Abstract
The dinoflagellates are an assemblage of autotrophic, myxotrophic and heterotrophic species and play important roles in marine ecosystems. Most of them are free-living, but several are known as symbionts of marine invertebrates or as parasites of aquatic animals and protists. Molecular phylogenetic studies on parasitic dinoflagellates reveal that the parasitism has evolved polyphyletically appearing several times independently within the division Dinophyta. The Dinophyta consists of “core” dinoflagellates (typical dinoflagellates) and “basal” dinoflagellates. Within the basal dinoflagellates, the parasitic clades of Perkinsea, Ellobiophyceae and Syndiniophyceae are recognized. A large portion of environmental clone sequences recovered from various parts of the oceanic environments are thought to be members of the parasitic order Syndiniales (Syndiniophyceae). Therefore, the ecological function of parasitic dinoflagellates in the ocean is now better understood. The members of parasitic genera such as Parvilucifera (Perkinsea) and Amoebophrya (Syndiniophyceae) infect other dinoflagellates; therefore, much attention has been paid, because of their possible ability to control harmful algal blooms (HABs). The parasitism has also evolved within the “core” dinoflagellates (Dinophyceae) a number of times. These include Blastodinium, Chytriodinium, Dissodinium, Haplozoon, Oodinium, Paulsenella and Tintinnophagus. Because there are already several reviews on diversity of parasitic dinoflagellates, in this volume, only recent developments in phylogenetic studies on parasitic marine dinoflagellates are mainly reviewed here.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alves-de-Souza C, Cornet C, Nowaezyk A, Gasparini S, Skovgaard A, Guillow L (2011) Blastodinium spp. infect copepods in the ultra-oligotrophic marine waters of the Mediterranean Sea. Biogeosciences 8:2125–2136
Appleton PL, Vickerman KV (1988) In vitro cultivation and development cycle in culture of a parasitic dinoflagellate (Hematodinium sp.) associated with mortality of the Norway lobster (Nephrops norvegicus) in British waters. Parasitology 116:115–130
Bachvaroff TR, Kim S, Guillou L, Delwiche CF, Wayne C (2012) Molecular diversity of the syndenean genus Euduboscquella based on single-cell PCR analysis. Appl Environ Microbiol 78:334–345
Bachvaroff TR, Gornik SG, Concepcion GT, Waller RF, Mendez GS, Lippmeier JC, Delwiche CF (2014) Dinoflagellate phylogeny revisited: using ribosomal proteins to resolve deep branching dinoflagellate clades. Mol Phylogenet Evol 70:314–322
Briåte J, Logares R, Berney C, Ree DK, Klaveness D, Jakobsen KS, Shalchian-Tabrizi K (2010) Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4:1144–1153
Brown EM, Hovasse R (1946) Amyloodinium ocellatum (Brown), a peridinian parasitic on marine fishes. A complementary study. Proc Zool Soc Lond 116:33–46
Cachon J (1964) Contribution a l’étude des Péridiniens parasites: cytology, cycles évolutifs. Ann Sci Nat Zool 6:1–158
Cachon J, Cachon M (1977) Observations on the mitosis and on the chromosome evolution during the life-cycle of Oodinium. A parasitic dinoflagellate. Chromosoma 60:237–251
Cachon J, Cachon M (1987) Parasitic dinoflagellates. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell, Oxford, pp 540–552
Caullery M (1910) Ellobiopsis chattoni, n. g., n. sp., parasite de Calanus helgolandicus Claus, apparent probablement aux Péridiens. Bull Sci Fr Belg 44:201–214
Chambouvet A, Morin P, Marie D, Guillou L (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322:1254–1257
Chambouvet A, Laabir M, Sengco M, Vaquer A, Guillow L (2011) Genetic diversity of Amoebophryidae (Syndiniales) during Alexandrium catenella/tamarense (Dinophyceae) blooms in the Thau lagoon (Mediterranean Sea, France). Res Microbiol 162:959–968
