The 3D structure of the apical complex and association with the flagellar apparatus revealed by serial TEM tomography in Psammosa pacifica, a distant relative of the Apicomplexa.

Noriko Okamoto,Patrick J Keeling,Stuart Alexander Ralph

doi:10.1371/journal.pone.0084653

Abstract

The apical complex is one of the defining features of apicomplexan parasites, including the malaria parasite Plasmodium, where it mediates host penetration and invasion. The apical complex is also known in a few related lineages, including several non-parasitic heterotrophs, where it mediates feeding behaviour. The origin of the apical complex is unclear, and one reason for this is that in apicomplexans it exists in only part of the life cycle, and never simultaneously with other major cytoskeletal structures like flagella and basal bodies. Here, we used conventional TEM and serial TEM tomography to reconstruct the three dimensional structure of the apical complex in Psammosa pacifica, a predatory relative of apicomplexans and dinoflagellates that retains the archetype apical complex and the flagellar apparatus simultaneously. The P. pacifica apical complex is associated with the gullet and consists of the pseudoconoid, micronemes, and electron dense vesicles. The pseudoconoid is a convex sheet consisting of eight short microtubules, plus a band made up of microtubules that originate from the flagellar apparatus. The flagellar apparatus consists of three microtubular roots. One of the microtubular roots attached to the posterior basal body is connected to bypassing microtubular strands, which are themselves connected to the extension of the pseudoconoid. These complex connections where the apical complex is an extension of the flagellar apparatus, reflect the ancestral state of both, dating back to the common ancestor of apicaomplexans and dinoflagellates.

Highlights

The apicomplexans are a group of obligate intracellular parasitic protists that includes human parasites such as malaria parasites Plasmodium, a major disease for which about half the world population is at risk [1]
The extended conoid microtubules (ECM) fall between the gullet and the other long vacuole located on the ventral side of the right anterior part of the cell (Fig. 3)
Posterior to the apical complex, the ECM are joined by another set of microtubular strands (MS) that are directly connected to the flagellar apparatus

Summary

Introduction

The apicomplexans are a group of obligate intracellular parasitic protists that includes human parasites such as malaria parasites Plasmodium, a major disease for which about half the world population is at risk [1]. Other major human pathogens include Toxoplasma gondii, which infects up to a third of world population [2], and Cryptosporidium, a major contaminant of drinking water. The apical complex was first observed in thin sectioned Toxoplasma gondii under transmission electron microscopy (TEM) [4] and intensively studied in other apicomplexan parasites from the late 1950’s through the 1970’s (for review, [5,6,7]). The apical complex is fundamental to apicomplexan infection, because it mediates the processes of host attachment and invasion (for recent reviews see [10,11]). The molecular components of the apical complex and their role in the invasion machinery have been intensively investigated based upon cell biological, genomic, transcriptomic, and proteomic information accumulated in the last decade [12,13]

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Discussion

Conclusion