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

Genes and genomes can evolve through interchanging genetic material, this leading to reticular evolutionary patterns. However, the importance of reticulate evolution in eukaryotes, and in particular of horizontal gene transfer (HGT), remains controversial. Given that metabolic pathways with taxonomi...

Descripción completa

Detalles Bibliográficos
Autores: Ocaña Pallarès, Eduard, 1991-, Najle, Sebastián R., Scazzocchio, Claudio, Ruiz Trillo, Iñaki
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/45122
Acceso en línea:http://hdl.handle.net/10230/45122
http://dx.doi.org/10.1371/journal.pgen.1007986
Access Level:acceso abierto
Palabra clave:Eukaryota
Phylogenetic analysis
Nitrates
Phylogenetics
Protein domains
Sequence alignment
Oomycetes
Evolutionary genetics
id ES_2bc7235d9d9a0b51ebc9ce8fce80ca39
oai_identifier_str oai:repositori.upf.edu:10230/45122
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
title Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
spellingShingle Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
Ocaña Pallarès, Eduard, 1991-
Eukaryota
Phylogenetic analysis
Nitrates
Phylogenetics
Protein domains
Sequence alignment
Oomycetes
Evolutionary genetics
title_short Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
title_full Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
title_fullStr Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
title_full_unstemmed Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
title_sort Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway
dc.creator.none.fl_str_mv Ocaña Pallarès, Eduard, 1991-
Najle, Sebastián R.
Scazzocchio, Claudio
Ruiz Trillo, Iñaki
author Ocaña Pallarès, Eduard, 1991-
author_facet Ocaña Pallarès, Eduard, 1991-
Najle, Sebastián R.
Scazzocchio, Claudio
Ruiz Trillo, Iñaki
author_role author
author2 Najle, Sebastián R.
Scazzocchio, Claudio
Ruiz Trillo, Iñaki
author2_role author
author
author
dc.subject.none.fl_str_mv Eukaryota
Phylogenetic analysis
Nitrates
Phylogenetics
Protein domains
Sequence alignment
Oomycetes
Evolutionary genetics
topic Eukaryota
Phylogenetic analysis
Nitrates
Phylogenetics
Protein domains
Sequence alignment
Oomycetes
Evolutionary genetics
description Genes and genomes can evolve through interchanging genetic material, this leading to reticular evolutionary patterns. However, the importance of reticulate evolution in eukaryotes, 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 previous results revealed a patchy distribution and suggested that the nitrate assimilation cluster 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 previously 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 history, underlying the origin of the canonical eukaryotic nitrate reductase, and of a chimeric nitrate reductase in Ichthyosporea (Opisthokonta). We show that the ichthyosporean pathway, including this novel nitrate reductase, is physiologically active and transcriptionally co-regulated, responding to different nitrogen sources; similarly to distant eukaryotes with independent 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.
publishDate 2019
dc.date.none.fl_str_mv 2019
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/45122
http://dx.doi.org/10.1371/journal.pgen.1007986
url http://hdl.handle.net/10230/45122
http://dx.doi.org/10.1371/journal.pgen.1007986
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv PLoS Genet. 2019; 15(2):e1007986
info:eu-repo/grantAgreement/EC/FP7/616960
info:eu-repo/grantAgreement/ES/1PE/BFU2014-57779-P
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science (PLoS)
publisher.none.fl_str_mv Public Library of Science (PLoS)
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869405179831386112
spelling Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathwayOcaña Pallarès, Eduard, 1991-Najle, Sebastián R.Scazzocchio, ClaudioRuiz Trillo, IñakiEukaryotaPhylogenetic analysisNitratesPhylogeneticsProtein domainsSequence alignmentOomycetesEvolutionary geneticsGenes and genomes can evolve through interchanging genetic material, this leading to reticular evolutionary patterns. However, the importance of reticulate evolution in eukaryotes, 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 previous results revealed a patchy distribution and suggested that the nitrate assimilation cluster 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 previously 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 history, underlying the origin of the canonical eukaryotic nitrate reductase, and of a chimeric nitrate reductase in Ichthyosporea (Opisthokonta). We show that the ichthyosporean pathway, including this novel nitrate reductase, is physiologically active and transcriptionally co-regulated, responding to different nitrogen sources; similarly to distant eukaryotes with independent 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.This work was supported by: -an European Research Council Consolidator Grant (ERC-2012-Co-616960) to IRT https://cordis.europa.eu/project/rcn/185646_en.html https://erc.europa.eu -support from the Secretary's Office for Universities and Research of the Generalitat de Catalunya (project 2014 SGR 619) to Xavier Bellés. http://universitatsirecerca.gencat.cat/en/inici/ -a grant from the Spanish Ministry for Economy and Competitiveness (MINECO; BFU2014-57779-P, with European Regional Development Fund support), to IRT. http://www.mineco.gob.es/portal/site/mineco/?lang_choosen=en -SRN is a member of the Carrera del Investigador Científico from CONICET, Argentina. -EOP was supported by a pre-doctoral FPI grant from MINECO. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Public Library of Science (PLoS)202020202019info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/45122http://dx.doi.org/10.1371/journal.pgen.1007986reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésPLoS Genet. 2019; 15(2):e1007986info:eu-repo/grantAgreement/EC/FP7/616960info:eu-repo/grantAgreement/ES/1PE/BFU2014-57779-P© 2019 Ocaña-Pallarès et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/451222026-06-12T07:21:37Z
score 15,812429

Similares en LA Referencia