Chatton E (1910) Sur l’existence de dinoflagellés parasites coelomiques. Les Syndinium chez les copépodes pélagiques. C R Hebd Séances Acad Sci 102:654–656
Chatton E (1912) Diagnoses préliminare de Péridiniens parasites nouveaux. Bull Soc Zool Fr 37:85–93
Chatton E (1920) Les Péridiniens parasites. Morphologie, reproduction, éthologie. Arch Zool Exp Gén 59:1–475
Chatton E (1952) Classses des dinoflagellés ou péridiniens (Dinoflagellata Bütschli, 1885 Peridinaea Ehrenberg, 1830 Peridiniales Schütt, 1896). In: Grassé P (ed) Traité de Zoologie, vol 1. Masson et Cie, Paris, pp 1309–1406
Chatton E, Poisson R (1931) Sur l’existence, dans le sang des Crabes, de Peridiniens parasites: Hematodinium perezi n. g., n. sp. (Syndinidae). C R Seances Soc Biol Paris 105:553–557
Coats DW (1988) Duboscquella cachoni sp. nov., a parasitic dinoflagellate lethal to its tintinnine host Eutintinnus pectinis. J Protozool 35:607–617
Coats DW (1999) Parasitic life styles of marine dinoflagellates. J Eukaryot Microbiol 46:402–409
Coats DW, Bachvaroff TR (2013) Parasites of Tintinnids. In: Dolan JR, Montagnes DJS, Agatha S, Coats DW, Stoecker DK (eds) The biology and ecology of Tintinnid Ciliates. Wiley, Hoboken, pp 145–170
Coats DW, Heisler JJ (1989) Spatial and temporal occurrence of the parasitic dinoflagellate Duboscquella cachoni and its tintinnine host Eutintinnus pectinis in Chesapeake Bay. Mar Biol 101:401–409
Coats DW, Bachvaroff T, Handy SM, Kim S, Gárate Lizárraga I, Delwiche CF (2008) Prevalence and phylogeny of parasitic dinoflagellates (genus Blastodinium) infecting copepods in the Gulf of California. CICIMAR Oceánies 23:67–77
Coats DW, Kim S, Bachvaroff TR, Handy SM, Delwiche CF (2010) Tintinnophagus acutus n. g., n. sp. (Phylum Dinoflagellata), an ectoparasite of the ciliate Tintinnopsis cylindrical Dady 1887, and its relationship to Duboscquodinium collini Grassé. J Eukaryot Microbiol 57:468–482
Coats DW, Bachvaroff TR, Delwiche CF (2012) Revision of the family Duboscquellidae with description of Euduboscquella crenulata n. gen., n. sp (Dinoflagellata, Syndinea), an intracellular parasite of the ciliate Favella panamensis Kofoid & Campbell, 1929. J Eukaryot Microbiol 59:1–11
Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000) Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302–317
Dogiel V (1906) Beiträge zur Kenntnis der Perdineen. Mitt Zool Stn Neapel 18:1–45
Dolven JK, Lindqvist C, Albert VA, Bjørklund KR, Yuasa T, Takahashi O, Mayama S (2007) Molecular diversity of alveolates associated with neritic North Atlantic radiolarians. Protist 158:65–76
Drebes G (1969) Dissodinium pseudocalani sp. nov., ein parasitischer Dinoflagellat auf Copepodeneiern. Helgoländer Meersun 19:58–67
Drebes G, Schnepf E (1982) Phagotrophy and development of Paulsenella cf. chaetoceratis (Dinophyta), an ectoparasite of the diatom Streptotheca thamesis. Helgoländer Meersun 35:501–515
Drebes G, Schnepf E (1988) Paulsenella Chatton (Dinophyta), ectoparasites of marine diatoms: development and taxonomy. Helgoländer Meersun 52:1–14
Elbrächter M, Drebes G (1978) Life cycle, phylogeny and taxonomy of Dissodinium and Pyrocystis (Dinophyta). Helgoländer Meersun 31:347–366
Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Williams GL (1993) A classification of living and fossil dinoflagellates, American Museum of Natural History, Micropaleontology, Special Publication Number 7. pp 351
Figueroa RI, Garcés E, Massana R, Camp J (2008) Description, host-specificity, and strain selectivity of the dinoflagellate parasite Parvilucifera sinerae sp. nov. (Perkinsozoa). Protist 159:563–578
