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MBE Advance Access published online on April 25, 2003
Molecular Biology and Evolution, doi:10.1093/molbev/msg103
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2003; all rights reserved
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Accepted February 5, 2003
© 2003 Society for Molecular Biology and Evolution

Original Articles

Fungal Hydrogenosomes Contain Mitochondrial Heat-Shock Proteins

Mark van der Giezen 1, Graeme M. Birdsey 2, David S. Horner 1, John Lucocq 3, Patricia L. Dyal 1, Marlene Benchimol 4, Christopher J. Danpure 2, T. Martin Embley 1*

1 Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
2 Department of Biology, University College London, Gower Street, London WC1E 6BT, UK
3 School of Life Sciences, WTB/MSI complex, University of Dundee, Dundee DD1 5EH, UK
4 Universidade Santa Ursula, Rua Jornalista Orlando Dantas, 59, CEP 222-31-010, Botafogo, Rio de Janeiro, Brazil

* To whom correspondence should be addressed. E-mail: tme{at}nhm.ac.uk.


  Abstract

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 Hsp60 and Hsp70 proteins 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. The 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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