Insights into early animal evolution form the genome of the xenacoelomorph worm Xenoturbella bocki
- University of Cologne, Germany
- University College London, United Kingdom
- Durham University, United Kingdom
- Université Côte d'Azur, France
- UiT The Arctic University of Norway, Norway
- Institut Pasteur, France
- University of Greifswald, Germany
- University of Chicago, United States
- Sorbonne Université, France
- University of Oxford, United Kingdom
Abstract
The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can provide important comparative data and help to understand the evolution and biology of enigmatic species better. Here we assemble and analyse the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian evolution. Our highly contiguous genome assembly of X. bocki has a size of ~111 Mbp in 18 chromosome like scaffolds, with repeat content and intron, exon and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signalling pathways are also largely complete and most bilaterian miRNAs are present. Overall, we conclude that X. bocki has a complex genome typical of bilaterians, which does not reflect the apparent simplicity of its body plan that has been so important to proposals that the Xenacoelomorpha are the simple sister group of the rest of the Bilateria.
Data availability
All read sets (RNA and DNA derived) used in this study will be made available with the publication of this manuscript on the SRA database under the BioProject ID PRJNA864813. Hi-C reads are deposited under SAMN30224387, RNA-Seq under SAMN35083895. The genome assemblies of X. bocki (ERS12565994, ERA16814408) and the Chlamydia sp. (ERS12566084, ERA16814775) are deposited under PRJEB55230 at ENA.Supplementary online material (described in the manuscript) has be made available on Zenodo: doi:10.5281/zenodo.6962271
-
Supplementary files for the Xenoturbella bocki genome analysisdoi:10.5281/zenodo.6962271.
-
The genome of Xenoturbella bockiNCBI BioProject, PRJNA864813.
Article and author information
Author details
Philipp H Schiffer
Maximilian J Telford
Funding
European Research Council (ERC-2012-AdG 322790)
- Philipp H Schiffer
- Helen E Robertson
- Anne C Zakrzewski
- Steven Mueller
- Maximilian J Telford
Deutsche Forschungsgemeinschaft (434028868)
- Philipp H Schiffer
Biotechnology and Biological Sciences Research Council (BB/R016240/1)
- Paschalis Natsidis
- Maximilian J Telford
Leverhulme Trust (RPG-2018-302)
- Daniel J Leite
- Maximilian J Telford
HORIZON EUROPE Marie Sklodowska-Curie Actions (764840 IGNITE)
- Paschalis Natsidis
- Maximilian J Telford
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2024, Schiffer et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,204
- views
-
- 254
- downloads
-
- 1
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Insights into early animal evolution form the genome of the xenacoelomorph worm Xenoturbella bocki
eLife 13:e94948.
https://doi.org/10.7554/eLife.94948
Further reading
-
- Evolutionary Biology
- Neuroscience
The first complete 3D reconstruction of the compound eye of a minute wasp species sheds light on the nuts and bolts of size reduction.
-
- Evolutionary Biology
- Genetics and Genomics
Copy number variants (CNVs) are an important source of genetic variation underlying rapid adaptation and genome evolution. Whereas point mutation rates vary with genomic location and local DNA features, the role of genome architecture in the formation and evolutionary dynamics of CNVs is poorly understood. Previously, we found the GAP1 gene in Saccharomyces cerevisiae undergoes frequent amplification and selection in glutamine-limitation. The gene is flanked by two long terminal repeats (LTRs) and proximate to an origin of DNA replication (autonomously replicating sequence, ARS), which likely promote rapid GAP1 CNV formation. To test the role of these genomic elements on CNV-mediated adaptive evolution, we evolved engineered strains lacking either the adjacent LTRs, ARS, or all elements in glutamine-limited chemostats. Using a CNV reporter system and neural network simulation-based inference (nnSBI) we quantified the formation rate and fitness effect of CNVs for each strain. Removal of local DNA elements significantly impacts the fitness effect of GAP1 CNVs and the rate of adaptation. In 177 CNV lineages, across all four strains, between 26% and 80% of all GAP1 CNVs are mediated by Origin Dependent Inverted Repeat Amplification (ODIRA) which results from template switching between the leading and lagging strand during DNA synthesis. In the absence of the local ARS, distal ones mediate CNV formation via ODIRA. In the absence of local LTRs, homologous recombination can mediate gene amplification following de novo retrotransposon events. Our study reveals that template switching during DNA replication is a prevalent source of adaptive CNVs.