Frischer ME, Lee RF, Sheppard MA, Mauer A, Rambow F, Neuman M, Brofft JE, Wizenmann T, Danforth JM (2006) Evidence for a free-living life stage of the blue crab parasitic dinoflagellate, Hematodinium sp. Harmful Algae 5:548–557
Fritz L, Nass M (1992) Development of the endoparasitic dinoflagellate Amoebophrya ceratii within host dinoflagellate species. J Phycol 28:312–320
Gaines G, Elbrächter M (1987) Heterotrophic nutrition. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell, Oxford, pp 224–268
Gómez F (2012) A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). CICIMAR Oceánies 27:65–140
Gómez F, López-García P, Nowaczyk A, Moreira D (2009) The crustacean parasites Ellobiopsis Caullery, 1910 and Thalassomyces Niezabitowski, 1913 for a monophyletic divergent clade within the Alveolata. Syst Parasitol 74:65–74
Gómez-Gutiérrez J, Kawaguchi S, Nicol S (2009) Epibiotic suctorians and enigmatic ecto and endoparasitoid dinoflagellates of euphausiid eggs (Euphausiaceae) off Oregon, USA. J Plankton Res 31:777–786
Gornik SG, Ford KL, Mulhern TD, Bacic A, McFadden GI, Waller RF (2012) Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Curr Biol 22:2303–2312
Gornik SG, Cranenburgh A, Waller RF (2013) New host range for Hematodinium in Southern Australia and novel tools for sensitive detection of parasitic dinoflagellates. PLoS One 8(12):e82774
Groisillier A, Massana R, Valentin K, Vaulot D, Guillou L (2006) Genetic diversity and habitats of two enigmatic marine alveolate lineages. Aquat Microb Ecol 42:277–291
Gruebl T, Fischer ME, Sheppard M, Neumann M, Maurer AN, Lee RF (2002) Development of an 18S rRNA gene-targeted PCR based diagnostic for the blue crab parasite Hematodinium sp. Dis Aquat Org 49:61–70
Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, Scanlan DJ, Worden AZ (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10:3349–3365
Gunderson JH, John SA, Boman IIWC, Coats DW (2002) Multiple strains of the parasitic dinoflagellate Amoebophyra exist in Chesapeake Bay. J Eukaryot Microbiol 49:469–474
Harada A, Ohtsuka S, Horiguchi T (2007) Species of the parasitic genus Duboscquella are members of the enigmatic Marine Alveolate Group I. Protist 158:337–347
Hollande A, Cachon J (1952) Un parasite des oeufs de sardine: l’Ichthyodinium chabelardi nov. gen. nov. sp. (Péridinien parasite). C R Acad. Sci, Paris 235:976–977
Horiguchi T, Ohtsuka S (2001) Oodinium inlandicum sp. nov. (Blastodiniales, Dinophyta) a new ectoparasitic dinoflagellate infecting a chaetognath, Sagitta crassa. Plankton Biol Ecol 48:85–95
Horiguchi T, Harada A, Ohtsuka S (2006) Taxonomic studies on parasitic dinoflagellates in Japan. Bull Plankton Soc Jpn 53:21–29 (in Japanese with English abstract)
Hovasse R (1935) Deux Peridiniens parasites convergents: Oodinium poucheti (Lemm.), Protoodinium chattoni gen. nov. sp. nov. Bull Biol Fr Belg 69:59–86
Hudson DA, Shields JD (1994) Hematodinium australis n. sp., a parasitic dinoflagellate of the sand crab Portunus pelagicus from Moreton Bay, Australia. Dis Aquat Org 19:109–119
Janson S, Gisselson LA, Salomon PS, Granéli E (2000) Evidence for multiple species within the endoparasitic dinoflagellate Amoebophrya ceratii as based on 18S rRNA gene-sequence analysis. Parasitol Res 86:929–933
Kane JE (1964) Thalassomyces marsupii, a new species of ellobiopsid on the hyperiid amphipod, Parathemist gauchudii (Guer.). N Z J Sci 7:289–303
Kim S, Park MG, Kim KY, Kim CH, Yih W, Park JS, Coats DW (2008) Genetic diversity of parasitic dinoflagellates in the genus Amoebophrya and its relationship to parasite biology and biogeography. J Eukaryot Microbiol 55:1–8
Kühn WF, Medlin LK (2005) The systematic position of the parasitoid marine dinoflagellate Paulsenella vonstoschii (Dinophyceae) inferred from nuclear-encoded small subunit ribosomal DNA. Protist 156:393–398
