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High-quality reannotation of the king scallop genome reveals no 'gene-rich' feature and evolution of toxin resistance.

ABSTRACT: The king scallop, Pecten maximus is a well-known, commercially important scallop species and is featured with remarkable tolerance to potent phytotoxins such as domoic acid. A high-quality genome can shed light on its biology and innovative evolution of toxin resistance. A reference genome has recently been published for P. maximus, however, it is suspicious that over 67,700 genes are annotated in this genome, which is unexpectedly larger than its close relatives of pectinids. Herein, we provide an improved high-quality chromosome-level reference genome assembly and annotation for the king scallop P. maximus. A final set of 26,995 genes is annotated after carefully checking and curation of the predicted gene models, which significantly improves the accuracy of gene structure information. The large number of gene duplicates in the previous genome is mainly distorted by the fragmented annotation. Through integrated genomic, evolutionary and transcriptomic analyses, we reveal that the Phi subfamily of ionotropic glutamate receptors (iGluRs) are well preserved in molluscs, and P. maximus experienced the rapid expansion of the Phi class of iGluR (GluF) gene family. The GluF genes exhibit ubiquitously high expression and altered sequence characteristics for ligand selectivity, which may contribute to the remarkable tolerance to neurotoxins in P. maximus. Taken together, our study disapproves the previous claim of the 'gene-rich' genome of this species and provides a high-quality genome assembly for further understanding of its biology and evolution of toxin resistance.

SUBMITTER: Zeng Q

PROVIDER: S-EPMC8437780 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:One of the fastest growing fisheries in the UK is the king scallop (Pecten maximus L.), also currently rated as the second most valuable fishery. Mass mortality events in scallops have been reported worldwide, often with the causative agent(s) remaining uncharacterized. In May 2013 and 2014, two mass mortality events affecting king scallops were recorded in the Lyme Bay marine protected area (MPA) in Southwest England. Histopathological examination showed gill epithelial tissues infected with intracellular microcolonies (IMCs) of bacteria resembling Rickettsia-like organisms (RLOs), often with bacteria released in vascular spaces. Large colonies were associated with cellular and tissue disruption of the gills. Ultrastructural examination confirmed the intracellular location of these organisms in affected epithelial cells. The 16S rRNA gene sequences of the putative IMCs obtained from infected king scallop gill samples, collected from both mortality events, were identical and had a 99.4% identity to 16S rRNA gene sequences obtained from "Candidatus Endonucleobacter bathymodioli" and 95% with Endozoicomonas species. In situ hybridization assays using 16S rRNA gene probes confirmed the presence of the sequenced IMC gene in the gill tissues. Additional DNA sequences of the bacterium were obtained using high-throughput (Illumina) sequencing, and bioinformatic analysis identified over 1,000 genes with high similarity to protein sequences from Endozoicomonas spp. (ranging from 77 to 87% identity). Specific PCR assays were developed and applied to screen for the presence of IMC 16S rRNA gene sequences in king scallop gill tissues collected at the Lyme Bay MPA during 2015 and 2016. There was 100% prevalence of the IMCs in these gill tissues, and the 16S rRNA gene sequences identified were identical to the sequence found during the previous mortality event.IMPORTANCE Molluscan mass mortalities associated with IMCs have been reported worldwide for many years; however, apart from histological and ultrastructural characterization, characterization of the etiological agents is limited. In the present work, we provide detailed molecular characterization of an Endozoicomonas-like organism (ELO) associated with an important commercial scallop species.

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High-quality reannotation of the king scallop genome reveals no 'gene-rich' feature and evolution of toxin resistance.

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