A new view on the morphology and phylogeny of eugregarines suggested by the evidence from the gregarine Ancora sagittata (Leuckart, 1860) Labbé, 1899 (Apicomplexa: Eugregarinida).

Timur G Simdyanov,Joseph Schrével,Kirill V Mikhailov,Andrei Y Diakin,Laure Guillou,Vladimir V Aleoshin

doi:10.7717/peerj.3354

Abstract

BackgroundGregarines are a group of early branching Apicomplexa parasitizing invertebrate animals. Despite their wide distribution and relevance to the understanding the phylogenesis of apicomplexans, gregarines remain understudied: light microscopy data are insufficient for classification, and electron microscopy and molecular data are fragmentary and overlap only partially.MethodsScanning and transmission electron microscopy, PCR, DNA cloning and sequencing (Sanger and NGS), molecular phylogenetic analyses using ribosomal RNA genes (18S (SSU), 5.8S, and 28S (LSU) ribosomal DNAs (rDNAs)).Results and DiscussionWe present the results of an ultrastructural and molecular phylogenetic study on the marine gregarine Ancora sagittata from the polychaete Capitella capitata followed by evolutionary and taxonomic synthesis of the morphological and molecular phylogenetic evidence on eugregarines. The ultrastructure of Ancora sagittata generally corresponds to that of other eugregarines, but reveals some differences in epicytic folds (crests) and attachment apparatus to gregarines in the family Lecudinidae, where Ancora sagittata has been classified. Molecular phylogenetic trees based on SSU (18S) rDNA reveal several robust clades (superfamilies) of eugregarines, including Ancoroidea superfam. nov., which comprises two families (Ancoridae fam. nov. and Polyplicariidae) and branches separately from the Lecudinidae; thus, all representatives of Ancoroidea are here officially removed from the Lecudinidae. Analysis of sequence data also points to possible cryptic species within Ancora sagittata and the inclusion of numerous environmental sequences from anoxic habitats within the Ancoroidea. LSU (28S) rDNA phylogenies, unlike the analysis of SSU rDNA alone, recover a well-supported monophyly of the gregarines involved (eugregarines), although this conclusion is currently limited by sparse taxon sampling and the presence of fast-evolving sequences in some species. Comparative morphological analyses of gregarine teguments and attachment organelles lead us to revise their terminology. The terms “longitudinal folds” and “mucron” are restricted to archigregarines, whereas the terms “epicystic crests” and “epimerite” are proposed to describe the candidate synapomorphies of eugregarines, which, consequently, are considered as a monophyletic group. Abolishing the suborders Aseptata and Septata, incorporating neogregarines into the Eugregarinida, and treating the major molecular phylogenetic lineages of eugregarines as superfamilies appear as the best way of reconciling recent morphological and molecular evidence. Accordingly, the diagnosis of the order Eugregarinida Léger, 1900 is updated.

Highlights

The Apicomplexa is a group of unicellular eukaryotes within the Alveolata encompassing parasites of humans and animals
All were infected and the number of gregarine trophozoites per host varied from several individuals up to about a 100. The parasites from both locations had the same morphology, which fitted the description of Ancora sagittata: an elongated body that narrowed toward the posterior end and with a rounded anterior end, without a septum, and with two lateral projections giving the cell the appearance of an anchor (Perkins et al, 2000)
The molecular phylogenies based on the SSU ribosomal DNA (rDNA) alone firmly delimit several major lineages in eugregarines but not their suborders (Aseptata and Septata), a finding that is more consistent with Grasse’s taxonomical scheme (Grasse, 1953) than with the current taxonomy established by Levine and the followers (Levine, 1985, 1988; Perkins et al, 2000)

Summary

Introduction

The Apicomplexa is a group of unicellular eukaryotes within the Alveolata encompassing parasites of humans and animals. The large majority of gregarines are monoxenous (have a single invertebrate host) and parasitize in the gut of their hosts, where they are commonly found as epicellular feeding stages, the trophozoites, which are conspicuous due to their large size (usually from 200 to 600 mm) Because of their minor economic importance, gregarines are poorly studied despite their widespread distribution and relevance to the reconstruction of the evolutionary history of apicomplexans. Gregarines are a group of early branching Apicomplexa parasitizing invertebrate animals Despite their wide distribution and relevance to the understanding the phylogenesis of apicomplexans, gregarines remain understudied: light microscopy data are insufficient for classification, and electron microscopy and molecular data are fragmentary and overlap only partially.

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Conclusion