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Species of the Parasitic Genus Duboscquella Are Members of the Enigmatic Marine Alveolate Group I

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Species of the Parasitic Genus Duboscquella Are Members of the Enigmatic Marine Alveolate Group I See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/6275809 Species of the Parasitic Genus Duboscquella are Members of the Enigmatic Marine Alveolate Group I Article in Protist · August 2007 DOI: 10.1016/j.protis.2007.03.005 · Source: PubMed CITATIONS READS 92 205 3 authors, including: Susumu Ohtsuka Hiroshima University 251 PUBLICATIONS 2,949 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Tropical foodwebs analysis View project Zooplankton Diversity View project All content following this page was uploaded by Susumu Ohtsuka on 29 December 2017. The user has requested enhancement of the downloaded file. ARTICLE IN PRESS Protist, Vol. 158, 337—347, July 2007 http://www.elsevier.de/protis Published online date 13 June 2007 ORIGINAL PAPER Species of the Parasitic Genus Duboscquella are Members of the Enigmatic Marine Alveolate Group I Ai Haradaa, Susumu Ohtsukab, and Takeo Horiguchic,1 aDivision of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo 060-0810, Japan bTakehara Marine Science Station, Setouchi Field Science Center, Graduate School of Biosphere Science, Hiroshima University, 5-8-1 Minato-machi, Takehara, Hiroshima 725-0024, Japan cDepartment of Natural History Sciences, Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan Submitted December 12, 2006; Accepted March 11, 2007 Monitoring Editor: Marina Montresor Small subunit ribosomal RNA gene sequences of Duboscquella spp. infecting the tintinnid ciliate, Favella ehrenbergii, were determined. Two parasites were sampled from different localities. They are morphologically similar to each other and both resemble D. aspida. Nevertheless, two distinct sequences (7.6% divergence) were obtained from them. Phylogenetic trees inferred from maximum likelihood and maximum parsimony revealed that these two Duboscquella spp. sequences are enclosed in an environmental clade named Marine Alveolate Group I. This clade consists of a large number of picoplanktonic organisms known only from environmental samples from various parts of the ocean worldwide, and which therefore lack clear characterization and identification. Here, we provide morphological and genetic characterization of these two Duboscquella genotypes included in this enigmatic clade. Duboscquella spp. produce a large number of small flagellated spores as dispersal agents and the presence of such small cells partially explains why the organisms related to these parasites have been detected within environmental genetic libraries, built from picoplanktonic size fractions of environmental samples. The huge diversity of the Marine Alveolate Group I and the finding that parasites from different marine protists belong to this lineage suggest that parasitism is a widespread and ecologically relevant phenomenon in the marine environment. & 2007 Elsevier GmbH. All rights reserved. Key words: alveolate; Duboscquella; environmental clone; Favella ehrenbergii; Marine Alveolate Group I; parasitic dinoflagellate. Introduction Analyses of small subunit ribosomal RNA gene unexpected diversity of picoplanktonic (o5 mm) (SSU rDNA) sequences from environmental sam- organisms in marine waters (Die´ z et al. 2001; ples (‘environmental clones’) have revealed an Lo´ pez-Garcia et al. 2001; Moon-van der Staay et al. 2001). Although environmental clones 1 Corresponding author; recovered from marine environments include fax +81 11 706 4851 many different taxonomic groups, including prasi- e-mail [email protected] (T. Horiguchi). nophytes, haptophytes, and acanthareans, two & 2007 Elsevier GmbH. All rights reserved. doi:10.1016/j.protis.2007.03.005 ARTICLE IN PRESS 338 A. Harada et al. groups, i.e. stramenopiles and alveolates are phology (Chatton 1952). Cachon (1964) described particularly dominant within genetic libraries five new species that were distinguished from (Lo´ pez-Garcia et al. 2001; Moon-van der Staay each other by virtue of their trophont morphology. et al. 2001). Such alveolates were further dis- Hosts of these new species include non-tintinnid covered to comprise, in addition to the sequences ciliates and dinoflagellates. Coats (1988) exam- belonging to ordinary dinoflagellate or ciliate ined the cytology and life history of a parasite in lineages, two distinct lineages with unknown the tintinnid ciliate, Entintinnus pectinis, and representatives, named the Marine Alveolate described it as D. cachoni Coats, differing from Group I and the Marine Alveolate Group II, other members of the genus by the structure of its respectively (Lo´ pez-Garcia et al. 2001). The latter trophont, the pattern of sporogenesis, and spore