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Eukaryotic Cell, April 2005, p. 814-826, Vol. 4, No. 4
1535-9778/05/$08.00+0     doi:10.1128/EC.4.4.814-826.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Maternal Inheritance and Stage-Specific Variation of the Apicoplast in Toxoplasma gondii during Development in the Intermediate and Definitive Host

David J. P. Ferguson,1* Fiona L. Henriquez,2 Michael J. Kirisits,3 Stephen P. Muench,4 Sean T. Prigge,5 David W. Rice,4 Craig W. Roberts,2 and Rima L. McLeod3*

Department of Pathology, University of Oxford, John Radcliffe Hospital, Oxford,1 Department of Immunology, University of Strathclyde, Glasgow,2 Department of Molecular Biology and Biotechnology, The University of Sheffield, Sheffield, United Kingdom,4 Department of Ophthalmology and Visual Sciences, University of Chicago, Chicago, Illinois,3 School of Public Health, Johns Hopkins University, Baltimore, Maryland5

Received 13 January 2005/ Accepted 25 January 2005

The structure and location of Toxoplasma gondii apicoplasts were examined in intermediate and definitive hosts and shown to vary in a stage-specific manner. Immunocytochemistry and electron microscopy studies were used to identify changes in the morphology of apicoplasts and in their enoyl reductase (ENR) content during asexual and sexual development. Apicoplasts in tachyzoites were small, multimembraned organelles anterior to nuclei that divided and segregated with the nuclei during endodyogeny. In nonproliferating bradyzoites within mature tissue cysts (1 to 24 months), apicoplasts had high levels of ENR. During coccidian development, asexual multiplication (endopolygeny), resulting in simultaneous formation of up to 30 daughters (merozoites), involved an initial growth phase associated with repeated nuclear divisions during which apicoplasts appeared as single, elongated, branched structures with increased levels of ENR. At initiation of merozoite formation, enlarged apicoplasts divided simultaneously, with constrictions, into portions that segregated to developing daughters. In sexual stages, apicoplast division did not occur during microgametogony, and apicoplasts were absent from the microgametes that were formed. In contrast, during macrogametogony, the apicoplast appeared as a large, branched, perinuclear structure that had very high levels of ENR in the absence of nuclear division. Marked increases in the size of apicoplasts and levels of ENR may be related to requirements of the macrogametocytes to synthesize and store all components necessary for oocyst formation and subsequent extracellular sporulation. Thus, it is shown that apicoplasts are present and contain ENR in all T. gondii life cycle stages except microgametes, which will result in maternal inheritance of the organelle.

* Corresponding author. Mailing address for Rima L. McLeod: The University of Chicago, 5841 S. Maryland Ave. (MC2114), AMB S-208, Chicago, IL 60637. Phone: (773) 834-4152. Fax: (773) 834-3577. E-mail: rmcleod{at}midway.uchicago.edu. Mailing address for David Ferguson: Nuffield Department of Pathology, Level 1, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom. Phone: 44 1865 220 514. Fax: 44 1865 220 033. E-mail: david.ferguson{at}ndcls.ox.ac.uk.

Eukaryotic Cell, April 2005, p. 814-826, Vol. 4, No. 4
1535-9778/05/$08.00+0     doi:10.1128/EC.4.4.814-826.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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