The Scaly-foot Snail genome and implications for the origins of biomineralised armour

Abstract

The Scaly-foot Snail, Chrysomallon squamiferum, presents a combination of biomineralised features, reminiscent of enigmatic early fossil taxa with complex shells and sclerites such as sachtids, but in a recently-diverged living species which even has iron-infused hard parts. Thus the Scaly-foot Snail is an ideal model to study the genomic mechanisms underlying the evolutionary diversification of biomineralised armour. Here, we present a high-quality wholegenome assembly and tissue-specific transcriptomic data, and show that scale and shell formation in the Scaly-foot Snail employ independent subsets of 25 highly-expressed transcription factors. Comparisons with other lophotrochozoan genomes imply that this biomineralisation toolkit is ancient, though expression patterns differ across major lineages. We suggest that the ability of lophotrochozoan lineages to generate a wide range of hard parts, exemplified by the remarkable morphological disparity in Mollusca, draws on a capacity for dynamic modification of the expression and positioning of toolkit elements across the genome.

The ‘biomineralization toolkit’ and the origin of animal skeletons

“…Brachiopods and molluscs have also possibly independently co-optedengrailed into shell formation (Shimizu et al, 2017). Among the suite of 25 transcription factors found by Sun et al (2020) are several involved in shell matrix protein production including pif, chitin-bindingperitrophin-A domain gene, and chitin synthase. Carbonic anhydrases, which have a wide range of fundamental physiological roles, have also been shown to play a crucial role in biomineralization in calcareous sponges (Jackson et al, 2007) and independently in different mollusc lineages (Jackson et al, 2010), also playing a role in calcification of organic precursors.…”

Dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis revealed by its hologenome

“…This is one of only a few chromosome-level genome assemblies currently available in Gastropoda or even Mollusca. The genome size of G. aegis is more than double of the C. squamiferum genome (~444.4 Mb) 17 mainly due to the larger contribution of repetitive regions (Fig. S1, Fig.…”

“…To predict the gene models, we run two rounds of the MAKER pipeline version 2.31.10 51 on the soft-masked genome. To guide the prediction, we used de novo assembled transcripts, Metazoan protein sequences downloaded from the Swiss-Prot database, as well as protein sequences of Chrysomallon squamiferum 17 (for details see the Supplementary Materials). The predicted protein sequences were searched against NCBI Non-Redundant (NR) database using BLASTp with an E-value cutoff of 1e-5.…”

“…If genes had a fold change larger than two and a significant FDR P-value (< 0.05), they were designated as highly expressed genes. To compare the genes expression of G. aegis and C. squamiferum, the same analysis pipeline was applied to the transcriptome sequencing data of foot tissue, ctenidium, mantle, and oesophageal gland from the C. squamiferum 17 .…”

“…From previous studies, we know that C. squamiferum hosts only one phylotype of sulphur-oxidising Gammaproteobacteria whose genome has been sequenced 3 . The whole genome of the host was also recently sequenced at chromosome-level 17 , but little has been explored in terms of its adaptations related to symbiosis. In the present study, we reveal that Gigantopelta aegis has a dual endosymbiosis, where the snail houses two Gammaproteobacteria endosymbionts, one sulphur-oxidising and one methane-oxidising, in its oesophageal gland.…”