Dynamics of genomic innovation in the unicellular ancestry of animals

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Abstract

Which genomic innovations underpinned the origin of multicellular animals is still an open debate. Here, we investigate this question by reconstructing the genome architecture and gene family diversity of ancestral premetazoans, aiming to date the emergence of animal-like traits. Our comparative analysis involves genomes from animals and their closest unicellular relatives (the Holozoa), including four new genomes: three Ichthyosporea and Corallochytrium limacisporum. Here we show that the earliest animals were shaped by dynamic changes in genome architecture before the emergence of multicellularity: an early burst of gene diversity in the ancestor of Holozoa, enriched in transcription factors and cell adhesion machinery, was followed by multiple and differently-timed episodes of synteny disruption, intron gain and genome expansions. Thus, the foundations of animal genome architecture were laid before the origin of complex multicellularity – highlighting the necessity of a unicellular perspective to understand early animal evolution.

Data availability

The following data sets were generated

1. X. Grau-Bové et al.
(2017) Genome sequencing and assembly data from Corallochytrium, Abeoforma, Pirum and Chromosphaera
BioProject accession PRJNA360047.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA360047
1. X. Grau-Bové et al.
(2017) Transcriptome sequencing data from Abeoforma and Chromosphaera
BioProject accession PRJNA360056.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA360056

Article and author information

Author details

Xavier Grau-Bové

Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain

For correspondence
xavier.graubove@gmail.com

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-1978-5824
Guifré Torruella

Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud/Paris-Saclay, Orsay, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6534-4758
Stuart Donachie

Department of Microbiology, University of Hawai'i at Mānoa, Honolulu, United States

Competing interests
The authors declare that no competing interests exist.
Hiroshi Suga

Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Shobara, Japan

Competing interests
The authors declare that no competing interests exist.
Guy Leonard

Department of Biosciences, Living Systems Institute, Exeter, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4607-2064
Thomas A Richards

Department of Biosciences, University of Exeter, Exeter, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Iñaki Ruiz-Trillo

Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain

For correspondence
inaki.ruiz@multicellgenome.org

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6547-5304

Funding

Ministerio de Economía y Competitividad (BFU2014-57779-P)

Iñaki Ruiz-Trillo

European Commission (ERC-2012-Co -616960)

Iñaki Ruiz-Trillo

Ministerio de Economía y Competitividad (BFU-2011-23434)

Iñaki Ruiz-Trillo

Generalitat de Catalunya (2014 SGR 619)

Iñaki Ruiz-Trillo

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

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.