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Microsporidia: why make nucleotides if you can steal them?

Lookup NU author(s): Dr Paul Dean, Professor Robert Hirt, Professor T. Martin Embley

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


Abstract

Microsporidia are strict obligate intracellular parasites that infect a wide range of eukaryotes including humans and economically important fish and insects. Surviving and flourishing inside another eukaryotic cell is a very specialised lifestyle that requires evolutionary innovation. Genome sequence analyses show that microsporidia have lost most of the genes needed for making primary metabolites, such as amino acids and nucleotides, and also that they have only a limited capacity for making adenosine triphosphate (ATP). Since microsporidia cannot grow and replicate without the enormous amounts of energy and nucleotide building blocks needed for protein, DNA, and RNA biosynthesis, they must have evolved ways of stealing these substrates from the infected host cell. Providing they can do this, genome analyses suggest that microsporidia have the enzyme repertoire needed to use and regenerate the imported nucleotides efficiently. Recent functional studies suggest that a critical innovation for adapting to intracellular life was the acquisition by lateral gene transfer of nucleotide transport (NTT) proteins that are now present in multiple copies in all microsporidian genomes. These proteins are expressed on the parasite surface and allow microsporidia to steal ATP and other purine nucleotides for energy and biosynthesis from their host. However, it remains unclear how other essential metabolites, such as pyrimidine nucleotides, are acquired. Transcriptomic and experimental studies suggest that microsporidia might manipulate host cell metabolism and cell biological processes to promote nucleotide synthesis and to maximise the potential for ATP and nucleotide import. In this review, we summarise recent genomic and functional data relating to how microsporidia exploit their hosts for energy and building blocks needed for growth and nucleic acid metabolism and we identify some remaining outstanding questions.


Publication metadata

Author(s): Dean P, Hirt RP, Embley TM

Publication type: Review

Publication status: Published

Journal: PLoS Pathogens

Year: 2016

Volume: 12

Issue: 11

Online publication date: 17/11/2016

Acceptance date: 17/10/2016

ISSN (electronic): 1553-7374

URL: http://dx.doi.org/10.1371/journal.ppat.1005870

DOI: 10.1371/journal.ppat.1005870

PubMed id: 27855212


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