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Lepelletier Et Al 2014 Dinomyces Arenysensis Gen.Pdf Protist, Vol. 165, 230–244, March 2014 http://www.elsevier.de/protis Published online date 1 March 2014 ORIGINAL PAPER Dinomyces arenysensis gen. et sp. nov. (Rhizophydiales, Dinomycetaceae fam. nov.), a Chytrid Infecting Marine Dinoflagellates a,b c,d e f,b Frédéric Lepelletier , Sergey A. Karpov , Elisabet Alacid , Sophie Le Panse , a,b e a,b a,b,1 Estelle Bigeard , Esther Garcés , Christian Jeanthon , and Laure Guillou a CNRS, UMR 7144, Place Georges Teissier, CS90074, 29688 Roscoff Cedex, France b Université Pierre et Marie Curie (Paris VI), Station Biologique de Roscoff, Place Georges Teissier, CS90074, 29688 Roscoff Cedex, France c Zoological Institute RAS, St. Petersburg, Russia d St. Petersburg State University, St. Petersburg, Russia e Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Pg. Marítim de la Barceloneta, 37-49, E08003 Barcelona, Spain f CNRS, FR 2424, Plate-forme Merimage, Station Biologique de Roscoff, Place Georges Teissier, CS90074, 29688 Roscoff Cedex, France Submitted January 14, 2014; Accepted February 21, 2014 Monitoring Editor: Michael Melkonian Environmental 18S rRNA gene surveys of microbial eukaryotes have recently revealed the diversity of major parasitic agents in pelagic freshwater systems, consisting primarily of chytrid fungi. To date, only a few studies have reported the presence of chydrids in the marine environment and a limited number of marine chytrids have been properly identified and characterized. Here, we report the isolation and cul- tivation of a marine chytrid from samples taken during a bloom of the toxic dinoflagellate Alexandrium minutum in the Arenys de Mar harbour (Mediterranean Sea, Spain). Cross-infections using cultures and natural phytoplankton communities revealed that this chytrid is only able to infect certain species of dinoflagellates, with a rather wide host range but with a relative preference for Alexandrium species. Phylogenetic analyses showed that it belongs to the order Rhizophydiales, but cannot be included in any of the existing families within this order. Several ultrastructural characters confirmed the placement of this taxon within the Rhizophydiales as well its novelty notably in terms of zoospore structure. This marine chytridial parasitoid is described as a new genus and species, Dinomyces arenysensis, within the Dinomycetaceae fam. nov. © 2014 Elsevier GmbH. All rights reserved. Key words: Fungi; chytrid; microbial parasitoids; dinoflagellates; Dinomyces arenysensis; Rhizophydiales. 1 Corresponding author; fax +33 2 98 29 23 24 e-mail [email protected] (L. Guillou). http://dx.doi.org/10.1016/j.protis.2014.02.004 1434-4610/© 2014 Elsevier GmbH. All rights reserved. Dinomyces arenysensis, a Chytrid Infecting Marine Dinoflagellates 231 Introduction a widespread toxic marine bloom-forming species (Anderson et al. 2012). Dinoflagellates of the genus Chytrids are true fungi that produce motile Alexandrium are known to produce toxins that zoospores with a single posteriorly directed fla- can be accumulated along the food chain and gellum. Barr (2001) originally placed them in cause paralytic shellfish poisoning (PSP) events the phylum Chytridiomycota. Asexual reproduction in the case of human ingestion of contaminated results in the formation of a sac-like structure, shellfish. It was recently demonstrated that A. min- the zoosporangium, in which zoospores are pro- utum populations could be efficiently controlled by duced. Chytrids may also produce sexual and highly virulent protozoan parasitoids (Chambouvet asexual resting spores that eventually germinate et al. 2008; Montagnes et al. 2008). Several into a sporangium after a period of dormancy. Most pathogens of A. minutum have recently been iden- chytrids produce a rhizoidal system for absorp- tified and described within the kingdom Alveolata tion of nutrients. Many chytrids have been reported (Chambouvet et al. 2008; Figueroa et al. 2008; as saprobes and/or parasites in a wide range of Lepelletier et al. 2014). This study demonstrates habitats, notably in freshwater and soil ecosystems that the diversity of their parasitoids also extends (Powell 1993; Shearer et al. 2007; Sime-Ngando to another eukaryotic lineage. 