Marine gregarine genomes reveal the breadth of apicomplexan diversity with a partially conserved glideosome machinery.

Our current view of the evolutionary history, coding and adaptive capacities of Apicomplexa, protozoan parasites of a wide range of metazoan, is currently strongly biased toward species infecting humans, as data on early diverging apicomplexan lineages infecting invertebrates is extremely limited. Here, we characterized the genome of the marine eugregarine Porospora gigantea, intestinal parasite of Lobsters, remarkable for the macroscopic size of its vegetative feeding forms (trophozoites) and its gliding speed, the fastest so far recorded for Apicomplexa. Two highly syntenic genomes named A and B were assembled. Similar in size (~ 9 Mb) and coding capacity (~ 5300 genes), A and B genomes are 10.8% divergent at the nucleotide level, corresponding to 16-38 My in divergent time. Orthogroup analysis across 25 (proto)Apicomplexa species, including Gregarina niphandrodes, showed that A and B are highly divergent from all other known apicomplexan species, revealing an unexpected breadth of diversity. Phylogenetically these two species branch sisters to Cephaloidophoroidea, and thus expand the known crustacean gregarine superfamily. The genomes were mined for genes encoding proteins necessary for gliding, a key feature of apicomplexans parasites, currently studied through the molecular model called glideosome. Sequence analysis shows that actin-related proteins and regulatory factors are strongly conserved within apicomplexans. In contrast, the predicted protein sequences of core glideosome proteins and adhesion proteins are highly variable among apicomplexan lineages, especially in gregarines. These results confirm the importance of studying gregarines to widen our biological and evolutionary view of apicomplexan species diversity, and to deepen our understanding of the molecular bases of key functions such as gliding, well known to allow access to the intracellular parasitic lifestyle in Apicomplexa.

Integrative taxonomy confirms that Gregarina garnhami and G. acridiorum (Apicomplexa, Gregarinidae), parasites of Schistocerca gregaria and Locusta migratoria (Insecta, Orthoptera), are distinct species.

Orthoptera are infected by about 60 species of gregarines assigned to the genus Gregarina Dufour, 1828. Among these species, Gregarina garnhami Canning, 1956 from Schistocerca gregaria (Forsskål, 1775) was considered by Lipa et al. in 1996 to be synonymous with Gregarina acridiorum (Léger 1893), a parasite of several orthopteran species including Locusta migratoria (Linné, 1758). Here, a morphological study and molecular analyses of the SSU rDNA marker demonstrate that specimens of S. gregaria and specimens of L. migratoria are infected by two distinct Gregarina species, G. garnhami and G. acridiorum, respectively. Validation of the species confirms that molecular analyses provide useful taxonomical information. Phenotypic plasticity was clearly observed in the case of G. garnhami: the morphology of its trophozoites, gamonts and syzygies varied according to the geographical location of S. gregaria and the subspecies infected.

TITLE: La taxonomie intégrative confirme que Gregarina garnhami et G. acridiorum (Apicomplexa, Gregarinidae), parasites de Schistocerca gregaria et Locusta migratoria (Insecta, Orthoptera), sont des espèces distinctes. ABSTRACT: Les orthoptères sont parasités par environ soixante espèces de grégarines affiliées au genre Gregarina Dufour, 1828. Parmi ces espèces Gregarina garnhami Canning, 1956 décrite chez Schistocerca gregaria (Forskål, 1775), a été mise en synonymie par Lipa et al. en 1996 avec Gregarina acridiorum (Léger 1893), parasite de plusieurs espèces d'orthoptères dont Locusta migratoria (Linné, 1758). Ici, une étude morphologique et des analyses moléculaires du marqueur SSU rDNA démontrent que les spécimens de S. gregaria et ceux de L. migratoria sont infectés par 2 espèces distinctes de grégarines, Gregarina garnhami et Gregarina acridiorum, respectivement. La validation de ces espèces confirme l'importance des informations fournies par les analyses moléculaires dans les études taxonomiques. Une plasticité phénotypique a été clairement observée dans le cas de G. garnhami : la morphologie de ses trophozoïtes, gamontes et syzygies varie selon la localisation géographique et la sous-espèce de S. gregaria infectée.

Why the -omic future of Apicomplexa should include gregarines.

Gregarines, a polyphyletic group of apicomplexan parasites infecting mostly non-vertebrates hosts, remains poorly known at taxonomic, phylogenetic and genomic levels. However, it represents an essential group for understanding evolutionary history and adaptive capacities of apicomplexan parasites to the remarkable diversity of their hosts. Because they have a mostly extracellular lifestyle, gregarines have developed other cellular developmental forms and host-parasite interactions, compared with their much better studied apicomplexan cousins, intracellular parasites of vertebrates (Hemosporidia, Coccidia, Cryptosporidia). This review highlights the promises offered by the molecular exploration of gregarines, that have been until now left on the side of the road of the comparative -omic exploration of apicomplexan parasites. Elucidating molecular bases for both their ultrastructural, functional and behavioural similarities and differences, compared with those of the typical apicomplexan models, is expected to provide entirely novel clues on the adaptive capacities developed by Apicomplexa over evolution. A challenge remains to identify which gregarines should be explored in priority, as recent metadata from open and host-associated environments have confirmed how underestimated is our current view on true gregarine biodiversity. It is now time to turn to gregarines to widen the currently highly skewed view we have of adaptive mechanisms developed by Apicomplexa.