New home for tiny symbionts: Dinophytes determined as Zooxanthella are Peridiniales and distantly related to Symbiodinium

Molecular Phylogenetics and Evolution

Volumn 67, Issue 1, 2013, Pages 217-222

  Gottschling, Marc ^a   McLean, Timothy I ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b University of Southern Mississippi   (United States)

Author keywords

Dinoflagellates; ITS; LSU; Molecular systematics; SSU; Zooxanthellae

Indexed keywords

PROTOZOAL DNA;

ANIMAL; ANTHOZOA; ARTICLE; BAYES THEOREM; CLASSIFICATION; CLUSTER ANALYSIS; DINOFLAGELLATE; DNA SEQUENCE; GENETICS; PHYLOGENY; PHYSIOLOGY; SEQUENCE ALIGNMENT; STATISTICAL MODEL; SYMBIOSIS;

ANIMALS; ANTHOZOA; BAYES THEOREM; CLUSTER ANALYSIS; DINOFLAGELLIDA; DNA, PROTOZOAN; LIKELIHOOD FUNCTIONS; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

ANTHOZOA; BACILLARIOPHYTA; DINOPHYCEAE; PERIDINIALES; RADIOLARIA (PROTOZOANS); SUESSIALES; SYMBIODINIUM; ZOOXANTHELLA NUTRICULA;

EID: 84875056143     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2013.01.003     Document Type: Article

References (59)

