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UNCORRECTED PROOF 105 Sporangium Undergoing Early Stages of Differentiation Within the Cyst Wall (Arrows)

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UNCORRECTED PROOF 105 Sporangium Undergoing Early Stages of Differentiation Within the Cyst Wall (Arrows) XML:ver:5:0:1 EJOP : 25086 Prod:Type:FTP ED:JyothiG 5 jena pp:1216ðcol:fig::NILÞ PAGN:Bhaskara SCAN: ARTICLE IN PRESS 1 European Journal of PROTISTOLOGY 3 European Journal of Protistology ] (]]]]) ]]]–]]] www.elsevier.de/ejop 5 7 9 Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagel- lates: Parvilucifera prorocentri sp. nov. (Alveolata, Myzozoa) 11 Brian S. LeanderÃ, Mona Hoppenrath 13 Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, Departments of Botany and Zoology, 15 University of British Columbia, Vancouver, BC, Canada V6T 1Z4 17 Received 18 April 2007; received in revised form 16 August 2007; accepted 21 August 2007 19 21 Abstract 23 We have characterized the intracellular development and ultrastructure of a novel parasite that infected the marine benthic dinoflagellate Prorocentrum fukuyoi. The parasite possessed a combination of features described for perkinsids 25 and syndineans, and also possessed novel characters associated with its parasitic life cycle. Reniform zoospores, about 4 mm long, possessed a transverse flagellum, alveoli, a refractile body, a mitochondrion with tubular cristae, a 27 syndinean-like nucleus with condensed chromatin, micronemes, bipartite trichocysts with square profiles (absent in perkinsids) and oblong microbodies. Like Parvilucifera, the zoospores also possessed a shorter posterior flagellum, a 29 heteromorphic pair of central microtubules in the anterior axoneme and a reduced pseudoconoid positioned directly above an orthogonal pair of basal bodies. Early developmental stages consisted of a sporangium about 5–15 mmin 31 diam that contained spherical bodies and amorphous spaces. The undifferentiated sporangium increased to about 20–25 mm in diam before being enveloped by a wall with a convoluted mid-layer. The sporangium differentiated into an 33 unordered mass of zoospores that escaped from the cyst through a pronounced germ tube about 4–5 mm in diam and 10–15 mm long. Weakly developed germ tubes have been described in Perkinsus but are absent altogether in 35 Parvilucifera and syndineans. Comparison of these data with other myzozoans led us to classify the parasite as Parvilucifera prorocentri sp. nov., Myzozoa. Although we were hesitant to erect a new genus name in the absence of 37 molecular sequence data, our ultrastructural data strongly indicated that this parasite is most closely related to perkinsids and syndineans, and represents an intriguing candidate for the cellular identity of a major subclade of 39 Group I alveolates. r 2007 Published by Elsevier GmbH. 41 Keywords: Colpodella; Group I alveolates; Parvilucifera; Perkinsus; Syndinium; Ultrastructure 43 45 57 Introduction understanding of myzozoan lineages that do not fall 47 neatly within the Apicomplexa and the Dinoflagellata 59 The Myzozoa is a clade of alveolates consisting of the sensu stricto is critical for inferring the earliest stages of 49 most recent commonUNCORRECTED ancestor of apicomplexans and alveolate evolutionPROOF (Cavalier-Smith and Chao 2004; 61 dinoflagellates and all of its descendants. An improved Kuvardina et al. 2002; Leander and Keeling 2003; 51 Siddall et al. 2001). Several genera of predatory and 63 parasitic flagellates have been shown to diverge near the à 53 Corresponding author. Tel.: 1 604 822 2474; fax: 1 604 822 6089. phylogenetic origins of dinoflagellates and apicomplex- 65 E-mail address: [email protected] (B.S. Leander). 55 0932-4739/$ - see front matter r 2007 Published by Elsevier GmbH. 67 doi:10.1016/j.ejop.2007.08.004 Please cite this article as: Leander, B.S., Hoppenrath, M., Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata,.... Eur. J. Protistol. (2007), doi:10.1016/j.ejop.2007.08.004 EJOP : 25086 ARTICLE IN PRESS 2 B.S. Leander, M. Hoppenrath / European Journal of Protistology ] (]]]]) ]]]–]]] 1 an parasites, namely Alphamonas, Chilovora, Colpodella, and play important roles in the ecological dynamics of 57 Duboscquella, Parvilucifera, Perkinsus, Rastrimonas plankton communities (Park et al. 2004). 