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Keywords ABSTRACT
Copepod; Dissodinium; Gymnodinium sensu
stricto; parasite Dinophyta; parasitism. The dinoflagellate genus Chytriodinium, an ectoparasite of copepod eggs, is
reported for the first time in the North and South Atlantic Oceans. We provide
Correspondence the first large subunit rDNA (LSU rDNA) and Internal Transcribed Spacer 1
F. Gomez, Laboratory of Plankton Systems, (ITS1) sequences, which were identical in both hemispheres for the Atlantic
sala 100, Oceanographic Institute, University Chytriodinium sp. The first complete small subunit ribosomal DNA (SSU rDNA)
of S~
ao Paulo, Pracßa do Oceanografico 191, of the Atlantic Chytriodinium sp. suggests that the specimens belong to an
Cidade Universit
aria, S~ao Paulo, undescribed species. This is the first evidence of the split of the Gymnodinium
SP 05508-900, Brazil clade: one for the parasitic forms of Chytriodiniaceae (Chytriodinium, Dissodini-
Telephone number: +55-11-30918963; um), and other clade for the free-living species.
Fax: +55-11-30916607; e-mail: fernando.
gomez@fitoplancton.com
doi:10.1111/jeu.12180
COPEPODS dominate the zooplankton biomass and are western Mediterranean Sea, with some recent records of
considered to be the most abundant animals in the ocean. C. affine from the Pacific Ocean (Go mez-Gutie rrez et al.
The lipid-rich copepod eggs are the target of the special- 2009; Meave del Castillo et al. 2012). It is clear that abun-
ized parasitic dinoflagellates Chytriodinium and Dissodini- dance and ecological role is being underestimated.
um which dinospores are able to infest crustacean eggs, Gomez et al. (2009) provided the first molecular data
absorb the host content and form successive cysts that based on the partial SSU rDNA sequence of the species
produce colorless gymnodinioid spores (Cachon and Ca- Chytriodinium affine and C. roseum from the Mediterra-
chon 1968; see Video S1 http://youtu.be/nwFZQAAm- nean Sea. Chytriodinium branched within the so-called
QaA). Gymnodinium sensu stricto or Gymnodinium clade
Our knowledge of the members of the family Chytriodi- (Daugbjerg et al. 2000). This clade showed a strong diver-
niaceae is limited. Some stages of the life cycle of Dissodi- sification in the trophic modes with plastids of different
nium psedolunula, such as the lunate sporangia, are highly microalgal origins and development of specialized organ-
distinctive and commonly recognized by plankton research- elles (nematocyst, ocelloid, or piston) that are unknown in
ers (Gomez and Artigas 2013). In contrast, Chytriodinium other dinoflagellate clades.
is absent in identification guides, and it easily goes unno- The current molecular information on Chytriodinium is
ticed especially in fixed samples. The genus comprises restricted to partial SSU rDNA sequences of Mediterra-
three species. In Chytriodinium affine, the numerous di- nean specimens. The complete SSU rDNA sequence and
nospores develops in a coiled chain inside a hyaline spheri- additional molecular markers (LSU rDNA, ITS1) will allow
cal membrane that was absent in the chain of C. roseum. to test whether the heterotrophic Chytriodinium and pho-
Chytriodinium parasiticum parasitizes larger crustacean tosynthetic Dissodinium were or maybe are derived from
eggs, and forms a sophisticated stalk apparatus (Cachon a recent common ancestor or the parasitism appeared
and Cachon 1968). These species are only known from the independently in the Gymnodinium clade.
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
422 Journal of Eukaryotic Microbiology 2015, 62, 422–425
mez & Skovgaard
Go Phylogeny of Parasitic Chytriodinium in Gymnodinium Clade
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
Journal of Eukaryotic Microbiology 2015, 62, 422–425 423
Phylogeny of Parasitic Chytriodinium in Gymnodinium Clade mez & Skovgaard
Go
Figure 1 Phylogeny tree inferred from the SSU rDNA sequences using Bayesian inference method. The species newly sequenced in this study
are bold. Accession numbers are provided. Posterior probability of 1 is denoted with a black circle; white circles denote posterior probability of
0.95–0.99. ML bootstrap support (when above 50%) is given near nodes. The scale bar represents the number of substitutions per site. Numbers
at the end of each taxon name are GenBank accession numbers.
morphology of the dinospores of the Mediterranean Chytri- odinium affine and Chytriodinium sp. from the tropical
odinium affine has not been examined in detail in order to Atlantic Ocean. The size, shape and general appearance
establish differences with other tentative species. No obvi- of the infective spores of the Mediterranean and Atlantic
ous differences exist between the Mediterranean Chytri- species is similar. The life cycle and appearance of the
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
424 Journal of Eukaryotic Microbiology 2015, 62, 422–425
mez & Skovgaard
Go Phylogeny of Parasitic Chytriodinium in Gymnodinium Clade
sporangium is also similar. All the reported observations of Coats, D. W., Kim, S., Bachvaroff, T. R., Handy, S. M. & Delwi-
Chytriodinium affine in the Mediterranean Sea concern che, C. F. 2010. Tintinnophagus acutus n. g., n. sp. (Phylum Di-
infections of individual eggs of free-spawning copepod noflagellata), an ectoparasite of the ciliate Tintinnopsis cylindrica
species (Cachon and Cachon 1968; Go mez et al. 2009). In Daday 1887, and its relationship to Duboscquodinium collini
Grasse 1952. J. Eukaryot. Microbiol., 57:468–482.
