Tracing animal genomic evolution with the chromosomal-level assembly of the freshwater sponge Ephydatia muelleri

Nathan J Kenny,Sara Camilli,Maša Roller,Ana Riesgo,Lael D Barlow,Warren R Francis,Alex De Mendoza,Sally P Leys,April L Hill,Ramón E Rivera-Vicéns,Luis A Bezares-Calderón,Joseph F Ryan,Lauren Grombacher,Ryan Lister,Cristina Díez-Vives,Gert Wörheide,Ksenia Juravel

doi:10.1038/s41467-020-17397-w

Abstract

The genomes of non-bilaterian metazoans are key to understanding the molecular basis of early animal evolution. However, a full comprehension of how animal-specific traits, such as nervous systems, arose is hindered by the scarcity and fragmented nature of genomes from key taxa, such as Porifera. Ephydatia muelleri is a freshwater sponge found across the northern hemisphere. Here, we present its 326 Mb genome, assembled to high contiguity (N50: 9.88 Mb) with 23 chromosomes on 24 scaffolds. Our analyses reveal a metazoan-typical genome architecture, with highly shared synteny across Metazoa, and suggest that adaptation to the extreme temperatures and conditions found in freshwater often involves gene duplication. The pancontinental distribution and ready laboratory culture of E. muelleri make this a highly practical model system which, with RNAseq, DNA methylation and bacterial amplicon data spanning its development and range, allows exploration of genomic changes both within sponges and in early animal evolution.

Highlights

The genomes of non-bilaterian metazoans are key to understanding the molecular basis of early animal evolution
We have produced a high-quality assembly of the 326 Mb Ephydatia muelleri genome using PacBio, Chicago, and Dovetail Hi-C libraries sequenced to approximately 1490 times total coverage (Supplementary Note 2)
The resulting assembly has 1444 scaffolds with a scaffold N50 of 9.8 Mb (Fig. 2a–c, Supplementary Note 3) and 83.7% of the genome (270 Mb) is encompassed in the largest 24 scaffolds in the assembly. These 24 scaffolds encompass 22 of the 23 Ephydatia muelleri chromosomes (2n = 46)[29] as single sequences, with one chromosome represented by two sequences likely split at the centromere (Fig. 2b)

Summary

Introduction

The genomes of non-bilaterian metazoans are key to understanding the molecular basis of early animal evolution. The events that enabled this transformation can often be inferred by comparing the genomes of living representatives of non-bilaterian animals to those of bilaterians and their sister taxa, and determining shared characters and key differences between them[2]. Determining the origin of these characteristics requires more robust and contiguous genomic resources than are currently available for non-bilaterian animal taxa. There are over 9200 species of sponge (http:// www.marinespecies.org/porifera/,11), and understanding whether the unusual characteristics of A. queenslandica are typical of this large and diverse phylum can only be tested with additional, and more contiguous, genome assemblies. Sponges possess the fundamental characteristics shared by all animals, including development through embryogenesis to form tissues and signalling to coordinate whole body behaviour[13,14]. Despite the diversity of sponges in the most species-rich class, the Demospongiae, only one group, the Spongillida, made the transition to freshwater some 250–300 million years ago (Mya)

Methods

Results

Conclusion