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Convergent evolution of cytoskeletal traits in the intestinal parasites (Myzozoa, Platyproteum) of peanut worms Currie-Olsen, Danja

Abstract

The Myzozoa is a monophyletic group of primarily single-celled eukaryotes that have adopted diverse modes of nutrition, such as vampire-like predation, photoautotrophy and parasitism. Most myzozoans fall into two major subgroups, dinoflagellates and apicomplexans, but several lineages fall outside of these groups, such as predatory colpodellids and parasitic squirmids. In this study, the 3-dimensional cytoskeletal organization of a squirmid lineage, namely Platyproteum vivax, was investigated with confocal laser scanning microscopy (CLSM). Platyproteum inhabits the intestines of Pacific peanut worms (Phascolosoma agassizii) and has traits that are similar to other distantly related lineages of intestinal parasites within the Myzozoa called ‘gregarine apicomplexans’ (i.e., Selenidium), such as conspicuous feeding stages, called "trophozoites", capable of dynamic undulations via a system of longitudinal microtubules. More detailed characterizations of these traits will refine inferences about convergent evolution in the intestinal parasites of marine invertebrates. For instance, SEM and CLSM micrographs of P. vivax revealed the presence of an inconspicuous flagellar apparatus and a uniform array of longitudinal microtubules organized in bundles (LMBs). Extreme flattening of the trophozoites and a consistent orientation of the anterior end provided a reliable way to distinguish the dorsal and ventral surfaces. CLSM data also revealed a novel system of microtubules oriented in the flattened dorsoventral plane. Most of these ‘dorsoventral microtubule bundles’ (DVMBs) had a punctate distribution in dorsoventral view and were evenly spaced along a curved line spanning the longitudinal axis of the trophozoites. This configuration of microtubules is novel amongst myzozoans and is inferred to function in maintaining the flattened shape and potentially facilitate dynamic undulations via microtubule sliding. Overall, this study revealed novel traits in the trophozoites of Platyproteum, such as a flagellar apparatus and a system of DVMBs, that are consistent with phylogenomic data showing that this lineage of intestinal parasites is only distantly related to Selenidium and other marine gregarine apicomplexans. Therefore, similarities in the trophozoites of Platyproteum and Selenidium, such as relatively large trophozoites capable of dynamic undulations and uniform arrays of superficial microtubules, reflect convergent evolution within the intestines of marine invertebrates.

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