Evolution, Composition, Assembly, and Function of the Conoid in Apicomplexa

Abstract

The phylum Apicomplexa has been defined by the presence of the apical complex, a structure composed of secretory organelles and specific cytoskeletal elements. A conspicuous feature of the apical complex in many apicomplexans is the conoid, a hollow tapered barrel structure composed of tubulin fibers. In Toxoplasma gondii, the apical complex is a central site of convergence for calcium-related and lipid-mediated signaling pathways that coordinate conoid protrusion, microneme secretion and actin polymerization, to initiate gliding motility. Through cutting-edge technologies, great progress has recently been made in discovering the structural subcomponents and proteins implicated in the biogenesis and stability of the apical complex and, in turn, these discoveries shed new light on the function and evolution of this definitive structure. HighlightsRecent methods, such as proximity labeling, localization of organelle proteins by isotope tagging, and ultrastructure expansion microscopy, have greatly advanced the proteomic characterization of the different apical complex subcompartments.The subpellicular microtubules (SPMTs) are decorated by unique microtubule associated proteins and emerge from the apical polar ring (APR) by an unknown mechanism. The conoid is composed of open tubulin fibers that are bent by the recently characterized DCX protein.Recently characterized proteins, such as AC9, AC10, and ERK7, are essential for the stability of the APR, the conoid, and the SPMTs.In addition to its structural complexity, the apical complex acts as a signaling hub by being the point of convergence for many regulatory pathways.Broad evidence suggests that the conoid is derived from the flagellar root apparatus.

Expansion Microscopy provides new insights into the cytoskeleton of malaria parasites including the conservation of a conoid

“…Another characteristic of the T. gondii conoid lies in its ability to protrude through the apical polar ring upon stimulation of secretion and motility 33 . We thus tested whether the ATR position was linked to the motility of ookinete by comparing its position in motile and non-motile ookinetes ( Figure 4F-J ).…”

“…First, the ATR co-localises closely with the SAS6L ring 30 that was previously shown to be associated with the conoid in T. gondii 29 . Second, the ATR position relative to the APR depends on the activation of ookinete motility and secretion, a characteristic reminiscent of the enigmatic protrusion of the conoid that happens upon activation of secretion and motility in T. gondii tachyzoites 33 . Third, the ATR is associated with at least one additional tightly apposed ring that may correspond to one of the so-called preconoidal rings in T. gondii .…”

“…Interestingly, while MyoB is also expressed in schizonts 31 , the ATR/SAS6L ring is not observed at this stage 30 , further confirming that the Plasmodium apical complex shows stage-specific variations in its composition, as previously proposed 25,30 . In addition to SAS6L and MyoB, multiple other proteins associated with the conoid in T. gondii are expressed in Plasmodium 25,33 and we expect that U-ExM will allow to define their exact position in the Plasmodium apical complex.…”

Conservation of theToxoplasmaconoid complex proteome reveals a cryptic conoid inPlasmodiumthat differentiates between blood- and vector-stage zoites

“…Key to the successful parasitic strategies of apicomplexans is the apical complex-a specialisation of the cell apical cortex that coordinates the interaction and penetration of host cells [5]. Most of the apicomplexan cell is encased in a pellicle structure of flattened membrane vesicles beneath the plasma membrane, as are all members of the infrakingdom Alveolata including dinoflagellates and ciliates [6].…”

“…One is that we have little insight into the function of the conoid, so the consequences of its loss are difficult to predict. The other is that we still know relatively little of the molecular composition of the conoid that would allow the objective testing for the presence of a homologous structure [5]. The conspicuous ultrastructure of conoids such as those of coccidians draw attention to tubulin being a major element, however it is known that there are other conoid proteins responsible for its assembly, stability, and function during invasion [24,[28][29][30][31][32][33][34][35].…”