Divergent genomic trajectories predate the origin of animals and fungi

22 pages, 4 figures, supplementary information https://doi.org/10.1038/s41586-022-05110-4.-- Data availability: The raw sequence data and assembled genomes generated in this study have been deposited in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB52884 (https://www.ebi.ac.uk/ena/browser/view/PRJEB52884). The genome assemblies are also available in figshare (https://doi.org/10.6084/m9.figshare.19895962.v1). Protein sequences of the species used in this study were downloaded from the GenBank public databases (https://www.ncbi.nlm.nih.gov/protein/), Uniprot (https://www.uniprot.org/), JGI genome database (https://genome.jgi.doe.gov/portal/) and Ensembl genomes (https://www.ensembl.org). The following specific databases were also used in this study: Pfam A v29 (https://pfam.xfam.org/), EggNOG emapperdb-4.5.1 (http://eggnog5.embl.de) and UniProt reference proteomes release 2016_02 (https://www.uniprot.org/). The supporting data files of this study are available in the following repository: https://doi.org/10.6084/m9.figshare.13140191.v1.-- Code availability: The most relevant custom code developed for this study (the MAPBOS pipeline and the machine learning classifiers) is available at https://doi.org/10.5281/zenodo.6586559

Saved in:
Bibliographic Details
Main Authors: Ocaña-Pallarès, Eduard, Williams, Tom A., López-Escardó, David, Arroyo, Alicia S., Pathmanathan, Jananan S., Bapteste, Eric, Tikhonenkov, Denis V., Keeling, Patrick J., Szöllősi, Gergely J., Ruiz-Trillo, Iñaki
Other Authors: Ministerio de Economía y Competitividad (España)
Format: artículo biblioteca
Language:English
Published: Nature Publishing Group 2022-09
Online Access:http://hdl.handle.net/10261/280377
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/100000936
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/501100000270
http://dx.doi.org/10.13039/501100000288
http://dx.doi.org/10.13039/501100011033
Tags: Add Tag
No Tags, Be the first to tag this record!
id dig-icm-es-10261-280377
record_format koha
institution ICM ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-icm-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del ICM España
language English
description 22 pages, 4 figures, supplementary information https://doi.org/10.1038/s41586-022-05110-4.-- Data availability: The raw sequence data and assembled genomes generated in this study have been deposited in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB52884 (https://www.ebi.ac.uk/ena/browser/view/PRJEB52884). The genome assemblies are also available in figshare (https://doi.org/10.6084/m9.figshare.19895962.v1). Protein sequences of the species used in this study were downloaded from the GenBank public databases (https://www.ncbi.nlm.nih.gov/protein/), Uniprot (https://www.uniprot.org/), JGI genome database (https://genome.jgi.doe.gov/portal/) and Ensembl genomes (https://www.ensembl.org). The following specific databases were also used in this study: Pfam A v29 (https://pfam.xfam.org/), EggNOG emapperdb-4.5.1 (http://eggnog5.embl.de) and UniProt reference proteomes release 2016_02 (https://www.uniprot.org/). The supporting data files of this study are available in the following repository: https://doi.org/10.6084/m9.figshare.13140191.v1.-- Code availability: The most relevant custom code developed for this study (the MAPBOS pipeline and the machine learning classifiers) is available at https://doi.org/10.5281/zenodo.6586559
author2 Ministerio de Economía y Competitividad (España)
author_facet Ministerio de Economía y Competitividad (España)
Ocaña-Pallarès, Eduard
Williams, Tom A.
López-Escardó, David
Arroyo, Alicia S.
Pathmanathan, Jananan S.
Bapteste, Eric
Tikhonenkov, Denis V.
Keeling, Patrick J.
Szöllősi, Gergely J.
Ruiz-Trillo, Iñaki
format artículo
author Ocaña-Pallarès, Eduard
Williams, Tom A.
López-Escardó, David
Arroyo, Alicia S.
Pathmanathan, Jananan S.
Bapteste, Eric
Tikhonenkov, Denis V.
Keeling, Patrick J.
Szöllősi, Gergely J.
Ruiz-Trillo, Iñaki
spellingShingle Ocaña-Pallarès, Eduard
Williams, Tom A.
López-Escardó, David
Arroyo, Alicia S.
Pathmanathan, Jananan S.
Bapteste, Eric
Tikhonenkov, Denis V.
Keeling, Patrick J.
Szöllősi, Gergely J.
