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Cellular Identity of a Novel Small Subunit Rdna Sequence Clade of Apicomplexans: Description of the Marine Parasite Rhytidocystis Polygordiae N

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Cellular Identity of a Novel Small Subunit Rdna Sequence Clade of Apicomplexans: Description of the Marine Parasite Rhytidocystis Polygordiae N J. Eukaryot. Microbiol., 53(4), 2006 pp. 280–291 r 2006 The Author(s) Journal compilation r 2006 by the International Society of Protistologists DOI: 10.1111/j.1550-7408.2006.00109.x Cellular Identity of a Novel Small Subunit rDNA Sequence Clade of Apicomplexans: Description of the Marine Parasite Rhytidocystis polygordiae n. sp. (Host: Polygordius sp., Polychaeta) BRIAN S. LEANDERa and PATRICIA A. RAMEYb aCanadian Institute for Advanced Research, Program in Evolutionary Biology, Departments of Botany and Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4, and bInstitute of Marine and Coastal Sciences, Rutgers University, New Jersey 08901, USA ABSTRACT. A new species of Rhytidocystis (Apicomplexa) is characterized from North American waters of the Atlantic Ocean using electron microscopy and phylogenetic analyses of small subunit (SSU) rDNA sequences. Rhytidocystis polygordiae n. sp. is a parasite of the polychaete Polygordius sp. and becomes the fourth described species within this genus. The trophozoites of R. polygordiae were relatively small oblong cells (L 5 35–55 mm; W 5 20–25 mm) and distinctive in possessing subterminal indentations at both ends of the cell. The surface of the trophozoites had six to eight longitudinal series of small transverse folds and several micropores arranged in short linear rows. The trophozoites of R. polygordiae were positioned beneath the brush border of the intestinal epithelium but appeared to reside between the epithelial cells within the extracellular matrix rather than within the cells. The trophozoites possessed a uniform distribution of paraglycogen granules, putative apicoplasts, mitochondria with tubular cristae, and a centrally positioned nucleus. The trophozoites were non-motile and lacked a mucron and an apical complex. Intracellular sporozoites of R. polygordiae had a conoid, a few rhoptries, micronemes, dense granules, and a posteriorly positioned nucleus. Phylogenies inferred from SSU rDNA sequences demon- strated a close relationship between R. polygordiae and the poorly known parasite reported from the hemolymph of the giant clam Tridacna crocea. The rhytidocystid clade diverged early in the apicomplexan radiation and showed a weak affinity to a clade consisting of cryptosporidian parasites, monocystids, and neogregarines. Key Words. Agamococcidia, Apicomplexa, apicoplast, archiannelids, Coccidia Cryptosporidium, gregarines, molecular phylogeny, Rhytidocystis, ultrastructure. PICOMPLEXAN diversity is just beginning to be explored we describe a new rhytidocystid species that parasitizes Poly- A with molecular phylogenetic approaches, especially for gordius, a meiofaunal polychaete from North American waters of groups that do not have a direct impact on human welfare. Most the western Atlantic Ocean (Ramey, Fiege, and Leander 2006). likely, tens of thousands of apicomplexan species remain undis- Our ultrastructural and molecular phylogenetic data help clarify covered, especially those that inhabit marine environments. An the cellular identity of Rhytidocystis, and a poorly understood improved understanding of these lineages should shed consider- parasite of the giant clam Tridacna crocea. Moreover, these data ably more light on the unity and diversity of apicomplexan par- uncover another clade of enigmatic parasites that diverges early in asites and the earliest stages in the evolution of parasitism in the the apicomplexan radiation. group (Leander and Keeling 2004; Leander et al. 2006). Perhaps the least understood members of the Apicomplexa are gregarines MATERIALS AND METHODS and several enigmatic coccidian-like lineages with uncertain phylogenetic position. The ‘‘Agamococcidiorida’’ is an enigmat- Collection of organisms. Trophozoites of Rhytidocystis poly- ic and ill-named group of apicomplexans first recognized by gordiae n. sp. were isolated from the intestinal epithelium of the Levine (1979) because these organisms have eucoccidian-like polychaete Polygordius sp. Ramey, 2006. Host worms were col- cyst characteristics (e.g. oocysts containing sporocysts, each con- lected during the spring and summer months of 2004/05 by SCU- taining two sporozoites) but seem to lack gamonts, merogony, and BA divers near Station 9 at the LEO-15 research site on Beach any evidence of sexual reproduction. Most ‘‘agamococcidians’’ Haven Ridge, NJ (391280 N, 741150 W) (Ramey et al. 2006; Von have relatively large trophozoites, a general feature of many Alt and Grassle 1992). marine gregarines. Unlike most gregarines, however, the tropho- Microscopy. Host dissections and micromanipulation of indi- zoites