Epicellular Apicomplexans: Parasites “On the Way In”

The Coccidia and the Cryptosporidia infect both coldand warm-blooded vertebrates, yet members of the genera Toxoplasma, Eimeria, Sarcocystis, and Cryptosporidium (which mostly parasitize the latter hosts) have received most of the attention by far because of their importance to human and veterinary health. Our knowledge about a wide array of apicomplexans found in fish, amphibians, and reptiles is thus primarily confined to the morphological description of their exogenous stages (i.e., oocysts) and sites of infection, rarely with notes on pathogenicity. The life cycles of these “neglected” parasites resemble those of apicomplexans from birds and mammals. They undergo successive multiplication by merogony (asexual divisions producing meronts with merozoites), followed by gamogony (fusion of two types of gametes resulting in an oocyst), and sporogony (asexual reproduction producing sporozoites) [1]. In the Coccidia of homeotherms, these developmental phases take place in different hosts, whereas the majority of the Coccidia of poikilotherms typically have direct life cycles. The intestine is the favored site for sporogony, but piscine coccidians are characterized by their frequent extraintestinal development with either exogenous (outside the host) or endogenous (inside the host) sporulation [1]. Coccidians of poikilotherm hosts differ from those parasitizing homeotherms by (1) thin-walled oocysts lacking micropyle (an opening of oocyst wall), (2) macrogamonts without wall-forming bodies, (3) sporocysts with excystation structures (sutures) and projections of the sporocyst wall (membranaceous veils, sporopodia), and (4) frequent epicellular localization, which is shared with some gregarines, the protococcidian Eleuteroschizon dubosqi, and cryptosporidians [1–4]. Phylogenetic analyses based on the 18S rRNA gene sequences, now available from a number of apicomplexans parasitizing cold-blooded vertebrates (e.g., members of the genera Cryptosporidium, Goussia, Acroeimeria, Eimeria, Calyptospora, and Choleoeimeria), allowed for the inference of their phylogenetic relationships. Piscine cryptosporidians represent a well-defined monophyletic group at the base of the cryptosporidian clade, whereas amphibian and reptile cryptosporidians are mixed with those infecting homeotherms. Coccidians of poikilotherm hosts constitute basal lineages of the whole eucoccidian clade, or of its eimeriid or sarcocystid subclades, with piscine coccidians representing the most basal groups (Fig 1) [2,3,5–7]. Because of their early-branching position, these parasites of poikilotherms likely possess ancestral features, the scrutiny of which may help us better understand the evolution of Apicomplexa. Indeed, the simple excystation structures of piscine, amphibian, and reptile coccidians have diverged into more complex excystation structures in eimeriids, sarcocystids, and calyptosporiids [2,3]. The