Abstract
The obligate intracellular parasite Toxoplasma gondii replicates in an unusual process, described as internal budding. Multiple dausghter parasites are formed sequentially within a single mother cell, requiring replication and distribution of essential organelles such as micronemes. These organelles are thought to be formed de novo in the developing daughter cells. Using dual labelling of a microneme protein MIC2 and super-resolution microscopy, we show that micronemes are recycled from the mother to the forming daughter parasites using a highly dynamic F-actin network. While this recycling pathway is F-actin dependent, de novo synthesis of micronemes appears to be F-actin independent. The F-actin network connects individual parasites, supports long, multidirectional vesicular transport, and regulates transport, density and localisation of micronemal vesicles. The residual body acts as a storage and sorting station for these organelles. Our data describe an F-actin dependent mechanism in apicomplexans for transport and recycling of maternal organelles during intracellular development.
Highlights
The obligate intracellular parasite Toxoplasma gondii replicates in an unusual process, described as internal budding
A single mitochondrion and apicoplast divide and segregate into the forming daughters tightly coupled to the cell cycle[6], biogenesis of the unique secretory organelles and the Inner Membrane Complex (IMC, a Golgi derived organelle of flattened membrane vesicles that are tightly associated with the subpellicular microtubules and localised beneath the plasma membrane) is tightly linked to the secretory pathway of the parasite[7,8]
When a dual labelling experiment, as described above for micronemal protein 2 (MIC2), was performed, to discriminate maternal from de novo synthesised MyoA (Fig. 5e–g), we found that newly synthesised MyoA, appears in a diffuse cytoplasmic localisation and partially co-localises with maternal MyoA (Fig. 5e–g and intensity profiles 5 h), in good agreement with previous results, arguing for a cytosolic formation of the glideosome complex, which subsequently associates with the IMC of the daughter cells at the final
Summary
The obligate intracellular parasite Toxoplasma gondii replicates in an unusual process, described as internal budding. Multiple dausghter parasites are formed sequentially within a single mother cell, requiring replication and distribution of essential organelles such as micronemes. These organelles are thought to be formed de novo in the developing daughter cells. Recent findings demonstrated that parasites form an extensive nanotubular network in a F-actin[10] and myosin[11] dependent manner that is required for material exchange between individual parasites. This raises the possibility that actin-based vesicular transport mechanisms are involved in daughter cell assembly and recycling of maternal material from the mother to the daughter parasites. The role of parasite F-actin in apicoplast inheritance appears to be conserved, since disruption of Pfact[1] in Plasmodium falciparum results in loss of the apicoplast[17]
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