Organisms Diversity & Evolution

, Volume 18, Issue 1, pp 29–38 | Cite as

Absence of co-phylogeny indicates repeated diatom capture in dinophytes hosting a tertiary endosymbiont

  • Anže Žerdoner Čalasan
  • Juliane Kretschmann
  • Marc GottschlingEmail author
Original Article


Tertiary endosymbiosis is proven through dinophytes, some of which (i.e. Kryptoperidiniaceae) have engulfed diatom algae containing a secondary plastid. Chloroplasts are usually inherited together permanently with the host cell, leading to co-phylogeny. We compiled a diatom sequence data matrix of two nuclear and two chloroplast loci. Almost all endosymbionts of Kryptoperidiniaceae found their closest relatives in free-living diatoms and not in other harboured algae, rejecting co-phylogeny and indicating that resident diatoms were taken up by dinophytes multiple times independently. Almost intact ultrastructure and insignificant genome reduction are supportive for young, if not recent events of diatom capture. With their selective specificity on the one hand and extraordinary degree of endosymbiotic flexibility on the other hand, dinophytes hosting diatoms share more traits with lichens or facultatively phototrophic ciliates than with green algae and land plants. Time estimates indicate the dinophyte lineages as consistently older than the hosted diatom lineages, thus also favouring a repeated uptake of endosymbionts. The complex ecological role of dinophytes employing a variety of organismic interactions may explain their high potential and plasticity in acquiring a great diversity of plastids.


Chloroplast Dinoflagellates Dinotoms Endosymbiosis Evolution Mutualism 



Financial support was provided by the Deutsche Forschungsgemeinschaft (grant GO 1549 10-1) and the Münchener Universitätsgesellschaft. We thank Nina Simanovic for improving the English text, and the Scientific Committee of the 11th International Conference on Modern and Fossil Dinoflagellates for awarding the first author of this study with the Best Young Scientist Oral Presentation.

