A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi.

TitleA novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi.
Publication TypeJournal Article
Year of Publication2008
AuthorsTsaousis, AD, Kunji, ERS, Goldberg, AV, Lucocq, JM, Hirt, RP, T Embley, M
JournalNature
Volume453
Issue7194
Pagination553-6
Date Published2008 May 22
ISSN1476-4687
KeywordsAdenosine Triphosphate, Animals, Biological Transport, Carrier Proteins, Cell Line, Encephalitozoon cuniculi, Escherichia coli, Fungal Proteins, Genome, Fungal, Genome, Mitochondrial, Mitochondria, Models, Biological, Molecular Sequence Data, Rabbits, Rats, Symbiosis
Abstract

Mitochondria use transport proteins of the eukaryotic mitochondrial carrier family (MCF) to mediate the exchange of diverse substrates, including ATP, with the host cell cytosol. According to classical endosymbiosis theory, insertion of a host-nuclear-encoded MCF transporter into the protomitochondrion was the key step that allowed the host cell to harvest ATP from the enslaved endosymbiont. Notably the genome of the microsporidian Encephalitozoon cuniculi has lost all of its genes for MCF proteins. This raises the question of how the recently discovered microsporidian remnant mitochondrion, called a mitosome, acquires ATP to support protein import and other predicted ATP-dependent activities. The E. cuniculi genome does contain four genes for an unrelated type of nucleotide transporter used by plastids and bacterial intracellular parasites, such as Rickettsia and Chlamydia, to import ATP from the cytosol of their eukaryotic host cells. The inference is that E. cuniculi also uses these proteins to steal ATP from its eukaryotic host to sustain its lifestyle as an obligate intracellular parasite. Here we show that, consistent with this hypothesis, all four E. cuniculi transporters can transport ATP, and three of them are expressed on the surface of the parasite when it is living inside host cells. The fourth transporter co-locates with mitochondrial Hsp70 to the E. cuniculi mitosome. Thus, uniquely among eukaryotes, the traditional relationship between mitochondrion and host has been subverted in E. cuniculi, by reductive evolution and analogous gene replacement. Instead of the mitosome providing the parasite cytosol with ATP, the parasite cytosol now seems to provide ATP for the organelle.

DOI10.1038/nature06903
Alternate JournalNature
Citation Key10.1038/nature06903
PubMed ID18449191
Grant ListMC_U105663139 / / Medical Research Council / United Kingdom