3 (formerly Cryptophagus) and Voromonas (Brugerolle We have discovered an intracellular parasite of the 59 2002, 2003; Cavalier-Smith and Chao 2004; Harada et marine benthic, sand-dwelling dinoflagellate Prorocen- 5 al. 2007; Kuvardina et al. 2002; Leander and Keeling trum fukuyoi Murray et al. (2007) that shares several 61 2004; Leander et al. 2003; Nore´ n et al. 1999; Saldarriaga features described for perkinsids and syndineans, but 7 et al. 2003; Siddall et al. 1997). These organisms share also possesses novel characters associated with its 63 several homologous characteristics associated with parasitic life cycle. Our objective in this paper is to 9 myzocytotic modes of feeding (or intracellular infection) characterize the intracellular development and ultra- 65 that are inferred to be synapomorphic for the Myzozoa, structure of this parasite using light and electron 11 such as an apical complex consisting of micronemes, microscopy. Comparison of these data with other 67 rhoptry-like extrusomes and a pseudoconoid (syn. described myzozoan predators and parasites (e.g. 13 ‘‘open’’ conoid). The apical complex was retained and colpodellids, perkinsids and syndineans) led us to 69 further modified along the apicomplexan lineage (e.g. propose a new species name for this novel lineage, 15 the evolution of a ‘‘closed’’ conoid) and appears to have conservatively within the genus Parvilucifera. 71 been secondarily lost along the dinoflagellate lineage. 17 However, components of the apical complex are present 73 in several parasitic sister groups to the ‘‘core’’ dino- Materials and methods 19 flagellates, such as perkinsids. 75 Marine environmental sequencing surveys using small Collection of organisms 21 subunit (SSU) rDNA have demonstrated two large and 77 diverse groups of alveolates that show close phyloge- Sand samples containing Prorocentrum fukuyoi Mur- 23 netic affinity to perkinsids and ‘‘core’’ dinoflagellates, 79 ray et al., 2007 were collected with a spoon during low namely Group I alveolates and Group II alveolates tide at Centennial Beach, Boundary Bay, BC, Canada 25 (Diez et al. 2001; Dolven et al. 2007; Groisillier et al. 81 during the summer and fall months of 2004–2006 (see 2006; Lo´ pez-Garcı´ a et al. 2001; Moon-van der Staay et also Hoppenrath and Leander 2006). The sample used 27 al. 2001; Moreira and Lo´ pez-Garcı´ a 2002; Takishita et 83 for this investigation was taken on September 5, 2005. al. 2007; Worden 2006). Group I alveolates have been The sand samples were transported directly to the 29 shown to include parasites of tintinnid ciliates like 85 laboratory, and the flagellates were separated from the Duboscquella (Harada et al. 2007), and there is sand by extraction through a fine filter (mesh size 45 mm) 31 molecular phylogenetic evidence that at least some of 87 using melting seawater-ice (Uhlig 1964). The flagellates these alveolates are parasites of ‘‘radiolarians’’ (Dolven accumulated in a Petri dish beneath the filter and were 33 et al. 2007). Group II alveolates have been identified as 89 identified at 40  to 250  magnification. The original syndineans, a group consisting of several different extraction was kept as raw culture, supplemented with 35 genera of marine parasites, such as Amoebophrya, 91 filtered seawater and stored in the laboratory at about Hematodinium and Syndinium (Coats 1999; Moon-van 17 1C under normal daylight conditions. The ‘‘culture’’ 37 der Staay et al. 2001; Moreira and Lo´ pez-Garcı´ a 2002; 93 was examined periodically, and intracellular parasitic Saldarriaga et al. 2004; Skovgaard et al. 2005). As in infections of the P. fukuyoi were apparent following 3–4 39 perkinsids, the life cycle of syndineans consists of 95 weeks of incubation. zoospores (syn. zooids) that penetrate a host (e.g. 41 copepods, polycystines and dinoflagellates) and develop 97 into an undifferentiated sporangium (syn. plasmodium) Light microscopy 43 (Azevedo 1989; Azevedo et al. 1990; Blackbourn et al. 99 1998; Dungan and Reece 2006; Fritz and Nass 1992; Infected cells were observed directly with a Leica 45 Manier et al. 1971; Perkins 1976). The growing DMIL inverted microscope and observations with 101 sporangium eventually destroys the internal compart- differential interference contrast (DIC) were made using 47 ment of the host and differentiates into many minute a Zeiss Axioplan 2 imaging microscope. Digital images 103 zoospores (ranging from about 3 to 20 mm in length, were recorded in colour. 49 depending onUNCORRECTED the species) that escape the host in order PROOF 105 to infect a new one. Whether or not a sexual phase Scanning electron microscopy 51 involving anisogametes takes place during the zoospore 107 stage between host infections is poorly understood An extraction sample containing mainly infected cells 53 (Cachon and Cachon 1987; Coats 1999). Collectively, was fixed with two drops of acidic Lugol’s solution over 109 these parasites are widely distributed in marine environ- night. The fixed cells were placed on a 5-mm poly- 55 ments, infect a broad range of hosts (e.g. dinoflagellates) carbonate membrane filter (Corning Separations Div., 111 Acton, MA) and dehydrated with a series of increasing Please cite this article as: Leander, B.S., Hoppenrath, M., Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata,.... Eur. J. Protistol. (2007),
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