two groups are ubiquitous, being discovered morphology. virtually anywhere from tropic to Antarctic regions In most cases, species of Duboscquella are (Lo´ pez-Garcia et al. 2001; Moon-van der Staay lethal to their hosts, even having a significant et al. 2001), from coastal and oceanic waters, impact on entire populations. This is the case for sediments and hydrothermal vents to permanent Duboscquella cachoni and the ciliate Eutintinnus anoxic deep waters (Groisillier et al. 2006; Jeon pectinis in Chesapeake Bay, USA (Coats and et al. 2006; Stoeck et al. 2006). However, so far, Heisler 1989). The genus Duboscquella has a our knowledge of the kind of organisms, which characteristic pattern of sporogenesis: there are actually represent these lineages is incomplete. successive nuclear and cytoplasmic divisions Recently, some parasitic dinoflagellates belonging without interruption, termed ‘‘palintomy’’, through to the subdivision Syndinea of the division Dino- which a large number of biflagellate spores are flagellata (Fensome et al. 1993), such as Syndi- produced. Two types of motile spores have been nium, Hematodinium, and Amoebophrya, were reported, i.e. the macrospore and the microspore. found to belong to the Marine Alveolate Group II Both types of spore may be formed by the same (Groisillier et al. 2006; Skovgaard et al. 2005). The species, but only one type is released from a given Marine Alveolate Group I still remains ‘enigmatic’ host (Coats 1988). Ciliates play an important role (Groisilier et al. 2006; Stoeck et al. 2006) with no as predators of microorganisms in the marine food clear identifications having been made since the webs (e.g. Johannson et al. 2004), and therefore recognition of this group (Lo´ pez-Garcia et al. more attention should be paid to the ecology of 2001). Recently, Dolven et al. (2007) reported that their parasites. sequences of some of the ‘associates’ (probably The SSU rDNA of several samples of Dubosc- parasites) of four species of polycystine radiolar- quella spp. was sequenced and the resultant ians and one phaeodarian species are included in phylogenetic analysis revealed that the genus the clade of Marine Alveolate Group I, although no belongs to the Marine Alveolate Group I clade. morphological information of these species was This is the first time that this organism has been provided. linked with the ubiquitous, but enigmatic oceanic During the course of taxonomic studies on lineage. parasitic dinoflagellates along the Japanese coasts, members of the genus Duboscquella were often encountered. This genus is known to be Results parasitic mainly infecting tintinnid ciliates, although other types of hosts are known. The ciliates, Trophont Morphology and Sporogenesis Favella ehrenbergii (Clapare´ de et Lachmann) Jo¨ rgensen, Tintinnopsis campanula (Ehrenberg) Infected tintinnids were collected mainly in sum- Dady, and Codonella galea Haeckel, were mer. Individuals of Favella ehrenbergii in the late reported to be infected by Duboscquella tintinicola stage of infection by Duboscquella sp. were easily (Chatton 1920). However, it later became clear detected because the parasite can be seen that the flagellated dispersal stage from these through the transparent host lorica (Figs 1, 2). different hosts can be distinguished morphologi- Despite infection, most of the hosts in the cally and that their corresponding trophonts collected samples were alive and actively swim- (feeding stage) also have specific characters, ming. Sporogenesis (formation of spores) meaning that each ciliate species can be infected occurred outside the host cell, but within the host by a different species. A second species, lorica. Sometimes Duboscquella sporocytes (cells D. anisospora, is characterized by its unequal that give rise to spores) were found beyond the flagellated spore size and unique trophont mor- confines of the host lorica, spread by the activity ARTICLE IN PRESS Duboscquella Phylogeny 339 Figure 1. Duboscquella sp. 1 and sp. 2 infecting tintinnid ciliate, Favella ehrenbergii. The micrographs illustrate the cells used for single cell PCR. A. Duboscquella sp. 1 from Ishikari Harbor, Hokkaido, Japan. The host cell (H) and many spherical parasitic sporocysts (P) can be seen within the lorica (L). B. Duboscquella sp. 2 from Hamana Lake, Shizuoka, Japan. Both host (H) and parasites (P) can be seen within the lorica (L). C. Duboscquella sp. 2 from Kurosaki Harbor, Okayama, Japan. of the cilia or by the movement of the tintinnid. Figure 3B shows a section of a small spherical Even here, the parasite continued to exhibit sporocyte, roughly corresponding to the stage E normal cell division. In the sporogenesis stage, a of Figure 2. The cell possesses a nucleus long, rosary-like chain of transparent sporocytes with dense chromosome-like structures, but were formed
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