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J. Biol. Chem., Vol. 280, Issue 34, 30557-30563, August 26, 2005

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Protein Import, Replication, and Inheritance of a Vestigial Mitochondrion^*

Attila Regoes, Danai Zourmpanou¶, Gloria León-Avila¶||, Mark van der Giezen¶**, Jorge Tovar¶, and Adrian B. Hehl

From the Institute of Parasitology, University of Zürich, Winterthurerstrasse 266a, CH-8057 Zürich, Switzerland and the ^¶School of Biological Sciences, Royal Holloway University of London, Egham Hill, Egham TW20 0EX, United Kingdom

Mitochondrial remnant organelles (mitosomes) that exist in a range of "amitochondrial" eukaryotic organisms represent ideal models for the study of mitochondrial evolution and for the establishment of the minimal set of proteins required for the biogenesis of an endosymbiosis-derived organelle. Giardia intestinalis, often described as the earliest branching eukaryote, contains double membrane-bounded structures involved in iron-sulfur cluster biosynthesis, an essential function of mitochondria. Here we present evidence that Giardia mitosomes also harbor Cpn60, mtHsp70, and ferredoxin and that despite their advanced state of reductive evolution they have retained vestiges of presequence-dependent and -independent protein import pathways akin to those that operate in mammalian mitochondria. Although import of IscU and ferredoxin is still reliant on their amino-terminal presequences, targeting of Giardia Cpn60, IscS, or mtHsp70 into mitosomes no longer requires cleavable presequences, a derived feature from their mitochondrial homologues. In addition, we found that division and segregation of a single centrally positioned mitosome tightly associated with the microtubular cytoskeleton is coordinated with the cell cycle, whereas peripherally located mitosomes are inherited into daughter cells stochastically.

Received for publication, January 21, 2005 , and in revised form, April 18, 2005.

^* This work was supported in part by Swiss National Science Foundation Grant 3100A0-100270 (to A. B. H.) and by Wellcome Trust Grant 059845 (to J. T.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains four supplemental tables.

Both authors contributed equally to this work.

^|| Present address: Departamento de Genética y Biología Molecular, CINVESTAV IPN, 07360 México DF, México.

^** Present address: School of Biological Sciences, Queen Mary University of London, Mile End Rd., London E1 4NS, United Kingdom.

To whom correspondence may be addressed. Tel.: 44-1784-414159; Fax: 44-1784-434326; E-mail: j.tovar{at}rhul.ac.uk.

To whom correspondence may be addressed. Tel.: 41-44-635-8526/30; Fax: 41-44-635-8907; E-mail: Adrian.Hehl{at}access.unizh.ch.

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