The Lingula genome provides insights into brachiopod evolution and the origin of phosphate biomineralization.

Yi-Jyun Luo,Noriyuki Satoh,Mariia Khalturina,Ryo Koyanagi,Lixy Yamada,Shin-Ichi Yamasaki,Kazuyoshi Endo,Miyuki Kanda,Takeshi Takeuchi,Manabu Fujie

doi:10.1038/ncomms9301

Abstract

The evolutionary origins of lingulid brachiopods and their calcium phosphate shells have been obscure. Here we decode the 425-Mb genome of Lingula anatina to gain insights into brachiopod evolution. Comprehensive phylogenomic analyses place Lingula close to molluscs, but distant from annelids. The Lingula gene number has increased to ∼34,000 by extensive expansion of gene families. Although Lingula and vertebrates have superficially similar hard tissue components, our genomic, transcriptomic and proteomic analyses show that Lingula lacks genes involved in bone formation, indicating an independent origin of their phosphate biominerals. Several genes involved in Lingula shell formation are shared by molluscs. However, Lingula has independently undergone domain combinations to produce shell matrix collagens with EGF domains and carries lineage-specific shell matrix proteins. Gene family expansion, domain shuffling and co-option of genes appear to be the genomic background of Lingula's unique biomineralization. This Lingula genome provides resources for further studies of lophotrochozoan evolution.

Highlights

The evolutionary origins of lingulid brachiopods and their calcium phosphate shells have been obscure
Abundant in the fossil record, Darwin first referred to lingulid brachiopods as ‘living fossils,’ because their shell morphology has changed little since the Silurian[1]
We sequenced the 425-Mb genome of L. anatina (Fig. 1a–i) with B226-fold coverage using four next-generation sequencers. This effort yielded an assembly with a scaffold N50 size of 294 kb, comparable to those of other lophotrochozoan genomes[17,18,19] (Supplementary Note 1, Supplementary Figs 1–3 and Supplementary Tables 1–3)

Summary

Introduction

The evolutionary origins of lingulid brachiopods and their calcium phosphate shells have been obscure. Domain shuffling and co-option of genes appear to be the genomic background of Lingula’s unique biomineralization This Lingula genome provides resources for further studies of lophotrochozoan evolution. The Linguliformea, including the extant genus, Lingula, is recognized as the most primitive group, with a fossil record dating back to the early Cambrian and coinciding with the innovation of animal biomineralization[3] Their shells are composed of calcium phosphate and collagen fibres, characters shared only by evolutionarily distant vertebrates[1,4]. In contrast to mollusc shells and other invertebrate calcified tissues, Lingula shells comprises calcium phosphate, laminated, flexible and rich in organic materials[1] Despite their palaeontological importance, the evolutionary origin of Lingula shells is still unclear. Whether brachiopods are monophyletic or polyphyletic[2,13] and whether Brachiopoda is close to Phoronida, Nemertea, Mollusca, Annelida or other lophotrochozoan phyla, remains to be resolved[14,15,16]

Methods

Results

Conclusion