Supplementary material

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  1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alverson, A. J., Jansen, R. K., & Theriot, E. C. (2007). Bridging the Rubicon: phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Molecular Phylogenetics and Evolution, 45, 193–210.CrossRefPubMedGoogle Scholar
  3. Alverson, A. J., Beszteri, B., Julius, M. L., Theriot, E. C. (2011). The model marine diatom Thalassiosira pseudonana likely descended from a freshwater ancestor in the genus Cyclotella. BMC Evolutionary Biology, 11, 125.Google Scholar
  4. Burki, F. (2014). The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harbor Perspectives in Biology, 6, a016147.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chesnick, J. M., Kooistra, W. H. C. F., Wellbrock, U., & Medlin, L. K. (1997). Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta). Journal of Eukaryotic Microbiology, 44, 314–320.CrossRefPubMedGoogle Scholar
  6. Dodge, J. D. (1966). The Dinophyceae. In M. B. E. Godward (Ed.), The chromosomes of the algae (pp. 96–115). New York: St. Martin’s Press.Google Scholar
  7. Dodge, J. D. (1971). A dinoflagellate with both a mesokaryotic and a eukaryotic nucleus. I. Fine structure of the nuclei. Protoplasma, 73, 145–157.Google Scholar
  8. Dodge, J. D. (1983). The functional and phylogenetic significance of dinoflagellate eyespots. Biosystems, 16, 259–267.CrossRefPubMedGoogle Scholar
  9. Dodge, J. D. (1989). Phylogenetic relationship of dinoflagellates and their plastids. In J. C. Green, B. S. C. Leadbeater, & W. L. Diver (Eds.), The chromophyte algae. Problems and perspectives (pp. 205–227). Oxford: Clarendon Press.Google Scholar
  10. Dorrell, R. G., & Howe, C. J. (2015). Integration of plastids with their hosts: lessons learned from dinoflagellates. Proceedings of the National Academy of Science of the United States of America, 112, 10247–10254.CrossRefGoogle Scholar
  11. Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fensome, R. A., MacRae, R. A., Moldowan, J. M., Taylor, F. J. R., & Williams, G. L. (1996). The early Mesozoic radiation of dinoflagellates. Paleobiology, 22, 329–338.CrossRefGoogle Scholar
  13. Fensome, R. A., Saldarriaga, J. F., & Taylor, F. J. R. (1999). Dinoflagellate phylogeny revisited: reconciling morphological and molecular based phylogenies. Grana, 38, 66–80.CrossRefGoogle Scholar
  14. Figueroa, R. I., Bravo, I., Fraga, S., Garces, E., & Llaveria, G. (2009). The life history and cell cycle of Kryptoperidinium foliaceum, a dinoflagellate with two eukaryotic nuclei. Protist, 160, 285–300.CrossRefPubMedGoogle Scholar
  15. Gagat, P., Bodył, A., Mackiewicz, P., & Stiller, J. W. (2014). Tertiary plastid endosymbioses in dinoflagellates. In Löffelhardt (Ed.), Endosymbiosis (pp. 233–290). Vienna: Springer.Google Scholar
  16. Garcia-Cuetos, L., Moestrup, Ø., Hansen, P. J., & Daugbjerg, N. (2010). The toxic dinoflagellate Dinophysis acuminata harbors permanent chloroplasts of cryptomonad origin, not kleptochloroplasts. Harmful Algae, 9, 25–38.CrossRefGoogle Scholar
  17. Gast, R. J., Moran, D. M., Dennett, M. R., & Caron, D. A. (2007). Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environmental Microbiology, 9, 39–45.CrossRefPubMedGoogle Scholar
  18. Gottschling, M., & McLean, T. I. (2013). New home for tiny symbionts: dinophytes determined as Zooxanthella are Peridiniales and distantly related to Symbiodinium. Molecular Phylogenetics and Evolution, 67, 217–222.CrossRefPubMedGoogle Scholar
  19. Gottschling, M., Renner, S. S., Meier, K. J. S., Willems, H., & Keupp, H. (2008). Timing deep divergence events in calcareous dinoflagellates. Journal of Phycology, 44, 429–438.CrossRefPubMedGoogle Scholar
