clustered regularly interspaced short palindromic repeats‐associated protein) system in molluscs (Perry & Henry, ), together with the ever‐increasing genomic (Zhang et al, ; Simakov et al, ; Albertin et al, ; Li et al, ; Wang et al, ) and transcriptomic resources (De Oliveira et al, ; Li et al, ), provide an ideal base to finally pursue questions concerned with molluscan functional genetics. To this end, some molluscan species have already been demonstrated to be particularly amenable to becoming true laboratory models, including the gastropods Ilyanassa obsoleta (Goulding & Lambert, ) and Crepidula fornicata (Henry & Lyons, ).…”

The Gene-Rich Genome of the ScallopPecten maximus

“…At the time of writing, nine bivalve genomes are available, with those of the Pacific oyster Crassostrea gigas [15] and the pearl oyster Pinctada fucata [16] in particular having been used for a variety of investigations into bivalve biology. Scallops have been the subject of genome sequencing projects in the past, with genomes published for three species, Azumapecten farreri (as Chlamys [17]) and Mizuhopecten yessoensis (as Patinopecten; [18]) from the subfamily Pedinae, and Argopecten purpuratus from the subfamily Pectininae [19]. Other sequenced genomes for more distantly related bivalves include those of the Sydney Rock Oyster Saccostrea glomerata [20], Eastern oyster Crassostrea virginica [unpublished, but see 21], the Snout Otter Clam Lutraria rhynchaena [22], Blood Clam Scapharca broughtonii [23] and Manila Clam Ruditapes philippinarum [24].…”