1. Key Points

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We successfully assembled the whole genome of the enigmatic Scaly-foot Snail, a deep-sea hot vent snail famed for its unique, often iron-infused, scale armour

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We identified a set of 25 proteins (transcription factors) that regulate the making of hard parts in this enigmatic snail

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Comparisons with data from other related animals indicate that the modification of this ancient ‘biomineralisation toolkit’ underlies the ability for animals to repeatedly invent new types of hard parts and thus obtain novel functions

2．Overview

Modern animals produce a wide range of biomineralised hard parts and skeletons, for example bones and teeth in humans, shells of snails, scales of snakes, and chaetae of various worms. These have drastically different functions ranging from structural support to feeding to protection. As such, the evolution of novel hard parts is directly linked to the diversity and acquisition of new functions, and when biomineralised elements first appeared in the Cambrian Period they led to a burst of diversification in animal body forms. Lophotrochozoan^*1 invertebrates, which includes spineless animals such as molluscs (e.g. snails, clams, chitons, squids), polychaete worms, brachiopods, and bryozoans, are particularly adept at ‘inventing’ new hard structures. However, the genomic basis for these innovations have remained unresolved, although a universal ‘biomineralisation toolkit’ has been hypothesised.

The Scaly-foot Snail (Chrysomallon squamiferum; Figure 1) is unique among living snails in possessing dense dermal scales on its foot. Discovered 2001 and endemic to deep-sea hydrothermal vents in the Indian Ocean, its scales are often biomineralised with iron sulfide, making it the only known animal to use a significant amount of iron to construct its skeleton. Initially, the scales were considered to have a protective function, but recent studies indicate that they actually serve as sites for the snail to discard metabolites from its sulfur-oxidising endosymbiotic bacteria. It represents a rare case where an extensive scleritome is of a certainly recent origin (post-Jurassic), and therefore offers an ideal opportunity to test the toolkit hypothesis.

A research team led by Dr. Jin SUN (Hong Kong University of Science and Technology), Dr. Chong CHEN (SUGAR Program, X-STAR, JAMSTEC), and Dr. Norio MIYAMOTO (SUGAR Program, X-STAR, JAMSTEC) successfully sequenced the whole genome of the Scaly-foot Snail. The 444.4 Mb genome assembly is resolved at chromosomal level (Figure 1), and among the most complete and continuous among assembled mollusc or even lophotrochozoan genomes available to date (Figure 2).

By comparing genes highly expressed in tissues secreting the shell and the scales, 25 transcription factors*2 (regulatory proteins) appeared to be involved in regulating the making of hard parts in this enigmatic snail (Figure 3). Totally different subsets of these transcription factors were responsible for regulating the formation of shell and scales. Mapping these elements back to the Scaly-foot Snail genome revealed that most of them are localised on a single chromosome (‘Chr 11’ in the paper). Comparisons with an array of other lophotrochozoan animals indicated that various combinations of these transcription factors are always involved in the secretory control of all kinds of hard parts across different phyla. This suggests that these 25 transcription factors comprise the ‘biomineralisation toolkit’, which predates the origin of these lineages in the ‘Cambrian Explosion’.

These findings demonstrate that the key to inventing new hard structures is not the evolution of new genes, but instead modification and redeployment of an ancient, well-preserved suite of genomic tools. Future studies linking elements and properties of this toolkit to resulting phenotypes will shed light on how downstream processes are controlled to shape the wide variety of known hard parts, and even how to engineer new ones.

The results of this study were published in Nature Communications on April X^th, 2020 (JST). This research was supported by the Research Grants Council of Hong Kong (No. 16101219) and a Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research (18K06401).

Title：The Scaly-foot Snail genome and implications for the origins of biomineralised armour
Authors: Jin Sun^1*, Chong Chen^2*, Norio Miyamoto^2*, Runsheng Li³, Julia D. Sigwart^4,5, Ting Xu³, Yanan Sun¹, Wai Chuen Wong¹, Jack C.H. Ip³, Weipeng Zhang¹, Yi Lan1, Dass Bissessur⁶, Tomo-o Watsuji^2,7, Hiromi Kayama Watanabe², Yoshihiro Takaki², Kazuho Ikeo⁸, Nobuyuki Fujii⁸, Kazutoshi Yoshitake⁹, Jian-Wen Qiu³, Ken Takai², & Pei-Yuan Qian¹
Affiliations: 1Hong Kong University of Science and Technology; 2X-STAR, JAMSTEC; 3Hong Kong Baptist University; 4Queen’s University Belfast; 5Senckenberg Museum, Frankfurt, Germany; 6Department for Continental Shelf, Maritime Zones Administration & Exploration, Ministry of Defence and Rodrigues, Mauritius; 7Higashi-Chikushi Junior College; 8National Institute of Genetics; 9The University of Tokyo
*These authors contributed equally to this work.