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Phylogeny of Gregarines (Apicomplexa) As Inferred from Small-Subunit Rdna and B-Tubulin

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Phylogeny of Gregarines (Apicomplexa) As Inferred from Small-Subunit Rdna and B-Tubulin International Journal of Systematic and Evolutionary Microbiology (2003), 53, 345–354 DOI 10.1099/ijs.0.02284-0 Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and b-tubulin Brian S. Leander,1 Richard E. Clopton2 and Patrick J. Keeling1 Correspondence 1Canadian Institute for Advanced Research, Program in Evolutionary Biology, Department of Patrick Keeling Botany, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 [email protected] 2Division of Science and Technology, Peru State College, Peru, NE 68421, USA Gregarines are thought to be deep-branching apicomplexans. Accordingly, a robust inference of gregarine phylogeny is crucial to any interpretation of apicomplexan evolution, but molecular sequences from gregarines are restricted to a small number of small-subunit (SSU) rDNA sequences from derived taxa. This work examines the usefulness of SSU rDNA and b-tubulin sequences for inferring gregarine phylogeny. SSU rRNA genes from Lecudina (Mingazzini) sp., Monocystis agilis Stein, Leidyana migrator Clopton and Gregarina polymorpha Dufour, as well as the b-tubulin gene from Leidyana migrator, were sequenced. The results of phylogenetic analyses of alveolate taxa using both genes were consistent with an early origin of gregarines and the putative ‘sister’ relationship between gregarines and Cryptosporidium, but neither phylogeny was strongly supported. In addition, two SSU rDNA sequences from unidentified marine eukaryotes were found to branch among the gregarines: one was a sequence derived from the haemolymph parasite of the giant clam, Tridacna crocea, and the other was a sequence misattributed to the foraminiferan Ammonium beccarii. In all of our analyses, the SSU rDNA sequence from Colpodella sp. clustered weakly with the apicomplexans, which is consistent with ultrastructural data. Altogether, the exact position of gregarines with respect to Cryptosporidium and other apicomplexans remains to be confirmed, but the congruence of SSU rDNA and b-tubulin trees with one another and with morphological data does suggest that further sampling of molecular data will eventually put gregarine diversity into a phylogenetic context. INTRODUCTION Basing our understanding of apicomplexan biology and evolution solely on information from a few, potentially Apicomplexans are a diverse group of unicellular eukaryotes unrepresentative taxa may prove misleading. that parasitize the body cavities and tissues of meta- zoans. Some apicomplexans such as haemosporidians (e.g. Gregarines are a group of apicomplexans that are distinct Plasmodium, the causative agent of malaria), coccidians (e.g. from coccidians, haemosporidians and piroplasms and are Toxoplasma and Eimeria) and piroplasms (e.g. Babesia)are thought to be the earliest lineage of apicomplexans. They are pathogens of humans and domesticated vertebrates, making often found in marine worms and insects, where they are these parasites economically important and focal organisms extremely abundant and diverse. Although gregarines for medical research. There are approximately 4600 currently do not have a recognized impact on human described species of apicomplexans (Ellis et al., 1998), and welfare, some species could potentially serve as disease probably more than 10 times that number yet to be agents for the biological control of insects (Levine, 1985), discovered, but more is known about a handful of the and it has been suggested that gregarines are closely related medically important genera than about the rest combined. to the vertebrate pathogen Cryptosporidium (see Carreno et al., 1999). Gregarines are certainly significant from an Published online ahead of print on 26 July 2002 as DOI 10.1099/ evolutionary perspective because of their suspected early ijs.0.02284-0. diverging position within the Apicomplexa and their Abbreviations: ML, maximum likelihood for DNA; PML, protein maximum possession of several characteristics presumed to be plesio- likelihood; SSU, small subunit. morphic, such as an extracellular trophozoite stage, a mono- The GenBank accession numbers for the small-subunit rDNA xenous life-cycle and a prevailing presence in marine hosts sequences from Monocystis agilis, Lecudina sp., Gregarina polymorpha (Cox, 1994; The´odoride´s, 1984; Vivier & Desportes, 1990). and Leidyana migrator are respectively AF457127–AF457130. The GenBank accession number for the b-tubulin sequence from Leidyana Dinoflagellates and ciliates have been shown to share a migrator is AF457131. common ancestor with apicomplexans, collectively forming 02284 G 2003 IUMS Printed in Great Britain 345 B. S. Leander, R. E. Clopton and P. J. Keeling the Alveolata (Fast