of ‘‘agamococcidians’’ are non-motile and reside within the vidual parasites were conducted with a Leica MZ6 stereomicro- extracellular spaces of host epithelial tissues. This unique combi- scope and a Zeiss Axiovert 200 inverted microscope. Differential nation of features is significant from an evolutionary perspective interference contrast (DIC) light micrographs were produced by because a better understanding of these parasites could provide securing parasites under a cover slip with vaseline and viewing important insights into the deep relationships among gregarines, them with a Zeiss Axioplan 2 imaging microscope connected to a cryptosporidian parasites, and eucoccidians. Leica DC500 color digital camera. Rhytidocystis and Gemmocystis are the only described ‘‘aga- Parasites were released into seawater by teasing apart the host mococcidian’’ genera (Levine 1979; Upton and Peters 1986). The with fine-tipped forceps. Fifteen individual parasites were latter contains a single species, Gemmocystis cylindrus, described removed from the macerated tissue by micromanipulation and from the gastrodermis of scleractinian corals (Upton and Peters washed twice in filtered seawater. As described previously 1986). Rhytidocystis comprises three species, all of which were (Leander, Harper, and Keeling 2003b), washed parasites were de- collected from polychaetes in European waters of the eastern At- posited directly into the threaded hole of a Swinnex filter holder, lantic Ocean (de Beauchamp 1913; Porchet-Hennere 1972). Here containing a 5-mm polycarbonate membrane filter (Coring Sepa- rations Division, Acton, MA) submerged in seawater within a Corresponding Author: B. Leander, Canadian Institute for Advanced small canister. Whatman filter paper, mounted on the inside of a Research, Program in Evolutionary Biology, Departments of Botany beaker, was used to fix the parasites with OsO4 vapors for 30 min. and Zoology, University of British Columbia, Vancouver, BC V6T 1Z4 Five drops of 4% (w/v) OsO4 were added directly to the seawater Canada—Telephone number: 604-822-2474; FAX number: 604-822- and the trophozoites were fixed for an additional 30 min. The 6089; e-mail: [email protected] trophozoites were dehydrated with a graded series of ethyl alcohol 280 LEANDER AND RAMEY—DESCRIPTION OF RHYTIDOCYSTIS POLYGORDIAE N. SP. 281 and critical point dried with CO2. Filters were mounted on stubs, mer and Von Haeseler 1996) and trees were constructed with sputter coated with gold, and viewed under a Hitachi S4700 weighted neighbor joining (WNJ) using Weighbor (Bruno, Socci, Scanning Electron Microscope. Some SEM images were illustrat- and Halpern 2000). Five-hundred bootstrap datasets were gener- ed on a black background using Adobe Photoshop 6.0 (Adobe ated with SEQBOOT (Felsenstein 1993). Respective distances Systems, San Jose, CA). were calculated with the shell script ‘‘puzzleboot’’ (M. Holder Transmission electron microscopy (TEM) was conducted on and A. Roger, www.tree-puzzle.de) using the a shape parameter parasites in situ. Fragments of host worms were collected in and Ti/Tv ratios estimated from the original dataset and analyzed Eppendorf tubes and fixed in a 2% (v/v) glutaraldehyde in sea- with Weighbor. water at 4 1C for 1 h. The fixed worms were washed twice in sea- We also examined the 56-taxon dataset with Bayesian analysis water for 15 min and post-fixed with 1% (w/v) OsO4/seawater using the program MrBayes 3.0 set to operate with GTR, a g dis- cocktail at 4 1C for 1 h. Worm fragments were dehydrated with a tribution, and four MCMC chains (default temperature 5 0.2) graded series of ethyl alcohol and acetone, infiltrated with ace- (Huelsenbeck and Ronquist 2001). A total of 2,000,000 genera- tone-resin mixtures, and flat embedded with pure Epon resin at tions were calculated with trees sampled every 100 generations 60 1C. Worm fragments were excised with a razor blade and glued and with a prior burn-in of 200,000 generations (2,000 sampled to Epon blocks. Ultrathin sections were generated using a Leica trees were discarded). A majority rule consensus tree was con- Ultracut T Ultramicrotome, post-stained with uranyl acetate and structed from 16,000 post-burn-in trees with PAUPÃ 4.0. Posterior lead citrate, and viewed under a Hitachi H7600 Transmission probabilities correspond to the frequency at which a given node is Electron Microscope. found in the post-burn-in trees. DNA isolation, PCR, cloning, and sequencing. Thirty-five GenBank accession numbers. Adelina bambarooniae trophozoites were manually isolated from dissected hosts, washed (AF494059), Amphidinium asymmetricum (AF274250), Babesia three times in filtered seawater, and deposited into 1.5 ml Eppen- bigemina (AY603402), Rhytidocystis polygordiae (DQ273988), dorf tubes. DNA was extracted with a standard CTAB extraction Blepharisma americanum (M97909), Colpoda inflata (M97908), protocol: pelleted parasites were suspended in 200
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