  20. Gottschling, M., & Söhner, S. (2013). An updated list of generic names in the Thoracosphaeraceae. Microorganisms, 1, 122–136.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gottschling, M., Söhner, S., Zinßmeister, C., John, U., Plötner, J., Schweikert, M., Aligizaki, K., & Elbrächter, M. (2012). Delimitation of the Thoracosphaeraceae (Dinophyceae), including the calcareous dinoflagellates, based on large amounts of ribosomal RNA sequence data. Protist, 163, 15–24.CrossRefPubMedGoogle Scholar
  22. Gouy, M., Guindon, S., & Gascuel, O. (2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221–224.CrossRefPubMedGoogle Scholar
  23. Gu, H., Kirsch, M., Zinßmeister, C., Söhner, S., Meier, K. J. S., Liu, T., & Gottschling, M. (2013). Waking the dead: morphological and molecular characterization of extant †Posoniella tricarinelloides (Thoracosphaeraceae, Dinophyceae). Protist, 164, 583–597.CrossRefPubMedGoogle Scholar
  24. Händeler, K., Wägele, H., Wahrmund, U., Rüdinger, M., & Knoop, V. (2010). Slugs’ last meals: molecular identification of sequestered chloroplasts from different algal origins in Sacoglossa (Opisthobranchia, Gastropoda). Molecular Ecology Resources, 10, 968–978.CrossRefPubMedGoogle Scholar
  25. Hansen, G., Daugbjerg, N., & Henriksen, P. (2003). Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov. (= Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. Journal of Phycology, 36, 394–410.CrossRefGoogle Scholar
  26. Harper, J. T., Waanders, E., & Keeling, P. J. (2005). On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. International Journal of Systematic and Evolutionary Microbiology, 55, 487–496.CrossRefPubMedGoogle Scholar
  27. Hehenberger, E., Imanian, B., Burki, F., & Keeling, P. J. (2014). Evidence for the retention of two evolutionary distinct plastids in dinoflagellates with diatom endosymbionts. Genome Biology and Evolution, 6, 2321–2334.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Horiguchi, T., Kawai, H., Kubota, M., Takahashi, T., & Watanabe, M. (1999). Phototactic responses of four marine dinoflagellates with different types of eyespot and chloroplast. Phycological Research, 47, 101–107.CrossRefGoogle Scholar
  29. Horiguchi, T., & Pienaar, R. N. (1994). Ultrastructure and ontogeny of a new type of eyespot in dinoflagellates. Protoplasma, 179, 142–150.CrossRefGoogle Scholar
  30. Horiguchi, T., & Takano, Y. (2006). Serial replacement of a diatom endosymbiont in the marine dinoflagellate Peridinium quinquecorne (Peridiniales, Dinophyceae). Phycological Research, 54, 193–200.CrossRefGoogle Scholar
  31. Imanian, B., & Keeling, P. J. (2007). The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum retain functionally overlapping mitochondria from two evolutionarily distinct lineages. BMC Evolutionary Biology, 7, 172.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Imanian, B., Pombert, J. F., Dorrell, R. G., Burki, F., & Keeling, P. J. (2012). Tertiary endosymbiosis in two dinotoms has generated little change in the mitochondrial genomes of their dinoflagellate hosts and diatom endosymbionts. PLoS One, 7, e43763.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Imanian, B., Pombert, J. F., & Keeling, P. J. (2010). The complete plastid genomes of the two ‘dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum. PLoS One, 5, e10711.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Inagaki, Y., Dacks, J. B., Doolittle, W. F., Watanabe, K. I., & Ohama, T. (2000). Evolutionary relationship between dinoflagellates bearing obligate diatom endosymbionts: insight into tertiary endosymbiosis. International Journal of Systematic and Evolutionary Microbiology, 50, 2075–2081.Google Scholar
  35. Janouškovec, J., Gavelis, G. S., Burki, F., Dinh, D., Bachvaroff, T. S., Gornik, S. G., et al. (2017). Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proceedings of the National Academy of Science of the United States of America, 114, 171–180.CrossRefGoogle Scholar
  36. Jeffrey, S. W. (1989). Chlorophyll c pigments and their distribution in the chromophyte algae. In J. C. Green, B. S. C. Leadbeater, & W. L. Diver (Eds.), The chromophyte algae. Problems and perspectives (pp. 13–36). Oxford: Clarendon Press.Google Scholar
