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Cryo-electron tomography reveals four-membrane architecture of the Plasmodium apicoplast

Leandro Lemgruber1, Mikhail Kudryashev2, Chaitali Dekiwadia3, David T Riglar45, Jake Baum45, Henning Stahlberg2, Stuart A Ralph3* and Friedrich Frischknecht1*

Author Affiliations

1 Parasitology, Department of Infectious Diseases, University of Heidelberg Medical School, Im Neuenheimer Feld 324, Heidelberg 69120, Germany

2 Center for Cellular Imaging and Nano Analytics (C-CINA), Biozentrum, University of Basel, Mattenstrasse 26, Basel, CH-4058, Switzerland

3 Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Victoria 3010, Australia

4 Division of Infection and Immunity, The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, 3052, Australia

5 Department of Medical Biology, University of Melbourne, Parkville, VIC, 3052, Australia

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Malaria Journal 2013, 12:25  doi:10.1186/1475-2875-12-25

Published: 19 January 2013

Abstract

Background

The apicoplast is a plastid organelle derived from a secondary endosymbiosis, containing biosynthetic pathways essential for the survival of apicomplexan parasites. The Toxoplasma apicoplast clearly possesses four membranes but in related Plasmodium spp. the apicoplast has variably been reported to have either three or four membranes.

Methods

Cryo-electron tomography was employed to image merozoites of Plasmodium falciparum and Plasmodium berghei frozen in their near-native state. Three-dimensional reconstructions revealed the number of apicoplast membranes and the association of the apicoplast with other organelles. Routine transmission electron microscopy of parasites preserved by high-pressure freezing followed by freeze substitution techniques was also used to analyse apicoplast morphology.

Results

Cryo-preserved parasites showed clearly four membranes surrounding the apicoplast. A wider gap between the second and third apicoplast membranes was frequently observed. The apicoplast was found in close proximity to the nucleus and to the rhoptries. The apicoplast matrix showed ribosome-sized particles and membranous whorls.

Conclusions

The Plasmodium apicoplast possesses four membranes, as do the apicoplasts of other apicomplexan parasites. This is consistent with a four-membraned secondary endosymbiotic plastid ancestor.

Keywords:
Apicoplast; Cryo-electron tomography; Symbiosis; Organelle interaction; Malaria