A highly dynamic F-actin network regulates transport and recycling of micronemes in Toxoplasma gondii vacuoles

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.

Fussing About Fission: Defining Variety Among Mainstream and Exotic Apicomplexan Cell Division Modes

“…Although the former informs about maturation and the latter about destabilization, neither informs directly on the basis of differential stability. In parallel, some of the maternal building blocks (e.g., IMC proteins, glideosome) are recycled in the final growth spurt of the daughters (Ouologuem and Roos, 2014;Periz et al, 2019). An additional mechanism is provided by differential components present on either mother [e.g., MSC1b (Lorestani et al, 2012), GAP45 (Gaskins et al, 2004), or IMC7, 12, 14, 17, 18, and20 Anderson-White et al, 2011;Chen A. L. et al, 2015] or daughter parasite [e.g., IMC16, 29 Chen A. L. et al, 2015;Chen et al, 2016], or swapping places from mother to daughter [e.g., SPM3 Samad et al, 2015].…”

“…Like in schizogony, daughter budding occurs in sync with S/M-phase and karyokinesis. Upon emergence of daughters, a narrow cytoplasmic bridge at the basal end remains connected with a residual body containing remnants of the mother cell, which will be largely resorbed into the daughters (Frenal et al, 2017b;Periz et al, 2019). As a result, the daughter parasites remain in contact with each other and could therefore have the false appearance of endopolygeny.…”

Biogenesis and discharge of the rhoptries: Key organelles for entry and hijack of host cells by the Apicomplexa

“…During T. gondii endodyogeny, the secretory organelles are made de novo at a late stage of the division cycle, likely by vesicular trafficking generated from the late Golgi compartment (Nishi et al., 2008) (Figure 2). In addition to the de novo synthesis, daughter micronemes seem also to be recycled from the mother in an F‐actin‐dependent process (Periz et al., 2019). Rhoptry biogenesis relies on the acidification of an endosome‐like compartment (ELC) found halfway between the Golgi apparatus and the apical pole of the parasite (Dubremetz, 2007; Shaw et al., 1998).…”

A brief history of the octopus imaging facility to celebrate its 10th anniversary

“…The expectation in the field was that new cohorts of sub‐cellular organelles would be created de novo in each developing daughter parasite. However, using 3D SIM, Javier Periz and colleagues from Glasgow University showed that organelles, like the secretory (micronemes), are instead recycled from the mother to the daughter parasites via a highly dynamic F‐actin network 74 . This actin network supports long‐range multidirectional vesicular transport between mother and daughters, and regulates density and localisation of micronemal vesicles (Figs.…”