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