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

Jin Sun,Wai Chuen Wong,Chong Chen,Kazuho Ikeo,Norio Miyamoto,Jack Chi-Ho Ip ,Weipeng Zhang,Dass Bissessur,Julia D Sigwart,Yanan Sun,Nobuyuki Fujii,Ting Xu,Kazutoshi Yoshitake,Yoshihiro Takaki,Li R ,Ken Takai,Jian Qiu ,Tomo O Watsuji ,Hiromi Watanabe ,Yi Lan,Pei Yuan Qian

doi:10.1038/s41467-020-15522-3

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 whole-genome 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.

Highlights

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
The channels within the scales of the Scaly-foot Snail are likely linked to another key adaptation, in that it hosts sulfur-oxidising bacteria within cells of a highly vascularised, hypertrophied oesophageal gland[13,14], and the sulfur may originate as metabolites from the endosymbionts[12]
The genome of a single specimen of Chrysomallon squamiferum (Fig. 1, Supplementary Fig. 1, Supplementary Table 1) collected from the Kairei hydrothermal vent field was sequenced with a combination of Oxford Nanopore Technologies and Illumina platforms (Supplementary Note 2; Supplementary Table 2)

Summary

Introduction

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. The. Scaly-foot Snail, Chrysomallon squamiferum, is unique among gastropod molluscs in having dense, imbricating chitinous sclerites covering the whole distal surface of the soft foot[6], forming a dermal scale armour in addition to a solid calcium carbonate coiled shell (Fig. 1). Scaly-foot Snail, Chrysomallon squamiferum, is unique among gastropod molluscs in having dense, imbricating chitinous sclerites covering the whole distal surface of the soft foot[6], forming a dermal scale armour in addition to a solid calcium carbonate coiled shell (Fig. 1) These hard parts, including sclerites and the shell, are often mineralised with iron sulfide, making it the only known metazoan using iron as a significant component of skeleton construction[7]. It is unclear whether the evolution of the sclerites in the Scaly-foot Snail should be interpreted as a recurring ancestral phenome, or a recently derived adaptive novelty

Methods

Results

Conclusion