The genome of the venomous snail Lautoconus ventricosus sheds light on the origin of conotoxin diversity

Abstract

Background: Venoms are deadly weapons to subdue prey or deter predators that have evolved independently in many animal lineages. The genomes of venomous animals are essential to understand the evolutionary mechanisms involved in the origin and diversification of venoms.

Results: Here, we report the chromosome-level genome of the venomous Mediterranean cone snail, Lautoconus ventricosus (Caenogastropoda: Conidae). The total size of the assembly is 3.59 Gb; it has high contiguity (N50 = 93.53 Mb) and 86.6 Mb of the genome assembled into the 35 largest scaffolds or pseudochromosomes. On the basis of venom gland transcriptomes, we annotated 262 complete genes encoding conotoxin precursors, hormones, and other venom-related proteins. These genes were scattered in the different pseudochromosomes and located within repetitive regions. The genes encoding conotoxin precursors were normally structured into 3 exons, which did not necessarily coincide with the 3 structural domains of the corresponding proteins. Additionally, we found evidence in the L. ventricosus genome for a past whole-genome duplication event by means of conserved gene synteny with the Pomacea canaliculata genome, the only one available at the chromosome level within Caenogastropoda. The whole-genome duplication event was further confirmed by the presence of a duplicated hox gene cluster. Key genes for gastropod biology including those encoding proteins related to development, shell formation, and sex were located in the genome.

Conclusions: The new high-quality L. ventricosus genome should become a reference for assembling and analyzing new gastropod genomes and will contribute to future evolutionary genomic studies among venomous animals.

Keywords: Lautoconus ventricosus; Mediterranean cone snail; chromosome-level genome; conotoxin precursor genes; venom gland transcriptome; whole-genome duplication.

Figure 1:

Genome organization. The 35 pseudochromosomes of the L. ventricosus genome are shown in red. In the inner rings, the distributions of genes (black; y-axis indicates percentage of genes per megabase, normalized to 40 genes) and of repetitive elements (green; y-axis indicates percentage of repetitive elements per megabase, normalized to 6,000 repetitive elements) are depicted.

Figure 2:

Conotoxin genes. The distribution of the conotoxin precursor (red), hormone (blue), and venom-related protein (green) genes in the 35 pseudochromosomes is shown. Genes closer than 2 Mb were clustered together and their number annotated in parentheses. A cone snail sketch (drawn by Lara de la Cita) highlighting (from left to right) the siphon (orange), proboscis (red), and radular sac (brown) and the duct (yellow) and bulb (white) of the venom gland is shown.

Figure 3:

Conserved synteny and whole-genome duplication. (A) Conserved synteny between L. ventricosus and P. canaliculata derived from ortholog proteins. (B) Distribution of synonymous divergence (Ks) between pairs of paralogs in L. ventricosus. The second Ks peak indicates the similar divergence between paralogs after the whole-genome duplication. (C) Annotation of hox and parahox clusters in L. ventricosus and comparison with other available gastropod genomes within a phylogenetic framework.