Motility in blastogregarines (Apicomplexa): Native and drug-induced organisation of Siedleckia nematoides cytoskeletal elements

Abstract

Recent studies on motility of Apicomplexa concur with the so-called glideosome concept applied for apicomplexan zoites, describing a unique mechanism of substrate-dependent gliding motility facilitated by a conserved form of actomyosin motor and subpellicular microtubules. In contrast, the gregarines and blastogregarines exhibit different modes and mechanisms of motility, correlating with diverse modifications of their cortex. This study focuses on the motility and cytoskeleton of the blastogregarine Siedleckia nematoides Caullery et Mesnil, 1898 parasitising the polychaete Scoloplos cf. armiger (Müller, 1776). The blastogregarine moves independently on a solid substrate without any signs of gliding motility; the motility in a liquid environment (in both the attached and detached forms) rather resembles a sequence of pendular, twisting, undulation, and sometimes spasmodic movements. Despite the presence of key glideosome components such as pellicle consisting of the plasma membrane and the inner membrane complex, actin, myosin, subpellicular microtubules, micronemes and glycocalyx layer, the motility mechanism of S. nematoides differs from the glideosome machinery. Nevertheless, experimental assays using cytoskeletal probes proved that the polymerised forms of actin and tubulin play an essential role in the S. nematoides movement. Similar to Selenidium archigregarines, the subpellicular microtubules organised in several layers seem to be the leading motor structures in blastogregarine motility. The majority of the detected actin was stabilised in a polymerised form and appeared to be located beneath the inner membrane complex. The experimental data suggest the subpellicular microtubules to be associated with filamentous structures (= cross-linking protein complexes), presumably of actin nature.

Gregarine single-cell transcriptomics reveals differential mitochondrial remodeling and adaptation in apicomplexans

“…However, gregarines complicate our understanding of these structures despite there being relatively few ultrastructural studies compared to their vast diversity. Cristae have been observed in the mitochondria of some archigregarines and blastogregarines [ 21 , 76 , 77 ], which are both lineages that retain a complete ETC (Fig. 2 ).…”

Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles

“…The use of the apical complex in extracellular attachment and secretion in the gut epithelium of animal hosts, for example, may have triggered convergent expansion in the cell size of gregarine, Digyalum and Symbiont X trophonts. Unsurprisingly, convergent similarities in the three lineages are accompanied by considerable differences in detailed morphology: Digyalum and Symbiont X do not glide or twist but they pulsate, and detailed ultrastructure of their apical complex and pellicle (Dyson et al, 1994; Dyson et al, 1993) (unpublished data) is distinct from that in gregarines (Kováčiková et al, 2017; Paskerova et al, 2018; Valigurová et al, 2017). Similar divergence characterizes their molecular make-ups: apicomplexans are well-known auxotrophs for purines, but Digyalum contains a pathway for their synthesis (data not shown) and, despite that both lineages lost photosynthesis, their plastid genomes have been reduced in different ways (Figure 3C).…”

Alveolar proteins stabilize cortical microtubules in Toxoplasma gondii

“…Microtubules lend structure, rigidity, and polarity to processes ranging from cell division to vesicular trafficking in eukaryotic cells. Unicellular organisms often display elaborate cytoskeletal adaptations that frequently involve the organisation of membranes around microtubule arrays 1–4 . Cortical microtubule arrays are frequently found subtending the plasmalemma of diverse organisms including alveolates, trypanosomes, and flatworm spermatozoa.…”