Leander BS, Hoppenrath M (2008) Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata, Myzozoa). Eur J Protistol 44:55–70
Leander BS, Keeling PJ (2003) Morphostasis in alveolate evolution. Trends Ecol Evol 18:395–402
Leander BS, Saldarriaga JF, Keeling PJ (2002) Surface morphology of the marine parasite Haplozoon axiothellae Siebert (Dinoflagellata). Eur J Protistol 38:287–297
Lepelletier F, Karpov SA, Panse SL, Bigeard E, Skovgaard A, Jeanthon C, Guillou L (2014) Parvilucifera rostrata sp. nov. (Perkinsozoa), a novel parasitoid that infects planktonic dinoflagellates. Protist 165:31–49
Levine ND (1978) Perkinsus gen. n. and other new taxa in the protozoan phylum Apicomplexa. J Parasitol 64:549
Loeblich AR III (1976) Dinoflagellate evolution: speculation and evidence. J Protozool 23:13–28
Lom J (1981) Fish invading dinoflagellates: a synopsis of existing and newly proposed genera. Folia Parasitol 28:3–11
López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607
McLean N, Nielsen C (1989) Oodinium jourdani n. sp., a dinoflagellate (Dinoflagellata, Oodinidae) ectoparasitic on Sagitta elegans (Chaetognatha). Dis Aquat Org 7:61–66
Miller JJ, Delwiche CF, Coats DW (2012) Ultrastructure of Amoebophrya sp. and its changes during the course of infection. Protist 163:720–745
Moon-van der Staay SY, Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607–610
Nagasawa K (2004) Aquaparasitology in the field in Japan. Tokai University Press, Hatano (in Japanese)
Norén F, Moestrup Ø, Rehnstam-Holm AS (1999) Parvilucifera infectans Norén et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Eur J Protistol 35:233–254
Not F, del Campo J, BlaquEé V, de Vargas C, Massana R (2009) Insights into the diversity of marine picoeukaryote. PLoS One 4(9):e7143
Okamoto N, Horák A, Keeling PJ (2012) Description of two species of early branching dinoflagellates, Psammosa pacifica n. g., n. sp. and P. atlantica n. sp. PLoS One 7(6):e34900
Park MG, Kim S, Shin EY, Yih W, Coats DW (2013) Parasitism of harmful dinoflagellates in Korean coastal waters. Harmful Algae 30:562–574
Pasternak AF, Arashkevich YG, Sorokin YS (1984) The role of the parasitic algal genus Blastodinium in the ecology of planktonic copepods. Oceanology 24:748–751
Peacock EE, Olson RJ, Sosik HM (2014) Parasitic infection of the diatom Guinardia delicatula, a recurrent and ecologically important phenomenon on the New England Shelf. Mar Ecol Prog Ser 503:1–10
Rueckert S, Leander BS (2008) Morphology and molecular phylogeny of Haplozoon praxillellae n. sp. (Dinoflagellata): a novel intestinal parasite of the maldanid polychatete Praxillella pacifica Berkeley. Eur J Protistol 44:299–307
Saldarriaga JF, Taylor FJR, Cavalier-Smith T, Menden-Deuer S, Keeling PJ (2004) Molecular data and the evolutionary history of dinoflagellates. Eur J Protistol 40:85–111
Salomon PS, Janson S, Granéli E (2003) Multiple species of the dinophagous dinoflagellate genus Amoebophrya infect the same host species. Environ Microbiol 5:1046–1052
Schnepf E, Drebes G (1986) Chemotaxis and appetence of Paulsenella sp. (Dinophyta), an ectoparasite of the marine diatom Streptotheca thamesis Shrubsole. Planta 167:337–343
Shields JD (1994) The parasitic dinoflagellates of marine crustaceans. Annu Rev Fish Dis 9:255–394
Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpekdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Bhattacharya D, Satoh N (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399–1408
Shumway W (1924) The genus Haplozoon. Dogiel observations on the life history and systematic position. J Parasitol 11:59–74
Siano R, Alves-de-Souza C, Foulon E, Bendif EM, Simon N, Guillou L, Not F (2011) Distribution and host diversity of Amoebophryidae parasites across oligotrophic waters of the Mediterranean Sea. Biogeosciences 8:267–278
