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

Jin SUN; Chong CHEN; Norio MIYAMOTO; Runsheng LI; Julia D. SIGWART; Ting XU; Yanan SUN; Wai Chuen WONG; Jack C.H. IP; Weipeng ZHANG; Yi LAN; Dass BISSESSUR; Tomo-o WATSUJI; Hiromi Kayama WATANABE; Yoshihiro TAKAKI; Kazuho IKEO; Nobuyuki FUJII; Kazutoshi YOSHITAKE; Jian Wen QIU; Ken TAKAI; Pei Yuan QIAN

doi:10.1038/s41467-020-15522-3

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

Jin SUN, Chong CHEN, Norio MIYAMOTO, Runsheng LI, Julia D. SIGWART, Ting XU, Yanan SUN, Wai Chuen WONG, Jack C.H. IP, Weipeng ZHANG, Yi LAN, Dass BISSESSUR, Tomo-o WATSUJI, Hiromi Kayama WATANABE, Yoshihiro TAKAKI, Kazuho IKEO, Nobuyuki FUJII, Kazutoshi YOSHITAKE, Jian Wen QIU, Ken TAKAIPei Yuan QIAN^*

^*Corresponding author for this work

Research output: Journal Publications › Journal Article (refereed) › peer-review

66 Citations (Scopus)

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.

Original language	English
Article number	1657
Number of pages	12
Journal	Nature Communications
Volume	11
Issue number	1
Early online date	8 Apr 2020
DOIs	https://doi.org/10.1038/s41467-020-15522-3
Publication status	Published - 1 Dec 2020
Externally published	Yes

Bibliographical note

Funding Information:
The authors thank the captain and crew of R/V Yokosuka during cruises YK13-02 (principal scientist: Manabu Nishizawa), YK13-03 (principal scientist: Kentaro Naka-mura) and YK16-02E (principal scientist: Ken Takai), and pilots of DSV Shinkai 6500. Takuro Nunoura (JAMSTEC) is gratefully acknowledged for bringing together collaborative efforts. This research was financially supported by the China Ocean Mineral Resource Research and Development Association (DY135-E2-1-03 to P.-Y.Q.), the Hong Kong Branch of South Marine Science and Engineering Guangdong Laboratory (SMSEGL20Sc01 to P.-Y.Q.), the Research Grants Council of Hong Kong (GRF grant No. 16101219 to J.S., C.C., and P.-Y.Q.), and a Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research (18K06401 to C.C. and H.K.W.). Illumina sequencing was performed by Novogene (Beijing, China). Sampling in the Mauritian EEZ was approved by Ministry of Foreign Affairs, Regional Integration, and International Trade, Mauritian Government (Ref. 29/2014; 50/38/24 V2).

Publisher Copyright:
© 2020, The Author(s).

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SUN, J., CHEN, C., MIYAMOTO, N., LI, R., SIGWART, J. D., XU, T., SUN, Y., WONG, W. C., IP, J. C. H., ZHANG, W., LAN, Y., BISSESSUR, D., WATSUJI, T., WATANABE, H. K., TAKAKI, Y., IKEO, K., FUJII, N., YOSHITAKE, K., QIU, J. W., ... QIAN, P. Y. (2020). The Scaly-foot Snail genome and implications for the origins of biomineralised armour. Nature Communications, 11(1), Article 1657. https://doi.org/10.1038/s41467-020-15522-3

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title = "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 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.",

author = "Jin SUN and Chong CHEN and Norio MIYAMOTO and Runsheng LI and SIGWART, {Julia D.} and Ting XU and Yanan SUN and WONG, {Wai Chuen} and IP, {Jack C.H.} and Weipeng ZHANG and Yi LAN and Dass BISSESSUR and Tomo-o WATSUJI and WATANABE, {Hiromi Kayama} and Yoshihiro TAKAKI and Kazuho IKEO and Nobuyuki FUJII and Kazutoshi YOSHITAKE and QIU, {Jian Wen} and Ken TAKAI and QIAN, {Pei Yuan}",

