Chromosome-level draft genome assembly of Hypomesus nipponensis reveals transposable element expansion reshaping the genome structure

Abstract

Hypomesus nipponensis a commercially valuable fish within the Osmeriformes order, is naturally found in northeastern Asia and has been extensively introduced for commercial purposes across eastern Asia. To investigate the taxonomic status and evolutionary history of Hypomesus nipponensis within the Osmeridae family, we first performed a de novo genome assembly using PacBio HiFi reads and CLR (Continuous Long Read) reads. Subsequently, we leveraged synteny information from closely related species to further refine the assembly and construct a chromosome-level genome. The final assembly spans 507.8 Mb, with a scaffold N50 of 20 Mb, achieving chromosome-level contiguity. It comprises 164 Mb of repetitive sequences and encodes 27,876 protein-coding genes. Compared to previous assembly, the H. nipponensis genome is notably more contiguous and complete. Notably, it contains an unusually high proportion of tandem repeats, which likely contributed to the assembly challenges encountered in earlier efforts. We also observed the transposons of H. nipponensis have expanded significantly in recent times, and paralogous gene families have expanded during the same period. Our analysis estimates that H. nipponensis, Osmerus eperlanus, and Hypomesus transpacificus diverged from a common ancestor approximately 24.1 million years ago, with significant chromosomal segment recombination events occurring during their divergence. Additionally, we compared the genomes of O. eperlanus and Hypomesus and found that most of the genes in the Presence/Absence Variants (PAVs) of O. eperlanus were associated with immune response. Our efforts significantly enhance the genome's integrity and continuity for this ecologically and commercially important fish, providing a chromosome-level genome draft that supports fundamental biological research while offering insights into the evolutionary relationships and genomic diversity within the Osmeriformes order. This advancement has profound implications for understanding the evolutionary history and adaptive strategies of H. nipponensis.

Keywords: Hypomesus nipponensis; evolutionary; gene family; genome; repeat sequence.

FIGURE 1

Circos plot of the Hypomesus nipponensis genome, with lines of different colors in the diagram represent the colinearity within the genome. The rings from inside to outside indicate (a) pseudochromosome length of the Hypomesus nipponensis genome (b) GC density (c) TE density, and (d) gene density; b-d were drawn in 100-kb sliding windows.

FIGURE 2

(A) The ratio of different repeat sequences. (B) The top of the stacking strip diagram represents the integrity assessment, and the lower part of the strip diagram represents the consistency assessment. (C) The left, middle, and right panels illustrate the distributions of mRNA length, exon length, and CDS length, respectively, in comparison with those of other representative species.

FIGURE 3

(A) Gene family analysis and divergence time of ten representative species, gray lines indicate confidence intervals. (B) The distribution of the synonymous substitution rates (Ks) of homologous genes between Esox lucius and Hypomesus nipponensis, O. eperlanus and Hypomesus nipponensis, Hypomesus transpacificus and Hypomesus nipponensis, P. chinensis and Hypomesus nipponensis. (C) Shows GO enrichment for expanded gene families. (D) shows GO enrichment for contracted.

FIGURE 4

(A) The number of tandem repeat sequences of different lengths in H. nippomensis, Gasterosteus aculeatus and Tetraodontidae. (B) Transposable element (TE) accumulation history in the Hypomesus nipponensis genome, based on a Kimura distance-based copy divergence analysis of TEs, with Kimura substitution level (CpG adjusted) illustrated on the x-axis, and percentage of the genome represented by each repeat type on the y-axis. The bar color indicates the repeat type. (C) HiFi reads the coverage depth of three scattered sequences. (D) Heatmap of average nucleotide identities between pairwise combinations of genomic intervals from three sequences.

FIGURE 5

(A) Ancestral karyotype and chromosomal evolution of various Salmoninae species. (B) Collinearity analysis of Hypomesus nipponensis, Esox lucius, and O. eperlanus genomes.