Trends in Parasitology
Volume 30, Issue 2, February 2014, Pages 58-64
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Opinion
The flagellar contribution to the apical complex: a new tool for the eukaryotic Swiss Army knife?

https://doi.org/10.1016/j.pt.2013.12.006Get rights and content

Highlights

  • A remarkable confluence of iconic structures contributes to apicomplexan success.

  • The apical complex is an example of flagellum adaptability.

  • Rootlet microtubules close the conoid to begin the path to the perfect pathogen.

Apicomplexa are an ancient group of single-celled pathogens of humans and animals that include the etiological agents of such devastating plagues as malaria, toxoplasmosis, and coccidiosis. The defining feature of the Apicomplexa is the apical complex, the invasion machinery used to gain access to host cells. Evidence gathered from apicomplexans and their closest relatives argues that the apical complex is an extreme example of flagellum adaptability. The value of non-apicomplexan models, such as Chromera velia, is considered in an effort to understand the modern apical complex. The origin of the apical complex is unknown, but recent evidence points to a remarkable contribution from the flagellum to its evolution.

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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