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MOLECULAR PHYLOGENY of PACIFIC ARCHIGREGARINES 233 Spp.) (Gunderson and Small 1986; Hoshide and Todd 1996; Scanning Electron Microscopy

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MOLECULAR PHYLOGENY of PACIFIC ARCHIGREGARINES 233 Spp.) (Gunderson and Small 1986; Hoshide and Todd 1996; Scanning Electron Microscopy The Journal of Published by the International Society of Eukaryotic Microbiology Protistologists J. Eukaryot. Microbiol., 59(3), 2012 pp. 232–245 © 2012 The Author(s) Journal of Eukaryotic Microbiology © 2012 International Society of Protistologists DOI: 10.1111/j.1550-7408.2012.00616.x Molecular Phylogeny of Pacific Archigregarines (Apicomplexa), Including Descriptions of Veloxidium leptosynaptae n. gen., n. sp., from the Sea Cucumber Leptosynapta clarki (Echinodermata), and Two New Species of Selenidium KEVIN C. WAKEMANa and BRIAN S. LEANDERa Department of Zoology, Program in Integrated Microbial Biodiversity, Canadian Institute for Advanced Research, University of British Columbia, #3529 6270 University Boulevard, Vancouver, BC, Canada, V6T 1Z4 ABSTRACT. Although archigregarines are poorly understood intestinal parasites of marine invertebrates, they are critical for understanding the earliest stages in the evolution of the Apicomplexa. Previous studies suggest that archigregarines are a paraphy- letic stem group from which other lineages of gregarines, and possibly all other groups of apicomplexans, evolved. However, sub- stantiating this inference is difficult because molecular phylogenetic data from archigregarines, in particular, and other gregarines, in general, are severely limited. In an attempt to help fill gaps in our knowledge of archigregarine diversity and phylogeny, we set out to discover and characterize novel lineages of archigregarines with high-resolution light and scanning electron microscopy and analyses of small subunit (SSU) rDNA sequences derived from single-cell (SC) PCR techniques. Here, we describe two novel spe- cies of Selenidium, namely Selenidium idanthyrsae n. sp. and S. boccardiellae n. sp., and demonstrate the surface morphology and molecular phylogenetic position of the previously reported species S. cf. mesnili. We also describe a novel genus of archigregarine, Veloxidium leptosynaptae n. gen., n. sp., which branches with an environmental sequence and, together, forms the nearest sister lineage to a diverse clade of marine eugregarines (i.e. lecudinids and urosporids). This molecular phylogenetic result is consistent with the hypothesis that archigregarines are deeply paraphyletic within apicomplexans, and suggests that convergent evolution played an important role in shaping the diversity of eugregarine trophozoites. Key Words. Alveolata, marine gregarine, parasite, phylogeny. RCHIGREGARINES are single-celled, intestinal parasites eugregarines differ significantly from their infective sporozoite A of marine invertebrates and are inferred to have retained stages. The trophozoite surface of most eugregarines has hun- many characteristics found in the most recent common ances- dreds of densely packed epicytic folds that run along the lon- tor of all apicomplexans (Cavalier-Smith and Chao 2004; Cox gitudinal axis of the cell (Leander et al. 2003b; Rueckert and 1994; Grasse´1953; Leander 2008; Leander and Keeling 2003). Leander 2010; Rueckert et al. 2010). This stands in contrast For instance, the extracellular trophozoites of archigregarines to archigregarines that typically have many fewer longitudinal are similar in morphology and motility to their infective spo- folds (i.e. 0–50) (Leander 2007, 2008; Leander et al. 2003b; rozoite stage and to the sporozoites of other apicomplexans Rueckert and Leander 2009; Schre´vel 1971a,b). The trophozo- (Cox 1994; Dyson et al. 1993, 1994; Kuvardina and Simdya- ite surface of archigregarines is supported by microtubules, nov 2002; Leander 2006; Ray 1930; Schre´vel 1968). Moreover, each surrounded by a transparent sheath, which are organized the oocysts of archigregarines contain just four infective spor- in one or more layers beneath the trilayered inner membrane ozoites, and the life cycle of archigregarines is completed complex (Leander 2007; Mellor and Stebbings 1980; Schre´vel within a single host species (Grasse´1953; Schre´vel 1970; 1971b; Stebbings et al. 1974; Vivier and Schre´vel 1964). This The´odoride` s 1984). The nearest free-living sister lineages to subcellular organization of microtubules is not present in the the obligately parasitic Apicomplexa are photosynthetic trophozoites of eugregarines (Leander 2008). chromerids and predatory, biflagellated colpodellids that, like Of the approximate 65 species of archigregarines that have some archigregarine trophozoites, possess an apical complex been described, roughly 56 belong to the genus Selenidium and utilize a vampire-like mode of feeding called “myzocyto- (Leander 2007; Levine 1971; Rueckert and Leander 2009). sis” (Barta and