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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...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6400420/ https://www.ncbi.nlm.nih.gov/pubmed/30789903 http://dx.doi.org/10.1371/journal.pgen.1007986 |
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author | Ocaña-Pallarès, Eduard Najle, Sebastián R. Scazzocchio, Claudio Ruiz-Trillo, Iñaki |
author_facet | Ocaña-Pallarès, Eduard Najle, Sebastián R. Scazzocchio, Claudio Ruiz-Trillo, Iñaki |
author_sort | Ocaña-Pallarès, Eduard |
collection | PubMed |
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. |
format | Online Article Text |
id | pubmed-6400420 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-64004202019-03-17 Reticulate evolution in eukaryotes: Origin and evolution of the nitrate assimilation pathway Ocaña-Pallarès, Eduard Najle, Sebastián R. Scazzocchio, Claudio Ruiz-Trillo, Iñaki PLoS Genet Research Article 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. Public Library of Science 2019-02-21 /pmc/articles/PMC6400420/ /pubmed/30789903 http://dx.doi.org/10.1371/journal.pgen.1007986 Text en © 2019 Ocaña-Pallarès et al http://creativecommons.org/licenses/by/4.0/ 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. |
spellingShingle | Research Article Ocaña-Pallarès, Eduard Najle, Sebastián R. Scazzocchio, Claudio Ruiz-Trillo, Iñaki 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 |
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_short | 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 |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6400420/ https://www.ncbi.nlm.nih.gov/pubmed/30789903 http://dx.doi.org/10.1371/journal.pgen.1007986 |
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