2012; Sparrow 1960), but only a few species have been found in marine environments (Gleason et al. 2011; Sparrow 1960). In freshwater, chytrid Results parasitoids of planktonic microalgae and chytrid- iomycoses play a crucial role in the regulation of Isolation and Culturing Methods sizes of populations of phytoplanktonic species Natural samples were collected weekly during a (Ibelings et al. 2004; Sime-Ngando 2012; Sparrow bloom of A. minutum in the Arenys de Mar har- 1960). In particular, they infect large and inedi- bour (Mediterranean Sea, Spain) in 2012. Maximal ble diatoms and green algae (Kagami et al. 2007; 6 -1 density of the toxic dinoflagellate (10 cells L ) Rasconi et al. 2012). Because chytrid zoospores was observed on February 15th. Cell density slowly are also grazed by predators, such parasitoids 5 decreased over the following weeks (8.9 x 10 cells are considered as key players in the transfer of -1 5 -1 L and 6.2 x 10 cells L on February 22nd and organic matter from such inedible phytoplanktonic March 14th, respectively). Chytrids (6 strains) were cells to higher trophic levels in the microbial food isolated during the first two weeks of the survey web (Kagami et al. 2007; Miki et al. 2011; Sime- period (February 15th and 22nd, Supplementary Ngando 2012). Environmental SSU rDNA surveys Material Table S1). Chytrids could easily be main- have revealed widespread occurrence and high tained in culture with their hosts at salinities ranging diversity of chytrids in lakes (Lefèvre et al. 2007, from 27 to 35. Strains RCC3404 and RCC3408 2008). Diverse and abundant environmental fun- were not able to form colonies on either of the agar gal sequences have been retrieved from particular media tested without their hosts (Koch’s K-1 and marine habitats, such as deep and anoxic marine F/2 supplemented with soil extract). ecosystems (Jebaraj et al. 2010; Le Calvez et al. 2009; Orsi et al. 2013). At the sea surface, where Host Specificity microalgae are abundant, their contribution is con- siderably lower (Massana and Pedrós-Alió 2008). Diatoms (5 strains), cryptophytes (3 strains), hap- Although literature on freshwater chytrids infecting tophytes (3 strains) and prasinophytes (2 strains) microalgae is extensive, very few chytrid species were resistant when cross infected with fungal infecting microalgae have been properly identified strains RCC3404 and RCC3408 (Table 1). Among in marine ecosystems (Gleason et al. 2011). To dinoflagellates, Akashiwo sanguinea, Amphidinium date, infections by chytrids have only been reported carterae, Coolia monotis, Gymnodinium spp., Kar- in marine diatoms (Elbrächter and Schnepf 1998; lodinium veneficum, Kryptoperidinium foliaceum, Hanic et al. 2009). The putative capacity of chytrids and Prorocentrum spp. were also resistant. Both to adapt to and/or compete with other parasites of fungal strains could infect most Alexandrium microalgae in marine environments has been pro- species. However, some host cells survived infec- posed (Richard et al. 2012). tions after 20 days in most of cases, except In this study, we report the isolation into cul- for few strains of A. minutum, A. ostenfeldii, A. ture and characterization of the first chytrid known tamarense and A. cf. catenella where host cells to infect marine dinoflagellates. This species was disappeared totally. Intra-specific variability in host isolated during a bloom of Alexandrium minutum, response was observed: of fifteen A. minutum 232 F. Lepelletier et al. Table 1. Cross-infections between the chytrid parasitoid Dinomyces arenysensis and selected hosts belonging to different microalgal lineages (for details see supplementary Table 1). Resistant= —, moderately resistant=-, sensitive=+++, moderately sensitive=+. ND= Not Done. Host Species Strain Ocean Dinomyces Dinomyces arenysensis sp. RCC3404 RCC3408 Dinophyceae Akashiwo sanguinea RCC3040 The Channel — ND Alexandrium andersonii ICMB222 Med Sea + + Alexandrium cf. catenella ACT2 Med Sea +++ ND (Group IV) Alexandrium cf. catenella ACT3 Med Sea + ND (Group IV) Alexandrium cf. catenella AC2C Med Sea — — (Group IV) Alexandrium cf. catenella VGO599 Med Sea + - (Group IV) Alexandrium cf. tamarense VGO1042 Med Sea — + (Group II) Alexandrium tamarense AT5 North Sea +++ ND (Group III) Alexandrium minutum AL2V Atlantic + ND Alexandrium minutum AL9C Med Sea + + Alexandrium minutum AMP4 Med Sea - - Alexandrium minutum RCC3020 The Channel + ND Alexandrium minutum SZN030 CC1 Med Sea + ND Alexandrium minutum CBA38 Med Sea +++ ND Alexandrium minutum RCC3021 Atlantic + ND Alexandrium minutum RCC2646 The Channel + ND Alexandrium minutum RCC3022 The Channel + ND Alexandrium minutum RCC3416 Med Sea + ND Alexandrium minutum RCC3409 Med Sea + ND Alexandrium minutum RCC3410 Med Sea + ND Alexandrium minutum RCC3411 Med Sea +++ ND Alexandrium minutum RCC3412 Med Sea +++ ND Alexandrium minutum RCC3413 Med Sea +++ ND Alexandrium ostenfeldii CCAP1119/45 North Sea +++ ND Alexandrium ostenfeldii VGO956 Med Sea + + Alexandrium tamutum SZN029 Med Sea + + Alexandrium tamutum A8 Med Sea + + Alexandrium taylori VGO703 Med Sea — — Amphidinium carterae RCC1522 The Channel — — Coolia monotis VGO941 Med Sea — — Gymnodinium impudicum GY3VA Med Sea — — Gymnodinium instriatum ICMB234 Med Sea — Gymnodinium litoralis ICMB226 Med Sea — — Heterocapsa triquetra RCC3044 The Channel
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