  37. Kamikawa, R., Tanifuji, G., Kawachi, M., Miyashita, H., Hashimoto, T., & Inagaki, Y. (2015). Plastid genome-based phylogeny pinpointed the origin of the green-colored plastid in the dinoflagellate Lepidodinium chlorophorum. Genome Biology and Evolution, 7, 1133–1140.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Keeling, P. J. (2004). Diversity and evolutionary history of plastids and their hosts. American Journal of Botany, 91, 1481–1493.CrossRefPubMedGoogle Scholar
  40. Keeling, P. J. (2010). The endosymbiotic origin, diversification and fate of plastids. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 729–748.CrossRefGoogle Scholar
  41. Keeling, P. J., Burki, F., Wilcox, H. M., Allam, B., Allen, E. E., Amaral-Zettler, L. A., et al. (2014). The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biology, 12, e1001889.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kempton, J. W., Wolny, J., Tengs, T., Rizzo, P., Morris, R., Tunnell, J., et al. (2002). Kryptoperidinium foliaceum blooms in South Carolina: a multi-analytical approach to identification. Harmful Algae, 1, 383–392.CrossRefGoogle Scholar
  43. Keupp, H. (1984). Revision der kalkigen Dinoflagellaten-Zysten G. Deflandres 1948. Palaeontologische Zeitschrift, 58, 9–31.CrossRefGoogle Scholar
  44. Keupp, H., & Ilg, A. (1989). Die kalkigen Dinoflagellaten im Ober-Callovium und Oxfordium der Normandie/Frankreich. Berliner Geowissenschaftliche Abhandlungen, A106, 165–206.Google Scholar
  45. Kretschmann, J., Žerdoner Čalasan, A., Gottschling, M. (in press). Molecular phylogenetics of dinophytes harboring diatoms as endosymbionts (Kryptoperidiniaceae, Peridiniales), with evolutionary interpretations and a focus on the identity of Durinskia oculata from Prague. Molecular Phylogenetics and Evolution.Google Scholar
  46. Leander, B. S., & Keeling, P. J. (2004). Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from hsp90 and actin phylogenies. Journal of Phycology, 40, 341–350.CrossRefGoogle Scholar
  47. Lee, J. J., McEnery, M. E., Ter Kuile, B., Erez, J., Röttger, R., Rockwell, R. F., et al. (1989). Identification and distribution of endosymbiotic diatoms in larger foraminifera. Micropaleontology, 35, 353–366.CrossRefGoogle Scholar
  48. Lee, J. J., Morales, J., Symons, A., & Hallock, P. (1995). Diatom symbionts in larger foraminifera from Caribbean hosts. Marine Micropaleontology, 26, 99–105.CrossRefGoogle Scholar
  49. Lee, M. A., Faria, D. G., Han, M. S., Lee, J., & Ki, J. S. (2013). Evaluation of nuclear ribosomal RNA and chloroplast gene markers for the DNA taxonomy of centric diatoms. Biochemical Systematics and Ecology, 50, 163–174.CrossRefGoogle Scholar
  50. Li, C. L., Ashworth, M. P., Witkowski, A., Dabek, P., Medlin, L. K., Kooistra, W. H. C. F., et al. (2015). New insights into Plagiogrammaceae (Bacillariophyta) based on multigene phylogenies and morphological characteristics with the description of a new genus and three new species. PLoS One, 10, e0139300.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Litchman, E., Klausmeier, C. A., & Yoshiyama, K. (2009). Contrasting size evolution in marine and freshwater diatoms. Proceedings of the National Academy of Science of the United States of America, 106, 2665–2670.CrossRefGoogle Scholar
  52. Lücking, R., Lawrey, J. D., Sikaroodi, M., Gillevet, P. M., Chaves, J. L., Sipman, H. J., & Bungartz, F. (2009). Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. American Journal of Botany, 96, 1409–1418.CrossRefPubMedGoogle Scholar
  53. McEwan, M. L., & Keeling, P. J. (2004). HSP90, tubulin and actin are retained in the tertiary endosymbiont genome of Kryptoperidinium foliaceum. Journal of Eukaryotic Microbiology, 51, 651–659.CrossRefPubMedGoogle Scholar
