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Multi-membrane-bound structures of Apicomplexa: I. the architecture of the Toxoplasma gondii apicoplast

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Abstract

Apicomplexan parasites carry a plastid-like organelle termed apicoplast. The previous documentation of four membranes bordering the Toxoplasma gondii apicoplast suggested a secondary endosymbiotic ancestry of this organelle. However, a four-membraned apicoplast wall could not be confirmed for all Apicomplexa including the malarial agents. The latter reportedly possesses a mostly tri-laminar plastid wall but also displays two multi-laminar wall partitions. Since these sectors apparently evolved from regional wall membrane infoldings, the malarial plastid could have lost one secondary wall membrane in the course of evolution. Such wall construction was however not unambiguously resolved. To examine whether the wall of the T. gondii apicoplast is comparably complex, serial ultra-thin sections of tachyzoites were analyzed. This investigation revealed a single pocket-like invagination within a four-laminar wall segment but also disclosed that four individual membranes do not surround the entire T. gondii apicoplast. Instead, this organelle possesses an extensive sector that is bordered by two membranes. Such heterogeneous wall construction could be explained if the inner two membranes of a formerly four-membraned endosymbiont are partially lost. However, our findings are more consistent with an essentially dual-membraned organelle that creates four-laminar wall sectors by expansive infoldings of its interior border. Given this architecture, the T. gondii apicoplast depicts a residual primary plastid not a secondary one as presently proposed.

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Acknowledgements

The author thanks John Boothroyd, Iain Wilson and Heinz Mehlhorn for critical reading of the manuscript and David Ferguson, Günter Schmahl and IngeLatka for technical support and assistance. This project was supported by the Heinrich Heine University of Düsseldorf and through a grant of the Deutsche Forschungsgemeinschaft (Ko1871/1–1).

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  1. Institute for Zoomorphology, Cell Biology and Parasitology, Heinrich Heine Universität Düsseldorf, Universitätsstrasse 1, 40225, Düsseldorf, Germany

    Sabine Köhler

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Köhler, S. Multi-membrane-bound structures of Apicomplexa: I. the architecture of the Toxoplasma gondii apicoplast. Parasitol Res 96, 258–272 (2005). https://doi.org/10.1007/s00436-005-1338-2

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