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Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole

Authors

  • Kildare Miranda,

    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
    2. Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941, Brazil.
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    • Both authors contributed equally.

  • Douglas A. Pace,

    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
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    • Both authors contributed equally.

  • Roxana Cintron,

    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
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  • Juliany C. F. Rodrigues,

    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
    2. Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941, Brazil.
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  • Jianmin Fang,

    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
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  • Alyssa Smith,

    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
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  • Peter Rohloff,

    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
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  • Elvis Coelho,

    1. Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941, Brazil.
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  • Felix De Haas,

    1. FEI Nanoport, Eindhoven, The Netherlands.
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  • Wanderley De Souza,

    1. Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941, Brazil.
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  • Isabelle Coppens,

    1. Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USA.
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  • L. David Sibley,

    1. Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110, USA.
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  • Silvia N. J. Moreno

    Corresponding author
    1. Center for Tropical and Emerging Global Diseases and Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
      E-mail smoreno@cb.uga.edu; Tel. (+706) 542 4736; Fax (+706) 542 9493.
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E-mail smoreno@cb.uga.edu; Tel. (+706) 542 4736; Fax (+706) 542 9493.

Summary

Toxoplasma gondii belongs to the phylum Apicomplexa and is an important cause of congenital disease and infection in immunocompromised patients. Like most apicomplexans, T. gondii possesses several plant-like features, such as the chloroplast-like organelle, the apicoplast. We describe and characterize a novel organelle in T. gondii tachyzoites, which is visible by light microscopy and possesses a broad similarity to the plant vacuole. Electron tomography shows the interaction of this vacuole with other organelles. The presence of a plant-like vacuolar proton pyrophosphatase (TgVP1), a vacuolar proton ATPase, a cathepsin L-like protease (TgCPL), an aquaporin (TgAQP1), as well as Ca2+/H+ and Na+/H+ exchange activities, supports similarity to the plant vacuole. Biochemical characterization of TgVP1 in enriched fractions shows a functional similarity to the respective plant enzyme. The organelle is a Ca2+ store and appears to have protective effects against salt stress potentially linked to its sodium transport activity. In intracellular parasites, the organelle fragments, with some markers colocalizing with the late endosomal marker, Rab7, suggesting its involvement with the endocytic pathway. Studies on the characterization of this novel organelle will be relevant to the identification of novel targets for chemotherapy against T. gondii and other apicomplexan parasites as well.

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