Fig 1.
This schematic phylogenetic tree shows the relationships among major groups of Apicomplexa and the evolution of host–parasite interactions.
Phylogenetic analysis is based on the alignment of 18S rRNA gene sequences from 140 apicomplexan taxa, which were aligned in Multiple Alignment using Fast Fourier Transform (MAFFT) and analyzed using maximum likelihood criterion in RAxML, both implemented in Geneious version 8.1.3. Coccidians are monophyletic, with epicellular (EPCL) species positioned at the base of the eimeriid group and the cryptosporidia cluster within gregarines. The parasitic lifestyle likely evolved from the free-living chromerids via the myzocytic feeding of colpodellids and archigregarines. The feeding strategies of Platyproteum and Filipodium (“archigregarine” clade III) are unknown (labelled with question mark), but most likely include a kind of surface-mediated acquisition of nutrients. Neogregarines and eugregarines developed a more permanent transmembrane feeding, whereas cryptosporidians exhibit EPCL mode of nutrition using the elaborate feeder organelle. EPCL coccidians uptake nutrients through the microvillous layer of host cells. Intracellular (INCL) Apicomplexa (most eimeriid and sarcocystid coccidians, piroplasms, and haemosporidians) use both transmembrane and micropore modes of nutrient uptake. Micropores are also used for endocytosis in rhytidocystids, which are embedded in the extracellular matrix of the host’s intestinal epithelium.
Fig 2.
Schematic interpretation of host–parasite interactions of epicellular piscine cryptosporidians and coccidians.
Monopodial stage of Cryptosporidium molnari with the detail of feeder organelle (inset) (A; modified from Alvarez-Pellitero P, Palenzuela O, Sitjà-Bobadilla A. 2002. Cryptosporidium molnari n. sp. (Apicomplexa: Cryptosporidiidae) infecting two marine fish species, Sparus aurata L. and Dicentrarchus labrax L. Figs 23 and 30. International Journal for Parasitology 32: 1007–1021. Elsevier 2002), Cryptosporidium villithecus (B; adapted from Landsberg and Paperna, 1986), Goussia janae (C; adapted from Lukeš J, Starý V. 1992. Ultrastructure of life cycle stages of Goussia janae (Apicomplexa, Eimeriidae) and X-ray microanalysis of accompanying precipitates. Canadian Journal of Zoology, 70 (12): 2382–2397, 2008 Canadian Science Publishing or its licensors. Reproduced with permission), Eimeria anguillae (D), Goussia spraguei (E; adapted from A new species of Goussia (Apicomplexa, Coccidia) in the kidney tubules of the cod, Gadus morhua L. Morrison CM, Poynton SL. Journal of Fish Diseases 12 (6). 1989. John Wiley & Sons, Inc. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2761.1989.tb00564.x/abstract), Eimeria puytoraci (F), Eimeria vanasi with the detail of its protrusions into the host cell cytoplasm (inset) (G; adapted from Paperna, (1991). Kim and Paperna (1992)); Spider-like stage of Goussia pannonica (H; adapted from Life cycle of Goussia pannonica (Molnár, 1989) (Apicomplexa, Eimeriorina), an extracytoplasmic coccidium from the white bream Blicca bjoerkna. Lukeš J. Journal of Protozoology 39 (4). 1992 John Wiley & Sons, Inc. http://onlinelibrary.wiley.com/doi/10.1111/j.1550-7408.1992.tb04836.x/abstract). In all figures, the scale bar is 1 μm, with the exception of insets (0.2 μm in A and 0.3 μm in G).
Fig 3.
Schematic interpretation of mechanisms of host invasion by the epicellular (EPCL) piscine cryptosporidians and coccidians.
(A) Invasion of host cell by Cryptosporidium spp. Zoite penetrates among the microvilli (A1), which eventually surround and enclose it within the parasitophorous sac (A2–A3). Finally, the feeder organelle is formed (A4). (B) The invasion mechanism resulting in the formation of monopodial stages of an EPCL coccidium. The beginning of invasion, until the enclosure of the parasite by the host cell membrane, is similar as in A (B1), but the feeder organelle does not form (B2) and the attachment remains monopodial (B3–B4). (C and D) Two possible mechanisms of formation of the spider-like EPCL stages. (C) The zoite settles down and fuses with the apical part of the microvillus (C1) and its growth progressively extends to the neighbouring microvilli (C2). Contact between the infected microvillar membrane and the membranes of other microvilli (C3) results in their fusions (C4), thus attaching the parasite to the host cell via additional region(s). (D) The zoite settles down at the microvillar zone laterally (D1), inducing fusion of non-neighbouring microvilli and its enclosure (D2–D3), thus forming a spider-like stage attached to the host cell (or more cells) in several regions (D4).