et al., 2001, 2002; Gajadhar et al., 1991; 1996; Siddall et al., 1997; Simpson & Patterson 1996; Wolters, 1991). Accordingly, apicomplexans possess tubular Whisler, 1990). Moreover, environmental PCR approaches mitochondrial cristae, micropores and a pellicle with three are identifying potentially intermediate lineages that membranous layers subtended by microtubules, character- still need to be characterized at the morphological level istics that define alveolates (Cavalier-Smith, 1993; Patterson, (Dı´ez et al., 2001; Lo´pez-Garcı´a et al., 2001; Moon-van der 1999). Flagella are absent in apicomplexans, except in the Staay et al., 2001). microgametes of some species. The phylum Apicomplexa is generally regarded as monophyletic, and a synapomorphy In terms of apicomplexans, the internal topology of the suggested for the group (from which the name is derived) is group is just beginning to emerge from comparisons of the presence of a microtubular apical complex, which morphological characteristics and gene sequences (Barta, consists of apical rings, a polar ring and a conoid (Barta et al., 1989; Ellis et al., 1992, 1995, 1998; Ellis & Morrison, 1995; 1991; Levine, 1970; Perkins, 1996; Vivier & Desportes, Escalante & Ayala, 1994; Hnida & Duszynski, 1999; 1990). The apical complex is functionally linked to secre- Holmdahl et al., 1999; Johnson et al., 1990; Morgan et al., tory organelles called rhopteries and micronemes, which 1999; Siddall, 1995; Siddall & Barta, 1992; Zhu et al., 2000); together play a role in the attachment to the host and in most however, most of this work has centred on representa- taxa, intracellular invasion (Black & Boothroyd, 2000). tives from three of the four major groups: coccidians, However, the presence or absence of an apical complex haemosporidians and piroplasms. Only two complete is rather ambiguous, since several predatory and parasitic small-subunit (SSU) rDNA sequences from gregarines have been reported (Carreno et al., 1999). We have alveolates (e.g. Colpodella and Acrocoelus) possess inter- sequenced four SSU rRNA genes and one b-tubulin gene mediate states for the apical complex and associated from four different gregarines, including two aseptate organelles, which makes their inclusion within the Api- eugregarines, in an attempt to examine the usefulness complexa sensu stricto controversial (Ferna´ndez et al., 1999; of SSU rDNA and b-tubulin for inferring the phylogeny of Foissner & Foissner, 1984; Siddall et al., 1997, 2001; Simpson these poorly understood parasites. Phylogenetic studies of & Patterson, 1996). For instance, the parasitic alveolate gregarines should help to provide the necessary framework Perkinsus possesses an apical-complex-like apparatus, but for beginning to reconstruct the nature of the last common molecular data show that Perkinsus is probably more closely ancestor of dinoflagellates and apicomplexans, and for related to modern dinoflagellates than to apicomplexans understanding the origin and early evolution of parasitism (Ellis et al., 1998; Goggin & Barker, 1993; Reece et al., 1997; in apicomplexans. Siddall et al., 1997). Another feature that unites the Apicomplexa (perhaps less ambiguously) is their specific parasitic life history. This life history is often complex and METHODS appears to vary considerably within the group (Levine, 1985; Siddall, 1995; Vivier & Desportes, 1990) but, in general, Organisms. All stages in the life cycle of the aseptate eugregarine consists of three alternating phases of development: Monocystis agilis Stein were found in the seminiferous vesicles of earthworms (Lumbricus terrestris) purchased from Berry’s Bait and merogony (asexual), gametogony (sexual) and sporogony Tackle (Fig. 1a, b); species identification was based on Meier (1956) (asexual). Gregarines display an interesting variety of these and Levine (1988). Forty to fifty gametocysts filled with ‘lemon- phases in the three subdivisions of the group: ‘neogrega- shaped’ oocysts (Fig. 1b) were micropipetted from the seminiferous rines’ possess all three phases and trophozoites contain vesicles, washed three times with distilled water and then collected ‘septa’ between cell regions; ‘archigregarines’ are thought in a 1?5 ml Eppendorf tube. Trophozoites of an unidentified species to possess all three phases (but merogony has not been of the aseptate eugregarine Lecudina Mingazzini (designated as Lecudina sp.) were identified in the gut of the marine polychaete indisputably observed) and here, trophozoites lack septa Nereis vexillosa, collected at low tide in Stanley Park, Vancouver, and are morphologically similar to the sporozoite stage; BC, Canada (Fig. 1c); genus identifications were based on Levine ‘eugregarines’ can be either septate or aseptate but are (1976, 1988) and Kozloff (1983). Approximately 40 trophozoites grouped together (perhaps artificially) based
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