note = "Funding Information: The authors thank the captain and crew of R/V Yokosuka during cruises YK13-02 (principal scientist: Manabu Nishizawa), YK13-03 (principal scientist: Kentaro Naka-mura) and YK16-02E (principal scientist: Ken Takai), and pilots of DSV Shinkai 6500. Takuro Nunoura (JAMSTEC) is gratefully acknowledged for bringing together collaborative efforts. This research was financially supported by the China Ocean Mineral Resource Research and Development Association (DY135-E2-1-03 to P.-Y.Q.), the Hong Kong Branch of South Marine Science and Engineering Guangdong Laboratory (SMSEGL20Sc01 to P.-Y.Q.), the Research Grants Council of Hong Kong (GRF grant No. 16101219 to J.S., C.C., and P.-Y.Q.), and a Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research (18K06401 to C.C. and H.K.W.). Illumina sequencing was performed by Novogene (Beijing, China). Sampling in the Mauritian EEZ was approved by Ministry of Foreign Affairs, Regional Integration, and International Trade, Mauritian Government (Ref. 29/2014; 50/38/24 V2). Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

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doi = "10.1038/s41467-020-15522-3",

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SUN, J, CHEN, C, MIYAMOTO, N, LI, R, SIGWART, JD, XU, T, SUN, Y, WONG, WC, IP, JCH, ZHANG, W, LAN, Y, BISSESSUR, D, WATSUJI, T, WATANABE, HK, TAKAKI, Y, IKEO, K, FUJII, N, YOSHITAKE, K, QIU, JW, TAKAI, K & QIAN, PY 2020, 'The Scaly-foot Snail genome and implications for the origins of biomineralised armour', Nature Communications, vol. 11, no. 1, 1657. https://doi.org/10.1038/s41467-020-15522-3

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T1 - The Scaly-foot Snail genome and implications for the origins of biomineralised armour

AU - SUN, Jin

AU - CHEN, Chong

AU - MIYAMOTO, Norio

AU - LI, Runsheng

AU - SIGWART, Julia D.

AU - XU, Ting

AU - SUN, Yanan

AU - WONG, Wai Chuen

AU - IP, Jack C.H.

AU - ZHANG, Weipeng

AU - LAN, Yi

AU - BISSESSUR, Dass

AU - WATSUJI, Tomo-o

AU - WATANABE, Hiromi Kayama

AU - TAKAKI, Yoshihiro

AU - IKEO, Kazuho

AU - FUJII, Nobuyuki

AU - YOSHITAKE, Kazutoshi

AU - QIU, Jian Wen

AU - TAKAI, Ken

AU - QIAN, Pei Yuan

N1 - Funding Information: The authors thank the captain and crew of R/V Yokosuka during cruises YK13-02 (principal scientist: Manabu Nishizawa), YK13-03 (principal scientist: Kentaro Naka-mura) and YK16-02E (principal scientist: Ken Takai), and pilots of DSV Shinkai 6500. Takuro Nunoura (JAMSTEC) is gratefully acknowledged for bringing together collaborative efforts. This research was financially supported by the China Ocean Mineral Resource Research and Development Association (DY135-E2-1-03 to P.-Y.Q.), the Hong Kong Branch of South Marine Science and Engineering Guangdong Laboratory (SMSEGL20Sc01 to P.-Y.Q.), the Research Grants Council of Hong Kong (GRF grant No. 16101219 to J.S., C.C., and P.-Y.Q.), and a Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research (18K06401 to C.C. and H.K.W.). Illumina sequencing was performed by Novogene (Beijing, China). Sampling in the Mauritian EEZ was approved by Ministry of Foreign Affairs, Regional Integration, and International Trade, Mauritian Government (Ref. 29/2014; 50/38/24 V2). Publisher Copyright: © 2020, The Author(s).

PY - 2020/12/1

Y1 - 2020/12/1

N2 - 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.

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DO - 10.1038/s41467-020-15522-3

M3 - Journal Article (refereed)

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JO - Nature Communications

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

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