Siebert AE, West JA (1974) The fine structure of the parasitic dinoflagellate Haplozoon axiothellae. Protoplasma 81:17–35
Silberman JD, Collins AG, Gershwin LA, Johnson PJ, Roger AJ (2004) Ellobiopsids of the genus Thalassomyces are alveolates. J Eukaryot Microbiol 52:246–252
Skovgaard A (2005) Blastodinium spp. in two Mediterranean copepods. Aquat Microb Ecol 38:93–101
Skovgaard A (2014) Dirty tricks in the plankton: diversity and role of marine parasitic protists. Acta Protozool 53:51–62
Skovgaard A, Salomonsen XM (2009) Blastodinium galatheanum sp. nov. (Dinophyceae) a parasite of the planktonic copepod Acartia negligens (Crustacea, Calanoida) in the central Atlantic Ocean. Eur J Phycol 44:425–438
Skovgaard A, Massana R, Balagué V, Saiz E (2005) Phylogenetic position of the copepod-infesting parasite Syndinium turbo (Dinoflagellata, Syndinea). Protist 156:413–423
Skovgaard A, Massana R, Saiz E (2007) Parasitic species of the genus Blastodinium (Blastodiniphyceae) are peridinioid dinoflagellates. J Phycol 43:553–560
Skovgaard A, Meneses I, Angélico MM (2009) Identifying the lethal fish egg parasite Ichthyodinium chabelardi as a member of Marine Alveolate Group I. Environ Microbiol 11:2030–2041
Skovgaard A, Karpov SA, Guillou L (2012) The parasitic dinoflagellates Blastodinium spp. inhabiting the gut of marine, planktonic copepods: morphology, ecology and unrecognized species diversity. Front Microbiol 3:305
Small HJ, Shields JD, Reece KS, Bateman K, Stentiford GD (2012) Morphological and molecular characterization of Hematodinium perezi (Dinophyceae, Syndiniales), a dinoflagellate parasite of the harbor crab, Liocarcinus depurator. J Eukaryot Microbiol 59:54–66
Sørensen SR, Tomkiewicz J, Skovgaard A (2014) Ichthyodinium identified in the eggs of European eel (Anguilla anguilla) spawned in captivity. Aquaculture 426–427:197–203
Soyer MO (1970) Etude ultrastructurale de l’endoplasme et des vacuoles chez deux types de Dinoflagellés aux genres Noctiluca (Suriray) et Blastodinium (Chatton). Z Ze forschMikrosk Anat 105:350–388
Soyer MO (1971) Structure du noyau des Blastodinium (Dinoflagellés parasites). Division et condensation chromatique. Chromosoma 33:70–114
Stentiford GD, Shields JD (2005) A review of the parasitic dinoflagellates Hematodinium species and Hematodinium-like species infections in marine crustaceans. Dis Aquat Org 66:47–70
Villalba A, Reece KS, Ordás MC, Casas SM, Figueras A (2004) Perkinsosis in molluscs: a review. Aquat Living Resour 17:411–432
Whisler HC (1990) Incertae Sedis, Ellobiopsida. In: Margulis L, Corliss JO, Melkonian M, Chapman DJ (eds) Handbook of Protoktista. Jones and Bartlett Publishers, Boston, pp 715–719
Zachs I (1923) Sur un nouveau Ellobiopsidé – Parasite du Nephtys ciliate Müll. Trav Soc Nat Petrograd 53:175–176
Acknowledgments
I would like to thank to the following colleagues for kindly providing the images of parasitic dinoflagellates, Dr. Gerhard Drebes, Dr. Mona Hoppenrath, Dr. Susumu Ohtsuka and Dr. Yoshihito Takano. My sincere thanks go to Dr. Jaime Gómez-Gutiérrez for kindly reading the manuscript. I also would like to thank my former students, Ms. Ai Harada and Mr. Kosho Ishiguro, who worked on parasitic dinoflagellates with me.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer Japan
About this chapter
Cite this chapter
Horiguchi, T. (2015). Diversity and Phylogeny of Marine Parasitic Dinoflagellates. In: Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N., Not, F. (eds) Marine Protists. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55130-0_16
Download citation
DOI: https://doi.org/10.1007/978-4-431-55130-0_16
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-55129-4
Online ISBN: 978-4-431-55130-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)