Reticulate evolution in eukaryotes: origin and evolution of the nitrate assimilation pathway

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dc.creator Ocaña-Pallarès, Eduard
dc.creator Najle, Sebastián R.
dc.creator Scazzocchio, Claudio
dc.creator Ruiz-Trillo, Iñaki
dc.date.accessioned 2021-03-15T23:33:00Z
dc.date.available 2021-03-15T23:33:00Z
dc.date.issued 2019-02-21
dc.identifier.issn 1553-7404
dc.identifier.uri http://hdl.handle.net/2133/20175
dc.description Genes and genomes can evolve through interchanging genetic material, this leading to reticular evolutionary patterns. However, the importance of reticulate evolution in eukary otes, and in particular of horizontal gene transfer (HGT), remains controversial. Given that metabolic pathways with taxonomically-patchy distributions can be indicative of HGT events, the eukaryotic nitrate assimilation pathway is an ideal object of investigation, as pre vious results revealed a patchy distribution and suggested that the nitrate assimilation clus ter of dikaryotic fungi (Opisthokonta) could have been originated and transferred from a lineage leading to Oomycota (Stramenopiles). We studied the origin and evolution of this pathway through both multi-scale bioinformatic and experimental approaches. Our taxon rich genomic screening shows that nitrate assimilation is present in more lineages than pre viously reported, although being restricted to autotrophs and osmotrophs. The phylogenies indicate a pervasive role of HGT, with three bacterial transfers contributing to the pathway origin, and at least seven well-supported transfers between eukaryotes. In particular, we propose a distinct and more complex HGT path between Opisthokonta and Stramenopiles than the one previously suggested, involving at least two transfers of a nitrate assimilation gene cluster. We also found that gene fusion played an essential role in this evolutionary his tory, underlying the origin of the canonical eukaryotic nitrate reductase, and of a chimeric nitrate reductase in Ichthyosporea (Opisthokonta). We show that the ichthyosporean path way, including this novel nitrate reductase, is physiologically active and transcriptionally co regulated, responding to different nitrogen sources; similarly to distant eukaryotes with inde pendent HGT-acquisitions of the pathway. This indicates that this pattern of transcriptional control evolved convergently in eukaryotes, favoring the proper integration of the pathway in the metabolic landscape. Our results highlight the importance of reticulate evolution in eukaryotes, by showing the crucial contribution of HGT and gene fusion in the evolutionary history of the nitrate assimilation pathway. es
dc.description Para citar este articulo: Ocaña-Pallarès E, Najle SR, Scazzocchio C, Ruiz-Trillo I (2019) Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway. PLoS Genet 15(2): e1007986. https://doi.org/10.1371/journal. pgen.1007986
dc.description.sponsorship European Research Council Consolidator Grant: ERC-2012-Co-616960 es
dc.description.sponsorship Secretary’s Office for Universities and Research of the Generalitat de Catalunya: project 2014 SGR 619 es
dc.description.sponsorship Ministerio de Economía Industria y Competitividad (MINECO) - Fondo Europeo de Desarrollo Regional (FEDER): BFU2014-57779-P es
dc.format application/pdf
dc.format.extent 1-39
dc.language.iso eng es
dc.publisher Public Library of Science (PLOS) es
dc.rights openAccess es
dc.rights.uri https://creativecommons.org/licenses/by/4.0/ *
dc.subject Eukaryota es
dc.subject Gene Transfer, Horizontal es
dc.subject Nitrate Assimilation es
dc.subject Computational Biology es
dc.subject Opisthokonta es
dc.subject Stramenopiles es
dc.title Reticulate evolution in eukaryotes: origin and evolution of the nitrate assimilation pathway es
dc.type publishedVersion
dc.rights.holder Universidad Nacional de Rosario es
dc.rights.holder Ocaña-Pallarès, Eduard es
dc.rights.holder Najle, Sebastián R. es
dc.rights.holder Scazzocchio, Claudio es
dc.rights.holder Ruiz-Trillo, Iñaki es
dc.relation.publisherversion https://doi.org/10.1371/journal.pgen.1007986 es
dc.relation.publisherversion https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1007986 es
dc.rights.text Attribution 4.0 International (CC BY 4.0) es
dc.citation.title PLoS Genetics
dc.citation.title 15(2)
dc.description.fil Fil: Ocaña-Pallarès, Eduard. Consejo Superior de Investigaciones Científicas (CSIC) - Universitat Pompeu Fabra. Institut de Biologia Evolutiva (IBE); España.
dc.description.fil Fil: Najle, Sebastián R. Consejo Superior de Investigaciones Científicas (CSIC) - Universitat Pompeu Fabra. Institut de Biologia Evolutiva (IBE); España.
dc.description.fil Fil: Najle, Sebastián R. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario (IBR -CONICET); Argentina.
dc.description.fil Fil. Scazzocchio, Claudio. Imperial College. Department of Microbiology; United Kingdom.
dc.description.fil Fil. Scazzocchio, Claudio. Institute for Integrative Biology of the Cell; France.
dc.description.fil Fil: Ruiz-Trillo, Iñaki. Consejo Superior de Investigaciones Científicas (CSIC) - Universitat Pompeu Fabra. Institut de Biologia Evolutiva (IBE); España.
dc.description.fil Fil: Ruiz-Trillo, Iñaki. Universitat de Barcelona. Facultat de Biologia. Departament de Genètica, Microbiologia i Estadística; España.
dc.description.fil Fil: Ruiz-Trillo, Iñaki. Universitat de Barcelona. Institut de Recerca de la Biodiversitat (IRBio); España.
dc.description.fil Fil: Ruiz-Trillo, Iñaki. Institución Catalana de Investigación y Estudios Avanzados (ICREA); España.


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