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The dynamic intein landscape of eukaryotes

BACKGROUND: Inteins are mobile, self-splicing sequences that interrupt proteins and occur across all three domains of life. Scrutiny of the intein landscape in prokaryotes led to the hypothesis that some inteins are functionally important. Our focus shifts to eukaryotic inteins to assess their diver...

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Detalles Bibliográficos
Autores principales: Green, Cathleen M., Novikova, Olga, Belfort, Marlene
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5784728/
https://www.ncbi.nlm.nih.gov/pubmed/29416568
http://dx.doi.org/10.1186/s13100-018-0111-x
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author Green, Cathleen M.
Novikova, Olga
Belfort, Marlene
author_facet Green, Cathleen M.
Novikova, Olga
Belfort, Marlene
author_sort Green, Cathleen M.
collection PubMed
description BACKGROUND: Inteins are mobile, self-splicing sequences that interrupt proteins and occur across all three domains of life. Scrutiny of the intein landscape in prokaryotes led to the hypothesis that some inteins are functionally important. Our focus shifts to eukaryotic inteins to assess their diversity, distribution, and dissemination, with the aim to comprehensively evaluate the eukaryotic intein landscape, understand intein maintenance, and dissect evolutionary relationships. RESULTS: This bioinformatics study reveals that eukaryotic inteins are scarce, but present in nuclear genomes of fungi, chloroplast genomes of algae, and within some eukaryotic viruses. There is a preponderance of inteins in several fungal pathogens of humans and plants. Inteins are pervasive in certain proteins, including the nuclear RNA splicing factor, Prp8, and the chloroplast DNA helicase, DnaB. We find that eukaryotic inteins frequently localize to unstructured loops of the host protein, often at highly conserved sites. More broadly, a sequence similarity network analysis of all eukaryotic inteins uncovered several routes of intein mobility. Some eukaryotic inteins appear to have been acquired through horizontal transfer with dsDNA viruses, yet other inteins are spread through intragenomic transfer. Remarkably, endosymbiosis can explain patterns of DnaB intein inheritance across several algal phyla, a novel mechanism for intein acquisition and distribution. CONCLUSIONS: Overall, an intriguing picture emerges for how the eukaryotic intein landscape arose, with many evolutionary forces having contributed to its current state. Our collective results provide a framework for exploring inteins as novel regulatory elements and innovative drug targets. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13100-018-0111-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-57847282018-02-07 The dynamic intein landscape of eukaryotes Green, Cathleen M. Novikova, Olga Belfort, Marlene Mob DNA Research BACKGROUND: Inteins are mobile, self-splicing sequences that interrupt proteins and occur across all three domains of life. Scrutiny of the intein landscape in prokaryotes led to the hypothesis that some inteins are functionally important. Our focus shifts to eukaryotic inteins to assess their diversity, distribution, and dissemination, with the aim to comprehensively evaluate the eukaryotic intein landscape, understand intein maintenance, and dissect evolutionary relationships. RESULTS: This bioinformatics study reveals that eukaryotic inteins are scarce, but present in nuclear genomes of fungi, chloroplast genomes of algae, and within some eukaryotic viruses. There is a preponderance of inteins in several fungal pathogens of humans and plants. Inteins are pervasive in certain proteins, including the nuclear RNA splicing factor, Prp8, and the chloroplast DNA helicase, DnaB. We find that eukaryotic inteins frequently localize to unstructured loops of the host protein, often at highly conserved sites. More broadly, a sequence similarity network analysis of all eukaryotic inteins uncovered several routes of intein mobility. Some eukaryotic inteins appear to have been acquired through horizontal transfer with dsDNA viruses, yet other inteins are spread through intragenomic transfer. Remarkably, endosymbiosis can explain patterns of DnaB intein inheritance across several algal phyla, a novel mechanism for intein acquisition and distribution. CONCLUSIONS: Overall, an intriguing picture emerges for how the eukaryotic intein landscape arose, with many evolutionary forces having contributed to its current state. Our collective results provide a framework for exploring inteins as novel regulatory elements and innovative drug targets. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13100-018-0111-x) contains supplementary material, which is available to authorized users. BioMed Central 2018-01-24 /pmc/articles/PMC5784728/ /pubmed/29416568 http://dx.doi.org/10.1186/s13100-018-0111-x Text en © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Green, Cathleen M.
Novikova, Olga
Belfort, Marlene
The dynamic intein landscape of eukaryotes
title The dynamic intein landscape of eukaryotes
title_full The dynamic intein landscape of eukaryotes
title_fullStr The dynamic intein landscape of eukaryotes
title_full_unstemmed The dynamic intein landscape of eukaryotes
title_short The dynamic intein landscape of eukaryotes
title_sort dynamic intein landscape of eukaryotes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5784728/
https://www.ncbi.nlm.nih.gov/pubmed/29416568
http://dx.doi.org/10.1186/s13100-018-0111-x
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