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Discovery of a Diverse Clade of Gregarine Apicomplexans (Apicomplexa: Eugregarinorida) from Pacific Eunicid and Onuphid Polychae

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Discovery of a Diverse Clade of Gregarine Apicomplexans (Apicomplexa: Eugregarinorida) from Pacific Eunicid and Onuphid Polychae The Journal of Published by the International Society of Eukaryotic Microbiology Protistologists Journal of Eukaryotic Microbiology ISSN 1066-5234 ORIGINAL ARTICLE Discovery of a Diverse Clade of Gregarine Apicomplexans (Apicomplexa: Eugregarinorida) from Pacific Eunicid and Onuphid Polychaetes, Including Descriptions of Paralecudina n. gen., Trichotokara japonica n. sp., and T. eunicae n. sp. Sonja Rueckerta,b, Kevin C. Wakemanc & Brian S. Leanderc a School of Life, Sport and Social Sciences, Edinburgh Napier University, Sighthill Campus, Sighthill Court, Edinburgh EH11 4BN, United Kingdom b Shimoda Marine Research Center, University of Tsukuba, 5-10-1, Shimoda, Shizuoka 415-0025, Japan c Department of Zoology, University of British Columbia, #3529–6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada Keywords ABSTRACT Eugregarines; parasite; phylogeny; taxonomy. Marine gregarines are poorly understood apicomplexan parasites with large trophozoites that inhabit the body cavities of marine invertebrates. Two novel Correspondence species of gregarines were discovered in polychaete hosts collected in Canada S. Rueckert, School of Life, Sport and Social and Japan. The trophozoites of Trichotokara japonica n. sp. were oval to Sciences, Edinburgh Napier University, rhomboidal shaped, and covered with longitudinal epicytic folds with a density Sighthill Campus, Sighthill Court, Edinburgh of six to eight folds/micron. The nucleus was situated in the middle of the cell, EH11 4BN, United Kingdom and the mucron was elongated and covered with hair-like projections; antler- Telephone number: +44 131 455 2490; like projections also extended from the anterior tip of the mucron. The distinc- FAX number: +44 131 455 2291; tively large trophozoites of Trichotokara eunicae n. sp. lacked an elongated e-mail: [email protected] mucron and had a tadpole-like cell shape consisting of a bulbous anterior region and a tapered tail-like posterior region. The cell surface was covered Received: 15 June 2012; revised 13 August with longitudinal epicytic folds with a density of three to five folds/micron. 2012; accepted September 25, 2012. Small subunit (SSU) rDNA sequences of both species were very divergent and formed a strongly supported clade with the recently described species Tricho- doi:10.1111/jeu.12015 tokara nothriae and an environmental sequence (AB275074). This phylogenetic context combined with the morphological features of T. eunicae n. sp. required us to amend the description for Trichotokara. The sister clade to the Trichoto- kara clade consisted of environmental sequences and Lecudina polymorpha, which also possesses densely packed epicyctic folds (3–5 folds/micron) and a prominently elongated mucron. This improved morphological and molecular phylogenetic context justified the establishment of Paralecudina (ex. Lecudina) polymorpha n. gen. et comb. GREGARINES are unicellular parasites of terrestrial, fresh- either septate or aseptate depending on whether or not water, and marine invertebrates that infect the digestive the cell is partitioned into two visible compartments (pro- tract, coelomic spaces, and reproductive vesicles of their tomerite and deutomerite). The anterior end of the troph- hosts. The vast majority of described gregarine species ozoites is modified for attachment to host tissues and is belong to so-called “eugregarines” (Grasse 1953; Leander considered an epimerite in septate species and a mucron 2008; Perkins et al. 2002), which possess an extracellular in aspetate species. Mucrons and epimerites can range feeding stage, the trophozoite, that are conspicuously dif- from being streamlined and inconspicuous to prominent ferent in morphology and motility from the infective sporo- and elongated, sometimes bearing multiple hair-like exten- zoite stage. Most eugregarines possess dense arrays of sions. longitudinal epicytic folds facilitating surface mediated The haploid life histories of eugregarines apparently lack nutrition (Leander 2008). Because of the large number of an asexual proliferation phase called “merogony”, folds, the cells are relatively stiff and move using an actin/ whereby the trophozoites are able to divide into many myosin-based gliding mechanism (Heintzelman 2004; genetically identical individuals (Levine 1977). In general, Leander 2008). The trophozoites of eugregarines are also eugregarines have (monoxenous) life cycles involving only © 2012 The Author(s) Journal of Eukaryotic Microbiology © 2012 International Society of Protistologists Journal of Eukaryotic Microbiology 2013, 60, 121–136 121 Diversity of Marine Gregarine Apicomplexans