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A mitochondrial remnant in the microsporidian Trachipleistophora hominis

Abstract

Microsporidia are obligate intracellular parasites of several eukaryotes. They have a highly complex and unique infection apparatus but otherwise appear structurally simple1. Microsporidia are thought to lack typical eukaryotic organelles, such as mitochondria and peroxisomes. This has been interpreted as support for the hypothesis that these peculiar eukaryotes diverged before the mitochondrial endosymbiosis, which would make them one of the earliest offshoots in eukaryotic evolution2,3. But microsporidial nuclear genes that encode orthologues of typical mitochondrial heatshock Hsp70 proteins have been detected, which provides evidence for secondary loss of the organelle or endosymbiont4,5,6. In addition, gene trees and more sophisticated phylogenetic analyses have recovered microsporidia as the relatives of fungi, rather than as basal eukaryotes7,8,9. Here we show that a highly specific antibody raised against a Trachipleistophora hominis Hsp70 protein detects the presence, under light and electron microscopy, of numerous tiny (50 × 90 nm) organelles with double membranes in this human microsporidial parasite. The finding of relictual mitochondria in microsporidia provides further evidence of the reluctance of eukaryotes to lose the mitochondrial organelle, even when its canonical function of aerobic respiration has been apparently lost.

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Figure 1: Characterization of a T. hominis gene encoding a mitochondrial Hsp70.
Figure 2: Analysis of the expression of the T. hominis Hsp70 in spores and infected and non-infected rabbit kidney (RK13) cells using a rabbit polyclonal antibody against T. hominis Hsp70.
Figure 3: Cellular localization of the T. hominis Hsp70 protein detected in situ using immunofluorescence and confocal microscopy.
Figure 4: Transmission electron microscopy of microsporidian structures.

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Acknowledgements

We thank E. Canning for the T. hominis culture system and advice on growing microsporidia; M. Duchen and A. Ball for help with confocal microscopy; C. Thomson for help with electron microscopy; and C. Danpure and G. Birdsey for comments on the manuscript and help with heterologous transfection experiments. J.M.L. was supported by a Wellcome Trust Research Leave Fellowship and Tenovus Scotland. B.A.P.W. was supported by a Wellcome Trust Biodiversity studentship, R.P.H. was supported by a Wellcome Trust University award.

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Correspondence to T. Martin Embley.

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Williams, B., Hirt, R., Lucocq, J. et al. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865–869 (2002). https://doi.org/10.1038/nature00949

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