1. Anderson O.R. Ultrastructure of a colonial radiolarian Collozoum inerme and a cytochemical determination of role of its zooxanthellae. Tissue Cell 1976, 8:195-208.
2. Anderson, D.M., 1989. Toxic algal blooms and red tides: A global perspective. In: Okaichi, T., Anderson, D.M., Nemoto, T. (Eds.), Red Tides: Biology, Environmental Science and Toxicology. Elsevier, pp. 11-16.
3. Annenkova N.V., Lavrov D.V., Belikov S.I. Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 2011, 162:222-236.
4. Brandt K.A.H. über das Zusammenleben von Thieren und Algen. Verh. Physiol. Ges. Berlin 1881, 1881:570-574.
5. Bråte J., Krabberød A.K., Dolven J.K., Ose R.F., Kristensen T., Bjørklund K.R., Shalchian-Tabrizi K. Radiolaria associated with large diversity of marine alveolates. Protist 2012, 163:767-777.
6. Chatton, é., Grassé, P.-P., 1952. Classe des dinoflagelles ou péridiniens. In: Grassé, P.-P. (Ed.), Phylogénie. Protozoaires: Généralités. Flagellés. Masson, Paris, pp. 309-406.
7. Craveiro S.C., Calado A.J., Daugbjerg N., Moestrup Ø. Ultrastructure and LSU rDNA-based revision of Peridinium group Palatinum (Dinophyceae) with the description of Palatinus gen. nov. J. Phycol. 2009, 45:1175-1194.
8. Daugbjerg N., Hansen G., Larsen J., Moestrup Ø. 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 2000, 39:302-317.
9. Decelle, J., Siano, R., Probert, I., Poirier, C., Not, F., in press. Multiple microalgal partners in symbiosis with the acantharian Acanthochiasma sp. (Radiolaria). Symbiosis. doi:10.1007/s13199-012-0195-x.
10. Deflandre G. Micropaléontologie - Calciodinellum nov. gen., premier repésentant d'une famille nouvelle de dinoflagellés à thèque calcaire. Compt. Rend. Hebd. Séances Acad. Sci. 1947, 224:1781-1782.
11. Dolven J.K., Lindqvist C., Albert V.A., Bjorklund K.R., Yuasa T., Takahashi O., Mayama S. Molecular diversity of alveolates associated with neritic North Atlantic radiolarians. Protist 2007, 158:65-76.
12. Fensome R.A., Taylor F.J.R., Norris G., Sarjeant W.A.S., Wharton D.I., Williams G.L. A classification of living and fossil dinoflagellates. Micropaleontol. Special Publ. 1993, 7:1-245.
13. Freudenthal H.D. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a Zooxanthella: Taxonomy, life cycle, and morphology. J. Protozool. 1962, 9:45-52.
14. Gast R.J., Caron D.A. Molecular phylogeny of symbiotic dinoflagellates from planktonic Foraminifera and Radiolaria. Mol. Biol. Evol. 1996, 13:1192-1197.
15. Gast R.J. Molecular phylogeny of a potentially parasitic dinoflagellate isolated from the solitary radiolarian, Thalassicolla nucleata. J. Eukaryot. Microbiol. 2006, 53:43-45.
16. Gemeinhardt, K., Schiller, J., 1930. Rabenhorst's Kryptogamen-Flora. Zweite Auflage. Band 10, Abt. 2. Alt. t.p.: Silicoflagellatae. Coccolithineae, Leipzig.
17. Gordon B.R., Leggat W. Symbiodinium-Invertebrate symbioses and the role of metabolomics. Mar. Drugs 2010, 8:2546-2568.
18. Gottschling M., Plötner J. Secondary structure models of the nuclear Internal Transcribed Spacer regions and 5.8S rRNA in Calciodinelloideae (Peridiniaceae) and other dinoflagellates. Nucl. Acids Res. 2004, 32:307-315.
19. Gottschling M., Keupp H., Plötner J., Knop R., Willems H., Kirsch M. Phylogeny of calcareous dinoflagellates as inferred from ITS and ribosomal sequence data. Mol. Phylogenet. Evol. 2005, 36:444-455.
20. Gottschling M., Söhner S., Zinßmeister C., John U., Plötner J., Schweikert M., Aligizaki K., Elbrächter M. Delimitation of the Thoracosphaeraceae (Dinophyceae), including the calcareous dinoflagellates, based on large amounts of ribosomal RNA sequence data. Protist 2012, 163:15-24.
21. Gribble K.E., Anderson D.M. Molecular phylogeny of the heterotrophic dinoflagellates, Protoperidinium, Diplopsalis and Preperidinium (Dinophyceae), inferred from large subunit rDNA. J. Phycol. 2006, 42:1081-1095.
22. Hallegraeff G.M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 2010, 46:220-235.
23. Hansen G., Daugbjerg N., Henriksen P. Baldinia anauniensis gen. et sp nov.: a 'new' dinotlagellate from Lake Tovel. N. Italy. Phycologia 2007, 46:86-108.
24. Hill M., Allenby A., Ramsby B., Schoenberg C., Hill A. Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: Evidence of heteroplasmy and putative host-specific symbiont lineages. Mol. Phylogenet. Evol. 2011, 59:81-88.
25. Hillis D.M., Dixon M.T. Ribosomal DNA: molecular evolution and phylogenetic inference. Q. Rev. Biol. 1991, 66:411-453.
26. Hoppenrath M., Leander B.S. Dinoflagellate phylogeny as inferred from Heat Shock Protein 90 and ribosomal gene sequences. Plos One 2010, 5:e13220.
27. Horiguchi T., Pienaar R.N. Ultrastructure of a new marine sand-dwelling dinoflagellate, Gymnodinium quadrilobatum sp. nov. (Dinophyceae) with special reference to its endosymbiotic alga. Eur. J. Phycol. 1994, 29:237-245.
28. Horiguchi T., Takano Y. Serial replacement of a diatom endosymbiont in the marine dinoflagellate Peridinium quinquecorne (Peridiniales, Dinophyceae). Phycol. Res. 2006, 54:193-200.
29. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
30. Imanian B., Pombert J.-F., Keeling P.J. The complete plastid genomes of the two 'dinotoms' Durinskia baltica and Kryptoperidinium foliaceum. Plos One 2011, 5:e10711.
31. Ishitani Y., Ujiie Y., de Vargas C., Not F., Takahashi K. Phylogenetic relationships and evolutionary patterns of the order Collodaria (Radiolaria). Plos One 2012, 7:e35775.
32. Katoh K., Kuma K., Toh H., Miyata T. MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucl. Acids Res. 2005, 33:511-518.
33. Klebs G.A. Flagellatenstudien. Z. Wiss. Zool. 1892, 5:265-445.
34. Knowlton N., Rohwer F. Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am. Nat. Suppl. 2003, 162:S51-S62.
35. Kremp A., Elbrächter M., Schweikert M., Wolny J.L., Gottschling M. Woloszynskia halophila (Biecheler) comb. nov.: a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J. Phycol. 2005, 41:629-642.
36. LaJeunesse T.C., Thornhill D.J. Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. Plos One 2011, 6:e29013.
37. Logares R., Shalchian-Tabrizi K., Boltovskoy A., Rengefors K. Extensive dinoflagellate phylogenies indicate infrequent marine-freshwater transitions. Mol. Phylogenet. Evol. 2007, 45:887-903.
38. Moestrup Ø., Daugbjerg N. On dinoflagellate phylogeny and classification. Unravelling the Algae, the Past, Present, and Future of Algal Systematics 2007, 215-230. CRC Press, Boca Raton. J. Brodie, J. Lewis (Eds.).
39. Orr R.J.S., Murray S.A., Stüken A., Rhodes L., Jakobsen K.S. When naked became armored: an eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS One 2012, 7:e50004.
40. Pace N.R. Mapping the tree of life: progress and prospects. Microbiol. Mol. Biol. R. 2009, 73:565-576.
41. Pfiester L.A., Anderson D.M. Dinoflagellate reproduction. The Biology of Dinoflagellates 1987, 611-648. Blackwell, Oxford. F.J.R.M. Taylor (Ed.).
42. Pochon X., Montoya-Burgos J.I., Stadelmann B., Pawlowski J. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol. Phylogenet. Evol. 2006, 38:20-30.
43. Saldarriaga J.F., Taylor F.J.R.M., Cavalier-Smith T., Menden-Deuerd S., Keeling P.J. Molecular data and the evolutionary history of dinoflagellates. Eur. J. Protistol. 2004, 40:85-111.
44. Siano R., Montresor M., Probert I., Not F., de Vargas C. Pelagodinium gen. nov and P. béii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist 2010, 161:385-399.
45. Smayda T.J., Reynolds C.S. Strategies of marine dinoflagellate survival and some rules of assembly. J. Sea Res. 2003, 49:95-106.
46. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
47. Stat M., Morris E., Gates R.D. Functional diversity in coral-dinoflagellate symbiosis. Proc. Natl Acad. Sci. USA 2008, 105:9256-9261.
48. Steidinger, K.A., Tangen, K., 1996. 3. Dinoflagellates. In: Tomas, C.R. (Ed.), Identifying Marine Diatoms and Dinoflagellates. Academic Press, San Diego (California), pp. 387-583.
49. Tamura M., Shimada S., Horiguchi T. Galeidiniium rugatum gen. et sp. nov. (Dinophyceae), a new coccoid dinoflagellate with a diatom endosymbiont. J. Phycol. 2005, 41:658-671.
50. Taylor F.J.R., Hoppenrath M., Saldarriaga J.F. Dinoflagellate diversity and distribution. Biodivers. Conserv. 2008, 17:407-418.
51. Tillmann U., Elbrächter M., Krock B., John U., Cembella A. Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. Eur. J. Phycol. 2009, 44:63-79.
52. Tillmann U., Salas R., Gottschling M., Krock B., O'Driscol D., Elbrächter M. Amphidoma languida sp. nov. (Dinophyceae) reveals a close relationship between Amphidoma and Azadinium. Protist 2012, 163:701-719.
53. Trench R.K. Dinoflagellates in non-parasitic symbioses. The Biology of Dinoflagellates 1987, 530-571. Blackwell, Oxford. F.J.R.M. Taylor (Ed.).
54. von Stosch H.A. Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates, Gymnodinium pseudopalustre Schiller and Woloszynskia apiculata sp. nov. Br. Phycol. J. 1973, 8:105-134.
55. Wiens J.J., Morrill M.C. Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Syst. Biol. 2011, 60:719-731.
56. Yamaguchi A., Kawamura H., Horiguchi T. A further phylogenetic study of the heterotrophic dinoflagellate genus, Protoperidinium (Dinophyceae) based on small and large subunit ribosomal RNA gene sequences. Phycol. Res. 2006, 54:317-329.
57. Zhang H., Bhattacharya D., Lin S. A three-gene dinoflagellate phylogeny suggests monophyly of Prorocentrales and a basal position for Amphidinium and Heterocapsa. J. Mol. Evol. 2007, 65:463-474.
58. Zhang Q., Liu G.X., Hu Z.Y. Durinskia baltica (Dinophyceae), a newly recorded species and genus from China, and its systematics. J. Syst. Evol. 2011, 49:476-485.
59. Zinßmeister C., Söhner S., Facher E., Kirsch M., Meier K.J.S., Gottschling M. Catch me if you can: the taxonomic identity of Scrippsiella trochoidea (F.Stein) A.R.Loebl. (Thoracosphaeraceae, Dinophyceae). Syst. Biodivers. 2011, 9:145-157.