The gene-rich genome of the scallop Pecten maximus

Abstract

Background: The king scallop, Pecten maximus, is distributed in shallow waters along the Atlantic coast of Europe. It forms the basis of a valuable commercial fishery and plays a key role in coastal ecosystems and food webs. Like other filter feeding bivalves it can accumulate potent phytotoxins, to which it has evolved some immunity. The molecular origins of this immunity are of interest to evolutionary biologists, pharmaceutical companies, and fisheries management.

Findings: Here we report the genome assembly of this species, conducted as part of the Wellcome Sanger 25 Genomes Project. This genome was assembled from PacBio reads and scaffolded with 10X Chromium and Hi-C data. Its 3,983 scaffolds have an N50 of 44.8 Mb (longest scaffold 60.1 Mb), with 92% of the assembly sequence contained in 19 scaffolds, corresponding to the 19 chromosomes found in this species. The total assembly spans 918.3 Mb and is the best-scaffolded marine bivalve genome published to date, exhibiting 95.5% recovery of the metazoan BUSCO set. Gene annotation resulted in 67,741 gene models. Analysis of gene content revealed large numbers of gene duplicates, as previously seen in bivalves, with little gene loss, in comparison with the sequenced genomes of other marine bivalve species.

Conclusions: The genome assembly of P. maximus and its annotated gene set provide a high-quality platform for studies on such disparate topics as shell biomineralization, pigmentation, vision, and resistance to algal toxins. As a result of our findings we highlight the sodium channel gene Nav1, known to confer resistance to saxitoxin and tetrodotoxin, as a candidate for further studies investigating immunity to domoic acid.

Keywords: bivalve; domoic; genome; mollusc; neurotoxin; scallop.

Figure 1:

A, Photo of both valves of the shell of Pecten maximus, from the specimen sequenced in this work (NHMUK 20170376). B, Diagrammatic cladogram illustrating the phylogeny of the Bivalvia (after Gonzalez et al. [37]), showing the major sub-classes of Bivalvia and (boxed in yellow) the major divisions of the Pteriomorphia. Pecten maximus is a member of the superfamily Pectinoidea, which includes Pectinidae (scallops), Propeamussiidae (glass scallops), and Spondylidae (spiny oysters), and together with their close relatives (Anomioidea, jingle shells; Dimyoidea, dimyarian oysters; and Plicatuloidea, kittenpaw clams) these superfamilies form the order Pectinida. C, Distribution map of P. maximus, showing range (dark blue) of species across northern Europe and surroundings (map from simplemaps, distribution according to [2]).

Figure 2:

A, Genomescope2 [49] plot of the 21-mer k-mer content within the Pecten maximus genome. Models fitted and resulting estimates of genome size and read data as shown on figure. B, Base pair count by depth in PacBio data, determined using PBreads/Minimap2. C, Blobplot [50] of content of the P. maximus genome. Note that little-to-no contamination of the assembly can be observed, with the small amount of sequence annotated as non-metazoan mirroring the metazoan content in GC content and average coverage. Additional Blobplot plots and data, including those separated by phylum/superkingdom, can be found in Supplementary File 2. D, Hi-C contact map based on assembly created using 3D-DNA and Juicebox Assembly Tools (see [51] for an interactive version of this panel).

Figure 3:

A, Orthofinder 2 [82] ortholog analysis of 8 sequenced marine bivalve species. Pecten maximus results shown in green. B, Phylogeny of bivalves using available marine bivalve genomes (generated from ortholog groups by STAG and displayed in Figtree), with root placed at midpoint. Blue dots indicate nodal support (=1 at every node). Numbers on internal nodes represent ancestrally shared duplications at the point of diversification. Numbers on leaf nodes indicate duplication events occurring solely in that taxon. C, Matrix showing numbers of overlapping orthogroups shared by the species examined. A colour scale has been applied to aid in identifying the most- and least-overlapping data sources.

Figure 4:

A, Diagrammatic representation of Hox and Parahox cluster chromosomal organization showing a shared pattern among selected Lophotrochozoan taxa (scallops Pecten maximus and Mizuhopecten yessoensis, Pacific oyster Crassostrea gigas, owl limpet Lottia gigantea, and annelid Capitella teleta) along with an outgroup (red flour beetle [Tribolium castaneum]). Grey bar linking genes represents regions of synteny. Silhouette sources: Phylopic as listed in Acknowledgements and –. Arrows show direction of transcription where known. B, Phylogeny of P. maximus Hox and Parahox genes alongside those of known homology from previous work [95, 96] inferred using MrBayes (MrBayes, RRID:SCR_012067) [97] under the Jones model (1,000,000 generations, with 25% discarded as “burn-in”) from a MAFFT alignment under the L-INS-I model [98]. Numbers at base of nodes are posterior probabilities, shown to 2 significant figures. Branches are coloured by gene.

Figure 5:

Domain alignments (generated using MAFFT using the E-INS-I model [98]) of the sodium channel Nav1 showing residues (text in red, highlighted in yellow) implicated in resistance to the neurotoxins tetrodotoxin (TTX) and saxitoxins (STX). Species of vertebrate and mollusc known to be resistant to TTX or STX [86–89] are shown alongside species and sub-populations with no resistance to these toxins. Species (and sub-populations) that produce or accumulate these toxins with little or no ill effect are marked with a skull-and-crossbones. Pecten maximus (bold text) shares a thymine residue in domain 3 known to confer neurotoxin resistance in several other species. It also has a number of residues (shown in green text with amber background) in Domains 3 and 4, which are either unique to P. maximus or shared with other resistant shellfish, but not seen in other species. These residues are good candidates for testing for a functional role in resistance in the future.