Divergent genomic trajectories predate the origin of animals and fungi

Eduard Ocana-Pallares*, Tom Williams, David Lopez-Escardo, Alicia S. Arroyo, Jananan S. Pathmanathan, Eric Bapteste, Denis V. Tikhonenkov, Patrick J. Keeling, Gergely J. Szöllősi, Iñaki Ruiz-Trillo*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

40 Citations (Scopus)
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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 isolation3,4,5. 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.
Original languageEnglish
Pages (from-to)747-753
Number of pages7
JournalNature
Volume609
Issue number7928
DOIs
Publication statusPublished - 24 Aug 2022

Bibliographical note

Funding Information:
E.O.-P. was supported by a predoctoral FPI grant from MINECO (BES-2015-072241) and by ESF Investing in your future. E.O.-P., D.L-E., A.S.A. and I.R.-T. received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7-2007-2013) (Grant agreement No. 616960) and also from grants (BFU2014-57779-P and PID2020-120609GB-I00) by MCIN/AEI/10.13039/501100011033 and ‘ERDF A way of making Europe’. E.O.-P. and G.J.Sz. received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation programme (Grant agreement No. 714774). T.A.W. was supported by a Royal Society University Research Fellowship (URF\R\201024) and NERC standard grant NE/P00251X/1. This work was supported by the Gordon and Betty Moore Foundation through grant GBMF9741 to T.A.W. and G.J.Sz. J.S.P. and E.B. received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7-2007-2013) (Grant agreement No. 615274). D.V.T. and cell culturing were supported by the Russian Science Foundation grant no. 18-14-00239, https://rscf.ru/project/18-14-00239/ . Culture of P. vietnamica was obtained as the result of field work in Vietnam as part of the project ‘Ecolan 3.2’ of the Russian–Vietnam Tropical Center. P.J.K. is supported by an Investigator Award from the Gordon and Betty Moore Foundation ( https://doi.org/10.37807/GBMF9201 ). We thank the CRG/UPF FACS Unit, the CRG Genomics Unit and M. Antó-Subirats for technical assistance; D. J. Richter, M. M. Leger and I. Patten for the feedback provided on the manuscript; and M. J. Greenacre for the feedback provided on multivariate statistics.

Publisher Copyright:
© 2022, The Author(s).

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