Thompson 2006; Cavalier-Smith and Chao Levine (1971) proposed that several species of Selenidium 2004; Grasse´1953; Leander 2008; Leander and Keeling 2003; should be considered eugregarines rather than archigregarines, Schre´vel 1971a,b; Simdyanov and Kuvardina 2007). This if there is no report of merogony/schizogony (i.e. asexual insight along with molecular phylogenetic analyses of small reproduction of trophozoites) at any point during the life subunit (SSU) rDNA has led to the hypothesis that archigre- cycle. As a result, the genus Selenidioides was erected to garines branched early within the Apicomplexa, and represent accommodate the 11 members of Selenidium with reports of a paraphyletic stem group from which all other gregarines, merogony, and the remaining members of Selenidium were and possibly the Apicomplexa as a whole, evolved (Leander moved into the order Eugregarinorida (Levine 1971). As 2008; Rueckert and Leander 2009). pointed out previously, the presence or absence of merogony There are several differences that distinguish archigregarine in the life cycle of any gregarine is difficult to substantiate, trophozoites from those of so-called “marine eugregarines” which makes this feature a poor indicator of phylogenetic (e.g. lecudinids and urosporids). The trophozoites of archigre- relationships (Leander 2006, 2007; Rueckert and Leander garines are generally spindle shaped and are capable of nema- 2009). Therefore, this study will consider Selenidium the main tode-like bending and coiling motility (e.g. Selenidium spp.) genus of archigregarines, which is consistent with most other (Rueckert and Leander 2009; Schre´vel 1970). The trophozoites contemporary work on this subject (Gunderson and Small of marine eugregarines, by contrast, are generally rigid and 1986; Kuvardina and Simdyanov 2002; Leander 2006, 2007; exhibit gliding motility (Leander 2008; Leander et al. 2003b; Rueckert and Leander 2009; Schre´vel 1971a; Simdyanov and Rueckert et al. 2010). Moreover, trophozoites of marine Kuvardina 2007; The´odoride` s 1984). Although our knowledge of archigregarines is based primar- Corresponding Author: K.C. Wakeman, Department of Zoology, ily on studies of species within the genus Selenidium, archigre- University of British Columbia, #3529—6270 University Blvd., garines are much more diverse. Close relatives of Selenidium Vancouver, BC V6T 1Z4, Canada—Telephone number: show twisting and peristaltic movements (e.g. Platyproteum +1 604 822 4892; FAX number: +1 604 822 6089; e-mail: wakeman. vivax) and highly modified morphology, such as matted hair- [email protected] like projections on the trophozoite surface (e.g. Filipodium 232 WAKEMAN & LEANDER—MOLECULAR PHYLOGENY OF PACIFIC ARCHIGREGARINES 233 spp.) (Gunderson and Small 1986; Hoshide and Todd 1996; scanning electron microscopy. Very few trophozoites are pres- Leander 2006; Rueckert and Leander 2009). Ultrastructural ent in some hosts; for instance, only nine trophozoites of V. information has been reported on fewer than 20 species of leptosynaptae were recovered from L. clarki. For each species, archigregarines, mostly Selenidium spp., and molecular phylo- a 10-lm polycarbonate membrane filter was placed within a genetic data of SSU rDNA are available for a mere six species Swinnex filter holder (Millipore Corp., Billerica, MA, USA); (e.g. Selenidium terebellae, Selenidium pisinnus, Selenidium ori- the filter holder was then placed within a small beaker (4 cm entale, Selenidium serpulae, Filipodium phascolosomae, and diam. and 5 cm tall) that was filled with 2.5% (v/v) glutaralde- Platyproteum vivax); none of these DNA sequences has a well- hyde in seawater. The manually isolated trophozoites were supported phylogenetic position within the context of all placed directly into the Swinnex filter holder and fixed on ice major lineages of apicomplexans (Leander 2006, 2007; Lean- for 15 min. Ten drops of 1% (w/v) OsO4 were then added der et al. 2003b; Rueckert and Leander 2009; Rueckert et al. directly to the opening of the Swinnex filter holder, and the 2011). Improved understanding of archigregarine diversity, samples were post-fixed on ice for 30 min. A syringe was especially from a molecular phylogenetic perspective, is attached to the Swinnex filter holder, and distilled water was expected to lead to the discovery of novel gregarine lineages, slowly run over the samples. A graded series of ethanol (30%, and shed considerable light on the earliest stages in apicom- 50%, 75%, 85%, 95%, and 100%) was then used to dehydrate plexan evolution. the fixed cells using the syringe system. Following dehydration, Here, we characterize the surface morphology and molecu- the polycarbonate membrane filters containing the trophozoites lar phylogeny of three species of Selenidium isolated from were transferred from the Swinnex filter holders into an alumi- polychaete hosts, namely Selenidium idanthyrsae n. sp. and num basket submerged
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