Trends in Parasitology
OpinionThe flagellar contribution to the apical complex: a new tool for the eukaryotic Swiss Army knife?
Section snippets
Apicomplexans: bringing together two iconic structures
Apicomplexan pathogens (see Glossary) are so successful that there is no vertebrate or invertebrate which is not parasitised by at least one species in this group. They form the most diverse group of single-celled pathogens and are responsible for numerous medically and commercially important diseases, including malaria, toxoplasmosis, and coccidiosis (Figure 1). The group is defined by the possession of an apical complex, a collection of cytoskeletal elements and secretory systems used to gain
A tool for all occasions
The solution to many problems encountered during eukaryotic evolution has been the flagellum. Flagella are employed in a vast diversity of conserved and specific roles across eukaryotic phyla 4, 5, 6, 7, 8, 9. In general concept, the flagellum might be considered to be the eukaryotic Swiss Army knife. The tools of such an implement would then be the specific combinations of flagellar form and function exhibited between different lineages, and even between cells of the same organism. Flagellate
The parasite's toolkit
Where the flagellum is conserved across eukaryotic phyla, the apical complex is the defining feature of the apicomplexans, and under some definitions is considered to be restricted to this group. The apical complex is a system of structural and secretory elements that evolved from the feeding apparatus of the free-living ancestors of the apicomplexans (Figure 2) 1, 18. The main role of this system is in host–parasite interactions including host-cell invasion. This role in host-cell invasion
A flagellar contribution to the apical complex
Apicomplexans evolved from free-living, photosynthetic (probably bi-)flagellate algae, as evidenced by their retention of a relict plastid, the apicoplast (Figure 1) [22]. It has long been thought that apicomplexans had mostly dispensed with their flagella. However, mounting evidence suggests that far from losing the flagellum in the apical complex, and particularly in the manner of formation and apportioning during daughter-cell biogenesis, we may be observing one of the most diverged examples
Origins of the apical complex–flagellum association
Repurposing of the flagellar apparatus and the specialisation of the conoid in T. gondii are faits accomplis. What then are the opportunities to investigate the origins of these structures? Although the apical complex is considered to be the defining feature of the Apicomplexa, several related lineages, for instance the perkinsids and some early-diverging dinoflagellates, also exhibit elements of these structures [28]. We can get even closer to the possible ancestral state of the apical complex
Rootlet microtubules close the conoid: path to the perfect pathogen
We hypothesise that, in the ancestral apicomplexan, these rootlet microtubules became integrated with the microtubules of the adjacent open conoid, in effect closing the conoid and beginning evolution of the structure we see in Apicomplexa today. This model might account for the apparent association of the T. gondii SFA fibre with both the conoid and the centriole. So far, there are no reports of striated fibres associated with the flagellar rootlet in C. velia, but given the phylogenetic
Concluding remarks
It is becoming more apparent that in the apical complex Apicomplexa may have added yet another tool to the eukaryotic Swiss Army knife. The flagellum has been studied extensively in numerous organisms over many years, and there is now the potential to leverage this wealth of knowledge to identify and understand novel mechanisms and components of apical complex structure, function, and inheritance. These recent findings also highlight the need for model organisms that give insight into the
Acknowledgements
Support for N.P. is provided by the University of Sydney Postdoctoral Research Fellowship scheme.
Glossary
- Apical complex
- a defining feature of Apicomplexa that comprises a system of structural and secretory elements. Facilitates interaction with the host cell. The main structures in the complex include the rhoptries, micronemes, apical polar ring, and conoid.
- Apical polar ring (APR)
- pivotal component of apical complex of all Apicomplexa; a microtubule-organizing centre. Nucleates the subpellicular microtubules.
- Apicomplexa
- a phylum of single-cell parasites of medical and veterinary importance; comprises
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2021, International Journal for ParasitologyCitation Excerpt :Numerous proteins found in the conoid and associated structures are conserved throughout the apicomplexan phylum and their nearest free-living relatives, suggesting that their functions may be ancient and broadly conserved (Bertiaux et al., 2021; Koreny et al., 2021). Curiously, some conoid-associated proteins have homology to proteins that function in flagella, suggesting that the conoid may represent a highly modified flagellum (Francia et al., 2012; de Leon et al., 2013; Portman and Šlapeta, 2014). The rhoptries are long, club-shaped organelles that emerge from the conoid region and stretch, in some instances, “as far as the nucleus” (Fig. 5A–C).
Photoparasitism as an Intermediate State in the Evolution of Apicomplexan Parasites
2020, Trends in ParasitologyCitation Excerpt :They are fully phototrophic, with plastid characterized by the absence of chlorophyll c, a pigment typical for algae with a rhodophyte-derived plastid [10,11]. Although the two species are the closest phototrophic relatives within apicomonads [9], they differ substantially in their morphology [10,11,19–23]; life cycles [10,11,21,23]; nuclear [24], plastid [25], and mitochondrial genomes [26]; and likely also their lifestyles. While an apical complex reduced to the form of the pre-conoid was found in C. velia [21,22], any such structure is absent from V. brassicaformis [23].
Evolution, Composition, Assembly, and Function of the Conoid in Apicomplexa
2020, Trends in ParasitologyCitation Excerpt :Very similar structures are seen in the related Chromera velia in which, moreover, a central pair of intraconoidal microtubules runs down the middle of the pseudoconoid, as is seen in Toxoplasma [85,86]. This apical complex is in close proximity to the flagella, and some pseudoconoid microtubules are continuous with, and seemingly part of, the flagellar rootlet fibers [87]. Unlike Colpodella, Chromera is photosynthetic, but while it is associated with coral communities [88] any direct interactions with animals or other organisms are poorly understood.
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2019, Trends in ParasitologyNovel cytoskeletal traits in the intestinal parasites (Squirmida, Platyproteum vivax) of Pacific peanut worms (Sipuncula, Phascolosoma agassizii)
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