Divergent genomic trajectories predate the origin of animals and fungi

Eduard Ocaña-Pallarès (), Tom A. Williams, David López-Escardó, Alicia S. Arroyo, Jananan S. Pathmanathan, Eric Bapteste, Denis V. Tikhonenkov, Patrick J. Keeling, Gergely J. Szöllősi and Iñaki Ruiz-Trillo ()
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Eduard Ocaña-Pallarès: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)
Tom A. Williams: University of Bristol
David López-Escardó: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)
Alicia S. Arroyo: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)
Jananan S. Pathmanathan: Université Pierre et Marie Curie
Eric Bapteste: Sorbonne Université, CNRS, Museum National d’Histoire Naturelle, EPHE, Université des Antilles
Denis V. Tikhonenkov: Russian Academy of Sciences
Patrick J. Keeling: University of British Columbia
Gergely J. Szöllősi: Eötvös Lorand University
Iñaki Ruiz-Trillo: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)

Nature, 2022, vol. 609, issue 7928, 747-753

Abstract: Abstract Animals and fungi have radically distinct morphologies, yet both evolved within the same eukaryotic supergroup: Opisthokonta1,2. Here we reconstructed the trajectory of genetic changes that accompanied the origin of Metazoa and Fungi since the divergence of Opisthokonta with a dataset that includes four novel genomes from crucial positions in the Opisthokonta phylogeny. We show that animals arose only after the accumulation of genes functionally important for their multicellularity, a tendency that began in the pre-metazoan ancestors and later accelerated in the metazoan root. By contrast, the pre-fungal ancestors experienced net losses of most functional categories, including those gained in the path to Metazoa. On a broad-scale functional level, fungal genomes contain a higher proportion of metabolic genes and diverged less from the last common ancestor of Opisthokonta than did the gene repertoires of Metazoa. Metazoa and Fungi also show differences regarding gene gain mechanisms. Gene fusions are more prevalent in Metazoa, whereas a larger fraction of gene gains were detected as horizontal gene transfers in Fungi and protists, in agreement with the long-standing idea that transfers would be less relevant in Metazoa due to germline isolation3–5. Together, our results indicate that animals and fungi evolved under two contrasting trajectories of genetic change that predated the origin of both groups. The gradual establishment of two clearly differentiated genomic contexts thus set the stage for the emergence of Metazoa and Fungi.

Date: 2022
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DOI: 10.1038/s41586-022-05110-4

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