Horseshoe crab genomes reveal the evolution of genes and microRNAs after three rounds of whole genome duplication

Normaz Wana Ismail ,Siddhartha Pati,Siu Gin Cheung,Kevin Yuk‐Lap Yip ,Sai Ming Ngai,Stephen S Tobe,Jerome H.l Hui ,Alexander Hayward,Zhe Qu,Ting‐Fung Chan ,Yiqian Li,Wenyan Nong,Ho Yin Yip,Hon Kit Wong ,Jianquan Cao,Satya Narayana,Jian Qiu ,William G Bendena,Hoi Ting Lee,Tobias Baril,Hoi Shan Kwan,Thomas Swale,Gianni Panagiotou,Pei‐Yuan Qian ,Akbar John,Tom Barton-Owen

doi:10.1038/s42003-020-01637-2

Abstract

Whole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates. Consequently, the WGD that occurred in the common ancestor of horseshoe crabs ~135 million years ago provides a rare opportunity to decipher the evolutionary consequences of a duplicated invertebrate genome. Here, we present a high-quality genome assembly for the mangrove horseshoe crab Carcinoscorpius rotundicauda (1.7 Gb, N50 = 90.2 Mb, with 89.8% sequences anchored to 16 pseudomolecules, 2n = 32), and a resequenced genome of the tri-spine horseshoe crab Tachypleus tridentatus (1.7 Gb, N50 = 109.7 Mb). Analyses of gene families, microRNAs, and synteny show that horseshoe crabs have undergone three rounds (3R) of WGD. Comparison of C. rotundicauda and T. tridentatus genomes from populations from several geographic locations further elucidates the diverse fates of both coding and noncoding genes. Together, the present study represents a cornerstone for improving our understanding of invertebrate WGD events on the evolutionary fates of genes and microRNAs, at both the individual and population level. We also provide improved genomic resources for horseshoe crabs, of applied value for breeding programs and conservation of this fascinating and unusual invertebrate lineage.

Highlights

Whole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates
A high-quality genome assembly was recently announced as a genomic resource for T. tridentatus[14,15], leaving an exciting research opportunity to analyse the genomes of other horseshoe crab species to understand how WGD events reshape the genome and rewire genetic regulatory networks in invertebrates
Genomic DNA was extracted from single individuals of two species of horseshoe crab, C. rotundicauda and T. tridentatus (Fig. 1b), and sequenced using Illumina short-read, 10X Genomics linked-read, and PacBio long-read sequencing platforms (Supplementary Tables 1–4)

Summary

Introduction

Whole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates. Genomic DNA was extracted from single individuals of two species of horseshoe crab, C. rotundicauda and T. tridentatus (Fig. 1b), and sequenced using Illumina short-read, 10X Genomics linked-read, and PacBio long-read sequencing platforms (Supplementary Tables 1–4).

Results

Conclusion