  54. Medlin, L. K. (2015). A timescale for diatom evolution based on four molecular markers: reassessment of ghost lineages and major steps defining diatom evolution. Vie et Milieu, 65, 219–238.Google Scholar
  55. Medlin, L. K., & Fensome, R. A. (2013). Dinoflagellate macroevolution: some considerations based on an integration of molecular, morphological and fossil evidence. In J. M. Lewis, F. Marret, & L. Bradley (Eds.), Biological and geological perspectives of dinoflagellates (pp. 263–274). Geological Society: London.CrossRefGoogle Scholar
  56. Moestrup, Ø., & Daugbjerg, N. (2007). On dinoflagellate phylogeny and classification. In J. Brodie & J. Lewis (Eds.), Unravelling the algae, the past, present, and future of algal systematics (pp. 215–230). CRC Press: Boca Raton.CrossRefGoogle Scholar
  57. Morden, C. W., & Sherwood, A. R. (2002). Continued evolutionary surprises among dinoflagellates. Proceedings of the National Academy of Science of the United States of America, 99, 11558–11560.CrossRefGoogle Scholar
  58. Moreno Díaz de la Espina, S., Alverca, E., Cuadrado, A., & Franca, S. (2005). Organization of the genome and gene expression in a nuclear environment lacking histones and nucleosomes: the amazing dinoflagellates. European Journal of Cell Biology, 84, 137–149.CrossRefPubMedGoogle Scholar
  59. Morris, R. L., Fuller, C. B., & Rizzo, P. J. (1993). Nuclear basic proteins from the binucleate dinoflagellate Peridinium foliaceum (Pyrrophyta). Journal of Phycology, 29, 342–347.CrossRefGoogle Scholar
  60. Nosenko, T., Lidie, K. L., Van Dolah, F. M., Lindquist, E., Cheng, J. F., & Bhattacharya, D. (2006). Chimeric plastid proteome in the Florida “red tide” dinoflagellate Karenia brevis. Molecular Biology and Evolution, 23, 2026–2038.CrossRefPubMedGoogle Scholar
  61. Okamoto, N., & Keeling, P. J. (2014). A comparative overview of the flagellar apparatus of dinoflagellate, perkinsids and colpodellids. Microorganisms, 2, 73–91.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Patron, N. J., Waller, R. F., & Keeling, P. J. (2006). A tertiary plastid uses genes from two endosymbionts. Journal of Molecular Biology, 357, 1373–1382.CrossRefPubMedGoogle Scholar
  63. Pienaar, R. N., Sakai, H., & Horiguchi, T. (2007). Description of a new dinoflagellate with a diatom endosymbiont, Durinskia capensis sp. nov. (Peridiniales, Dinophyceae) from South Africa. Journal of Plant Research, 120, 247–258.CrossRefPubMedGoogle Scholar
  64. Pochon, X., Putnam, H. M., Burki, F., & Gates, R. D. (2012). Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS One, 7, e29816.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Price, D. C., & Bhattacharya, D. (2017). Robust Dinoflagellata phylogeny inferred from public transcriptome databases. Journal of Phycology, 53, 725–729.CrossRefPubMedGoogle Scholar
  66. Qiu, D., Huang, L., & Lin, S. (2016). Cryptophyte farming by symbiotic ciliate host detected in situ. Proceedings of the National Academy of Science of the United States of America, 113, 12208–12213.CrossRefGoogle Scholar
  67. Rill, R. L., Livolant, F., Aldrich, H. C., & Davidson, M. W. (1989). Electron microscopy of liquid crystalline DNA: direct evidence for cholesteric-like organization of DNA in dinoflagellate chromosomes. Chromosoma, 98, 280–286.CrossRefPubMedGoogle Scholar
  68. Rines, J. E. B., & Hargraves, P. E. (1988). The Chaetoceros Ehrenberg (Bacillariophyceae) flora of Narragansett Bay, Rhode Island, U.S.A. Bibliotheca Phycologica, 79, 1–196.Google Scholar
  69. Rizzo, P. J. (2003). Those amazing dinoflagellate chromosomes. Cell Research, 13, 215–217.CrossRefPubMedGoogle Scholar
  70. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Schnepf, E., & Elbrächter, M. (1988). Cryptophycean-like double membranebound chloroplast in the dinoflagellate, Dinophysis Ehrenb.: Evolutionary, phylogenetic and toxicological implications. Botanica Acta, 101, 196–203.Google Scholar
  72. Schnepf, E., & Elbrächter, M. (1999). Dinophyte chloroplasts and phylogeny—a review. Grana, 38, 81–97.CrossRefGoogle Scholar