Ruiz-Trillo, Iñaki
Divergent genomic trajectories predate the origin of animals and fungi
author_sort Ocaña-Pallarès, Eduard
title Divergent genomic trajectories predate the origin of animals and fungi
title_short Divergent genomic trajectories predate the origin of animals and fungi
title_full Divergent genomic trajectories predate the origin of animals and fungi
title_fullStr Divergent genomic trajectories predate the origin of animals and fungi
title_full_unstemmed Divergent genomic trajectories predate the origin of animals and fungi
title_sort divergent genomic trajectories predate the origin of animals and fungi
publisher Nature Publishing Group
publishDate 2022-09
url http://hdl.handle.net/10261/280377
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/100000936
http://dx.doi.org/10.13039/501100003329
http://dx.doi.org/10.13039/501100000270
http://dx.doi.org/10.13039/501100000288
http://dx.doi.org/10.13039/501100011033
work_keys_str_mv AT ocanapallareseduard divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT williamstoma divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT lopezescardodavid divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT arroyoalicias divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT pathmanathanjananans divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT baptesteeric divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT tikhonenkovdenisv divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT keelingpatrickj divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT szollosigergelyj divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
AT ruiztrilloinaki divergentgenomictrajectoriespredatetheoriginofanimalsandfungi
_version_ 1777667853960347648
spelling dig-icm-es-10261-2803772022-11-04T16:38:29Z Divergent genomic trajectories predate the origin of animals and fungi Ocaña-Pallarès, Eduard Williams, Tom A. López-Escardó, David Arroyo, Alicia S. Pathmanathan, Jananan S. Bapteste, Eric Tikhonenkov, Denis V. Keeling, Patrick J. Szöllősi, Gergely J. Ruiz-Trillo, Iñaki Ministerio de Economía y Competitividad (España) European Commission Ministerio de Ciencia, Innovación y Universidades (España) Royal Society (UK) Natural Environment Research Council (UK) Gordon and Betty Moore Foundation Agencia Estatal de Investigación (España) 22 pages, 4 figures, supplementary information https://doi.org/10.1038/s41586-022-05110-4.-- Data availability: The raw sequence data and assembled genomes generated in this study have been deposited in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB52884 (https://www.ebi.ac.uk/ena/browser/view/PRJEB52884). The genome assemblies are also available in figshare (https://doi.org/10.6084/m9.figshare.19895962.v1). Protein sequences of the species used in this study were downloaded from the GenBank public databases (https://www.ncbi.nlm.nih.gov/protein/), Uniprot (https://www.uniprot.org/), JGI genome database (https://genome.jgi.doe.gov/portal/) and Ensembl genomes (https://www.ensembl.org). The following specific databases were also used in this study: Pfam A v29 (https://pfam.xfam.org/), EggNOG emapperdb-4.5.1 (http://eggnog5.embl.de) and UniProt reference proteomes release 2016_02 (https://www.uniprot.org/). The supporting data files of this study are available in the following repository: https://doi.org/10.6084/m9.figshare.13140191.v1.-- Code availability: The most relevant custom code developed for this study (the MAPBOS pipeline and the machine learning classifiers) is available at https://doi.org/10.5281/zenodo.6586559 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 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) With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S) Peer reviewed 2022-10-04T08:50:11Z 2022-10-04T08:50:11Z 2022-09 artículo Nature 609: 747-753 (2022) 0028-0836 CEX2019-000928-S http://hdl.handle.net/10261/280377 10.1038/s41586-022-05110-4 1476-4687 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/100000936 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000270 http://dx.doi.org/10.13039/501100000288 http://dx.doi.org/10.13039/501100011033 en #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/MINECO//BES-2015-072241/ES/BES-2015-072241/ info:eu-repo/grantAgreement/EC/FP7/616960 info:eu-repo/grantAgreement/MINECO//BFU2014-57779-P/ES/ORIGEN, DIVERSIFICACION Y DIVERSIDAD DE METAZOOS, HONGOS Y SUS PARIENTES UNICELULARES; UNA APROXIMACION ECOLOGICA Y EVOLUTIVA/ info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-120609GB-I00/ES/EL ORIGEN DE LOS ANIMALES: UNA APROXIMACION FUNCIONAL Y DE BIODIVERSIDAD/ info:eu-repo/grantAgreement/EC/H2020/714774 info:eu-repo/grantAgreement/EC/FP7/615274 Publisher's version https://doi.org/10.1038/s41586-022-05110-4 Sí open Nature Publishing Group