contrast, the Atlantic specimens of Chytriodinium of both
Daugbjerg, N., Hansen, G., Larsen, J. & Moestrup, Ø. 2000. Phy-
hemispheres were exclusively observed infecting egg sacs logeny of some of the major genera of dinoflagellates based on
of brood-carrying copepod species (Fig. S1–S2). To the ultrastructure and partial LSU rDNA sequence data, including
best of our knowledge this feature is reported for the first the erection of three new genera of unarmoured dinoflagellates.
time in the genus Chytriodinium. At the present, differ- Phycologia, 39:302–317.
ence in host species is the main character distinguishing mez, F. & Artigas, L. F. 2013. The formation of the twin resting
Go
the Atlantic species and Chytriodinium affine. However, it cysts in the dinoflagellate Dissodinium pseudolunula, a parasite
is necessary to perform infection experiments to verify of copepod eggs. J. Plankton Res., 35:1167–1171.
whether this apparent host specificity is exclusively due to mez, F., Moreira, D. & Lo
Go pez-Garcıa, P. 2009. Life cycle and
the type of egg available. molecular phylogeny of the dinoflagellates Chytriodinium and
Dissodinium, ectoparasites of copepod eggs. Eur. J. Protistol.,
Similar to the presence or absence of plastids, parasit-
45:260–270.
ism is known for numerous groups of dinoflagellates mez-Gutie
Go rrez, J., Kawaguchi, S. & Nicol, S. 2009. Epibiotic
(Coats et al. 2010). Gymnodinium aureolum ingests only suctorians and enigmatic ecto- and endoparasitoid dinoflagel-
small microalgal preys through a peduncle and divides by lates of euphausiid eggs (Euphausiacea) off Oregon, USA. J.
binary division (Jeong et al. 2010). This mechanism of Plankton Res., 31:777–785.
feeding may be essentially the same as in members of Jeong, H. J., Yoo, Y. D., Kang, N. S., Rho, J. R., Seong, K. A.,
Chytriodiniaceae that possess a more sophisticated Park, J. W., Nam, G. S. & Yih, W. 2010. Ecology of Gymnodini-
peduncle (i.e., C. parasiticum, see Video S1 as supporting um aureolum. I. Feeding in western Korean waters. Aquat. Mic-
information, http://youtu.be/nwFZQAAmQaA). Dissodini- rob. Ecol., 59:239–255.
Meave del Castillo, M. E., Zamudio-Rese ndiz, M. E. & Castillo-Ri-
um, Chytriodinium and Myxodinium are able to feed on
vera, M. 2012. Riqueza fitoplancto nica de la Bahıa de Acapulco
larger preys, and this allows producing a high number of
y zona costera aledan ~a, Guerrero, Me xico. Acta Bot. Mex.,
dinospores after each infection. This study provides the 100:405–487.
first evidence of the split of the Gymnodinium clade: one
for the parasitic forms of Chytriodiniaceae (Chytriodinium,
Dissodinium), and other clade for the free-living species. SUPPORTING INFORMATION
Additional Supporting Information may be found in the
ACKNOWLEDGMENTS online version of this article:
We thank E. Otero and B. M. Soler for the hospitality Figure S1. Light micrographs of Chytriodinium sp. from
extended during the sampling in Puerto Rico, and the Bahıa Fosforescente, Puerto Rico.
assistance of CEBIMar technical staff (USP, S~ao Sebas- Figure S2. Light micrographs of Chytriodinium sp. from
ti~
ao). F.G. is currently supported by the Brazilian Conselho S~
ao Sebasti~ ao Channel, Brazil.
Nacional de Desenvolvimento Cientıfico e Tecnolo gico Figure S3. Phylogeny tree inferred from LSU rDNA
(grant number BJT 370646/2013-14). A.S. was supported sequences using Bayesian inference method.
through the project IMPAQ - IMProvement of AQuaculture Data S1. Materials and methods.
high quality fish fry production, funded by the Danish Video S1. The parasitic dinoflagellate Chytriodinium from
Council for Strategic Research. Villefranche sur Mer, France, by J. Cachon and M. Cachon,
http://youtu.be/nwFZQAAmQaA.
Video S2. The parasitic dinoflagellate Chytriodinium from
LITERATURE CITED
Bahı́a Fosforescente, Puerto Rico, http://youtu.be/JA_
Cachon, J. & Cachon, M. 1968. Cytologie et cycle e volutif des Gu57WkXQ.
Chytriodinium (Chatton). Protistologica, 4:249–262.
© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists
Journal of Eukaryotic Microbiology 2015, 62, 422–425 425