  73. Sorhannus, U. (2007). A nuclear-encoded small-subunit ribosomal RNA timescale for diatom evolution. Marine Micropaleontology, 65, 1–12.CrossRefGoogle Scholar
  74. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Stoecker, D. K. (1999). Mixotrophy among dinoflagellates. Journal of Eukaryotic Microbiology, 46, 397–401.CrossRefGoogle Scholar
  76. Streng, M., Hildebrand-Habel, T., & Willems, H. (2004). A proposed classification of archeopyle types in calcareous dinoflagellate cysts. Journal of Paleontology, 78, 456–483.CrossRefGoogle Scholar
  77. Takano, Y., Hansen, G., Fujita, D., & Horiguchi, T. (2008). Serial replacement of diatom endosymbionts in two freshwater dinoflagellates, Peridiniopsis spp. (Peridiniales, Dinophyceae). Phycologia, 47, 41–53.CrossRefGoogle Scholar
  78. Takano, Y., Yamaguchi, H., Inouye, I., Moestrup, Ø., & Horiguchi, T. (2014). Phylogeny of five species of Nusuttodinium gen. nov. (Dinophyceae), a genus of unarmoured kleptoplastidic dinoflagellates. Protist, 165, 759–778.CrossRefPubMedGoogle Scholar
  79. Tamura, M., Shimada, S., & Horiguchi, T. (2005). Galeidinium rugatum gen. et sp. nov. (Dinophyceae), a new coccoid dinoflagellate with a diatom endosymbiont. Journal of Phycology, 41, 658–671.CrossRefGoogle Scholar
  80. Taylor, F. J. R. (1980). On dinoflagellate evolution. Biosystems, 13, 65–108.CrossRefPubMedGoogle Scholar
  81. Taylor, F. J. R., Hoppenrath, M., & Saldarriaga, J. F. (2008). Dinoflagellate diversity and distribution. Biodiversity and Conservation, 17, 407–418.CrossRefGoogle Scholar
  82. Theriot, E. C., Ashworth, M. P., Nakov, T., Ruck, E., & Jansen, R. K. (2015). Dissecting signal and noise in diatom chloroplast protein encoding genes with phylogenetic information profiling. Molecular Phylogenetics and Evolution, 89, 28–36.CrossRefPubMedGoogle Scholar
  83. Tillmann, U., Gottschling, M., Nézan, E., Krock, B., & Bilien, G. (2014). Morphological and molecular characterization of three new Azadinium species (Amphidomataceae, Dinophyceae) from the Irminger Sea. Protist, 165, 417–444.CrossRefPubMedGoogle Scholar
  84. Tomas, R., & Cox, E. (1973). Observations on symbiosis of Peridinium balticum and its intracellular alga. 1. Ultrastructure. Journal of Phycology, 9, 304–323.Google Scholar
  85. Whitten, D. J., & Hoyhome, B. A. (1986). Comparative electrophoretic analysis of two binucleate dinoflagellates. Journal of Phycology, 22, 348–352.CrossRefGoogle Scholar
  86. Wisecaver, J. H., & Hackett, J. D. (2011). Dinoflagellate genome evolution. Annual Review of Microbiology, 65, 369–387.CrossRefPubMedGoogle Scholar
  87. Yamada, N., Sym, S. D., & Horiguchi, T. (2017). Identification of highly-divergent diatom derived chloroplasts in dinoflagellates, including a description of Durinskia kwazulunatalensis sp. nov. (Peridiniales, Dinophyceae). Molecular Biology and Evolution, 34, 1335–1351.CrossRefPubMedGoogle Scholar
  88. You, X. J., Luo, Z. H., Su, Y. P., Gu, L., & Gu, H. (2015). Peridiniopsis jiulongensis, a new freshwater dinoflagellate with a diatom endosymbiont from China. Nova Hedwigia, 101, 313–326.Google Scholar
  89. Zhang, Q., Liu, G.-X., & Hu, Z.-Y. (2011a). Durinskia baltica (Dinophyceae), a newly recorded species and genus from China, and its systematics. Journal of Systematics and Evolution, 49, 476–485.CrossRefGoogle Scholar
  90. Zhang, Q., Liu, G.-X., & Hu, Z.-Y. (2011b). Morphological differences and molecular phylogeny of freshwater blooming species, Peridiniopsis spp. (Dinophyceae) from China. European Journal of Protistology, 47, 149–160.CrossRefPubMedGoogle Scholar

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© Gesellschaft für Biologische Systematik 2017

Authors and Affiliations

  1. 1.Department Biologie, Systematische Botanik und Mykologie, GeoBio-CenterLudwig-Maximilians-Universität MünchenMunichGermany

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