Rueckert et al. one host species. The relatively large trophozoites within the research vessel R/V Tsukuba based at the Shimoda a host pair up in a process called “syzygy” and become Marine Research Center, University of Tsukuba, Shimoda, gamonts. A cyst forms around the pair of gamonts, form- Shizuoka, Japan. Onuphid tubeworms Nothria cf. otsuchi- ing a gametocyst, and each gamont divides into numerous ensis (Imajima, 1986) were collected from these samples. gametes (Levine 1977). The pair-wise fusion of gametes The polychaete Eunice valens (Chamberlin, 1919) was col- derived from each gamont forms a zygote that is then sur- lected at a depth of 7–10 m while SCUBA diving at Ogden rounded by an oocyst wall. Within the oocyst, meiosis Point (48°24′48″N, 123°23′37″W), in August 2010, in Victo- occurs to yield four (or more, with subsequent rounds of ria, British Columbia, Canada. The intestines of the host ani- mitosis) spindle-shaped sporozoites (Kuriyama et al. 2005). mals were dissected with fine-tipped forceps under a low Hundreds of oocysts accumulate within each gametocyst, magnification stereomicroscope (Olympus SZ61, Olympus and are usually released via host faeces or via host death Corp. Tokyo, Japan/Leica MZ6, Wetzlar, Germany) to and remain in the environment until a new host ingests extract the trophozoites of Trichotokara japonica n. sp. and them. Once ingested, the sporozoites hatch from the Trichotokara eunicae n. sp. Gut contents containing tropho- oocysts and penetrate the host cells. The sporozoites zoites were examined using an inverted compound micro- enlarge to become trophozoites that emerge from the cell scope (Olympus CKX31, Olympus Corp./Zeiss Axiovert 200, and start feeding. Carl-Zeiss, Goettingen, Germany, or Leica DM IL, Wetzlar, Lecudina Mingazzini, 1899 (Levine, 1988) and the Lecu- Germany), and individual trophozoites were isolated by dinidae Kamm, 1922 (26 genera) are essentially “catch-all” micromanipulation. Before being prepared for microscopy taxa for marine eugregarines that infect mainly polychae- and DNA extraction, individual trophozoites were washed tes (Rueckert and Leander 2010). Emerging molecular three times in filtered and autoclaved seawater. phylogenetic data combined with ultrastructural data, how- ever, have improved our understanding of lecudinid inter- Light, scanning, and transmission electron microscopy relationships (Leander 2008; Leander et al. 2003b; Rueckert and Leander 2009, 2010; Simdyanov 2009). For instance, Differential interference contrast (DIC) light micrographs of Difficilina (Rueckert et al. 2010; Simdyanov 2009) and Tri- the trophozoites of T. japonica n. sp. were taken using a chotokara (Rueckert and Leander 2010) are recently estab- system microscope (Olympus BX50, Olympus Corp.) con- lished genera within the Lecudinidae that more accurately nected to a digital camera (Olympus DP70, Olympus characterize the diversity of marine eugregarines. The Corp.). The DIC light micrographs of the trophozoites of combination of molecular phylogenetic data, comparative T. eunicae n. sp. were taken with a compound microscope morphology, host affinity, and biogeography suggest that (Zeiss Axioplan 2, Carl-Zeiss) connected to a colour digital many more genera are warranted and that some known camera (Leica DC500). Individual trophozoites of T. japon- species of Lecudina need to be re-evaluated within the ica n. sp. (n = 55) and T. eunicae n. sp. (n = 60) were pre- context of available data (compare Levine 1977, 1979; Per- pared for scanning electron microscopy (SEM) using the kins et al. 2002; Landers and Leander 2005; Rueckert and OsO4 vapour protocol described previously (Rueckert and Leander 2008, 2009; Simdyanov 2009). The generation of Leander 2008, 2009). Isolated cells were deposited molecular phylogenetic data from characterized gregarine directly into the threaded hole of a Swinnex filter holder, species has also played a huge role in the interpretation of containing a 5 lm polycarbonate membrane filter environmental sequences generated from PCR surveys of (Millipore Corp., Billerica, MA), that was submerged in organismal diversity in specific habitats (e.g. Rueckert 10 ml of seawater within a small canister (2 cm diameter et al. 2011). and 3.5 cm tall). A piece of Whatman filter paper was In this vein, we discovered two novel species of marine mounted on the inside base of a beaker (4 cm diameter eugregarines in eunicid and onuphid polychaetes and char- and 5 cm tall) that was slightly larger than the canister. acterized their trophozoites with light microscopy (LM), The Whatman filter paper was saturated with 4% OsO4 scanning electron microscopy (SEM) and small subunit and the beaker was turned over the canister. The para- (SSU) rDNA sequences. Molecular phylogenetic analyses sites were fixed by OsO4 vapours for 30 min. Ten drops of the new sequences enabled us to (1) determine the of 4% OsO4 were added directly
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