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Transporter gene acquisition and innovation in the evolution of Microsporidia intracellular parasites

Lookup NU author(s): Dr Paul Dean, Dr Kacper Sendra, Dr Tom Williams, Andrew Watson, Dr Peter Major, Dr Sirintra Nakjang, Ekaterina Kozhevnikova, Professor Robert HirtORCiD, Emeritus Professor T. Martin Embley FMedSci FRSORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

The acquisition of genes by horizontal transfer can impart entirely new biological functions and provide an important route to major evolutionary innovation. Here we have used ancient gene reconstruction and functional assays to investigate the impact of a single horizontally transferred nucleotide transporter into the common ancestor of the Microsporidia, a major radiation of intracellular parasites of animals and humans. We show that this transporterprovided early microsporidians with the ability to steal host ATP and to become energy parasites. Gene duplication enabled the diversification of nucleotide transporter function to transport new substrates, including GTP and NAD+, and to evolve the proton-energised net import of nucleotides for nucleic acid biosynthesis, growth and replication. These innovations have allowed the loss of pathways for mitochondrial and cytosolic energy generation and nucleotide biosynthesis that are otherwise essential for free-living eukaryotes, resulting in the highly unusual and reduced cells and genomes of contemporary Microsporidia.


Publication metadata

Author(s): Dean P, Sendra KM, Williams TA, Watson AK, Major P, Nakjang S, Kozhevnikova E, Goldberg AV, Kunji ERS, Hirt RP, Embley TM

Publication type: Article

Publication status: Published

Journal: Nature Communications

Year: 2018

Volume: 9

Online publication date: 27/04/2018

Acceptance date: 22/03/2018

Date deposited: 01/05/2018

ISSN (electronic): 2041-1723

Publisher: Nature Publishing Group

URL: https://doi.org/10.1038/s41467-018-03923-4

DOI: 10.1038/s41467-018-03923-4

PubMed id: 29703975


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Funding

Funder referenceFunder name
089803/Z/09/ZWellcome Trust
ERC 2010-268701

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