Apicomplexa are unicellular eukaryotes that parasitise a wide spectrum of invertebrates and vertebrates, including humans. In their hosts, they occupy a variety of niches, from extracellular cavities (intestine, coelom) to epicellular and intracellular locations, depending on the species and/or developmental stages. During their evolution, Apicomplexa thus developed an exceptionally wide range of unique features to reach these diversified parasitic niches and to survive there, at least long enough to ensure their own transmission or that of their progeny. This review summarises the current state of knowledge on the attachment/invasive and nutrient uptake strategies displayed by apicomplexan parasites, focusing on trophozoite stages of their so far poorly studied basal representatives, which mostly parasitise invertebrate hosts. We describe their most important morphofunctional features, and where applicable, discuss existing major similarities and/or differences in the corresponding mechanisms, incomparably better described at the molecular level in the more advanced Apicomplexa species, of medical and veterinary significance, which mainly occupy intracellular niches in vertebrate hosts.

• Keywords
• apical complex, attachment, epimerite, feeder organelle, mucron, myzocytosis, nutrition, parasitophorous vacuole/sac, pores, trophozoite,
• Publication type
• Journal Article MeSH
• Review MeSH

This study focused on the attachment strategy, cell structure and the host-parasite interactions of the protococcidian Eleutheroschizon duboscqi, parasitising the polychaete Scoloplos armiger. The attached trophozoites and gamonts of E. duboscqi were detected at different development stages. The parasite develops epicellularly, covered by a host cell-derived, two-membrane parasitophorous sac forming a caudal tipped appendage. Staining with Evans blue suggests that this tail is protein-rich, supported by the presence of a fibrous substance in this area. Despite the ultrastructural evidence for long filaments in the tail, it stained only weakly for F-actin, while spectrin seemed to accumulate in this area. The attachment apparatus consists of lobes arranged in one (trophozoites) or two (gamonts) circles, crowned by a ring of filamentous fascicles. During trophozoite maturation, the internal space between the parasitophorous sac and parasite turns translucent, the parasite trilaminar pellicle seems to reorganise and is covered by a dense fibrous glycocalyx. The parasite surface is organised in broad folds with grooves in between. Micropores are situated at the bottom of the grooves. A layer of filaments organised in bands, underlying the folds and ending above the attachment fascicles, was detected just beneath the pellicle. Confocal microscopy, along with the application of cytoskeletal drugs (jasplakinolide, cytochalasin D, oryzalin) confirmed the presence of actin and tubulin polymerised forms in both the parasitophorous sac and the parasite, while myosin labelling was restricted to the sac. Despite positive tubulin labelling, no microtubules were detected in mature stages. The attachment strategy of E. duboscqi shares features with that of cryptosporidia and gregarines, i.e. the parasite itself conspicuously resembles an epicellularly located gregarine, while the parasitophorous sac develops in a similar manner to that in cryptosporidia. This study provides a re-evaluation of epicellular development in other apicomplexans and directly compares their niche with that of E. duboscqi.

• MeSH
• Actins ultrastructure   MeSH
• Apicomplexa classification   physiology   ultrastructure   MeSH
• Host-Parasite Interactions MeSH
• Polychaeta parasitology   MeSH
• Protozoan Proteins ultrastructure   MeSH
• Trophozoites physiology   MeSH
• Tubulin ultrastructure   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Actins MeSH
• Protozoan Proteins MeSH
• Tubulin MeSH

BACKGROUND: In the past decades, many studies focused on the cell motility of apicomplexan invasive stages as they represent a potential target for chemotherapeutic intervention. Gregarines (Conoidasida, Gregarinasina) are a heterogeneous group that parasitize invertebrates and urochordates, and are thought to be an early branching lineage of Apicomplexa. As characteristic of apicomplexan zoites, gregarines are covered by a complicated pellicle, consisting of the plasma membrane and the closely apposed inner membrane complex, which is associated with a number of cytoskeletal elements. The cell cortex of eugregarines, the epicyte, is more complicated than that of other apicomplexans, as it forms various superficial structures. RESULTS: The epicyte of the eugregarines, Gregarina cuneata, G. polymorpha and G. steini, analysed in the present study is organised in longitudinal folds covering the entire cell. In mature trophozoites and gamonts, each epicytic fold exhibits similar ectoplasmic structures and is built up from the plasma membrane, inner membrane complex, 12-nm filaments, rippled dense structures and basal lamina. In addition, rib-like myonemes and an ectoplasmic network are frequently observed. Under experimental conditions, eugregarines showed varied speeds and paths of simple linear gliding. In all three species, actin and myosin were associated with the pellicle, and this actomyosin complex appeared to be restricted to the lateral parts of the epicytic folds. Treatment of living gamonts with jasplakinolide and cytochalasin D confirmed that actin actively participates in gregarine gliding. Contributions to gliding of specific subcellular components are discussed. CONCLUSIONS: Cell motility in gregarines and other apicomplexans share features in common, i.e. a three-layered pellicle, an actomyosin complex, and the polymerisation of actin during gliding. Although the general architecture and supramolecular organisation of the pellicle is not correlated with gliding rates of eugregarines, an increase in cytoplasmic mucus concentration is correlated. Furthermore, our data suggest that gregarines utilize several mechanisms of cell motility and that this is influenced by environmental conditions.

• Publication type
• Journal Article MeSH

BACKGROUND: Gregarines represent a very diverse group of early emerging apicomplexans, parasitising numerous invertebrates and urochordates, and are considered of little practical significance. Recently, they have gained more attention since some analyses showed that cryptosporidia are more closely related to the gregarines than to coccidia. METHODOLOGY/PRINCIPAL FINDINGS: Using a combined microscopic approach, this study points out the spectacular strategy of Gregarina cuneata for attachment to host tissue and nutrient acquisition while parasitising the intestine of yellow mealworm larvae, and reveals the unusual dynamics of cellular interactions between the host epithelium and parasite feeding stages. Trophozoites of G. cuneata develop epicellularly, attached to the luminal side of the host epithelial cell by an epimerite exhibiting a high degree of morphological variability. The presence of contractile elements in the apical region of feeding stages indicates that trophozoite detachment from host tissue is an active process self-regulated by the parasite. A detailed discussion is provided on the possibility of reversible retraction and protraction of the eugregarine apical end, facilitating eventual reattachment to another host cell in better physiological conditions. The gamonts, found in contact with host tissue via a modified protomerite top, indicate further adaptation of parasite for nutrient acquisition via epicellular parasitism while keeping their host healthy. The presence of eugregarines in mealworm larvae even seems to increase the host growth rate and to reduce the death rate despite often heavy parasitisation. CONCLUSIONS/SIGNIFICANCE: Improved knowledge about the formation of host-parasite interactions in deep-branching apicomplexans, including gregarines, would offer significant insights into the fascinating biology and evolutionary strategy of Apicomplexa. Gregarines exhibit an enormous diversity in cell architecture and dimensions, depending on their parasitic strategy and the surrounding environment. They seem to be a perfect example of a coevolution between a group of parasites and their hosts.

• MeSH
• Actins metabolism   MeSH
• Apicomplexa cytology   physiology   ultrastructure   MeSH
• Epithelium metabolism   parasitology   ultrastructure   MeSH
• Epithelial Cells metabolism   parasitology   ultrastructure   MeSH
• Adaptation, Physiological * MeSH
• Host-Pathogen Interactions MeSH
• Myosins metabolism   MeSH
• Symbiosis * MeSH
• Tenebrio parasitology   MeSH
• Protein Transport MeSH
• Protein Binding MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Actins MeSH
• Myosins MeSH