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MBE Advance Access originally published online on April 25, 2003
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Mol. Biol. Evol. 20(7):1051-1061. 2003
DOI: 10.1093/molbev/msg103
© 2003 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038

Fungal Hydrogenosomes Contain Mitochondrial Heat-Shock Proteins

Mark van der Giezen*,1, Graeme M. Birdsey{dagger}, David S. Horner*,2, John Lucocq{ddagger}, Patricia L. Dyal*, Marlene Benchimol§, Christopher J. Danpure{dagger} and T. Martin Embley*,

* Department of Zoology, The Natural History Museum, London, United Kingdom
{dagger} Department of Biology, University College London, London, United Kingdom
{ddagger} School of Life Sciences, University of Dundee, Dundee, United Kingdom
§ Universidade Santa Ursula, Rio de Janeiro, Brazil

E-mail: tme{at}nhm.ac.uk.

At least three groups of anaerobic eukaryotes lack mitochondria and instead contain hydrogenosomes, peculiar organelles that make energy and excrete hydrogen. Published data indicate that ciliate and trichomonad hydrogenosomes share common ancestry with mitochondria, but the evolutionary origins of fungal hydrogenosomes have been controversial. We have now isolated full-length genes for heat shock proteins 60 and 70 from the anaerobic fungus Neocallimastix patriciarum, which phylogenetic analyses reveal share common ancestry with mitochondrial orthologues. In aerobic organisms these proteins function in mitochondrial import and protein folding. Homologous antibodies demonstrated the localization of both proteins to fungal hydrogenosomes. Moreover, both sequences contain amino-terminal extensions that in heterologous targeting experiments were shown to be necessary and sufficient to locate both proteins and green fluorescent protein to the mitochondria of mammalian cells. This finding, that fungal hydrogenosomes use mitochondrial targeting signals to import two proteins of mitochondrial ancestry that play key roles in aerobic mitochondria, provides further strong evidence that the fungal organelle is also of mitochondrial ancestry. The extraordinary capacity of eukaryotes to repeatedly evolve hydrogen-producing organelles apparently reflects a general ability to modify the biochemistry of the mitochondrial compartment.

Key Words: heat-shock proteins • hydrogenosomes • mitochondria • anaerobic eukaryotes • evolution


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