Pelagodinium gen. nov. and P. béii comb. nov., a dinoflagellate symbiont of planktonic foraminifera

Protist

Volumn 161, Issue 3, 2010, Pages 385-399

  Siano, Raffaele ^a   Montresor, Marina ^b   Probert, Ian ^a   Not, Fabrice ^a   de Vargas, Colomban ^a  

^a STATION BIOLOGIQUE   (France)

^b STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

Author keywords

Dinoflagellates; Foraminifera; Orbulina universa; Pelagodinium; Suessiales; Symbionts

Indexed keywords

PROTOZOAL DNA; PROTOZOAL RNA; RIBOSOME DNA; RIBOSOME RNA; RNA, RIBOSOMAL, 26S;

ALVEOLATA; ARTICLE; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; FORAMINIFER; GENETICS; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; RNA GENE; SCANNING ELECTRON MICROSCOPY; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ALVEOLATA; CLUSTER ANALYSIS; DNA, PROTOZOAN; DNA, RIBOSOMAL; FORAMINIFERA; GENES, RRNA; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, PROTOZOAN; RNA, RIBOSOMAL; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

DINOPHYCEAE; FORAMINIFERA; GYMNODINIUM; GYMNODINIUM BEII; ORBULINA UNIVERSA; SUESSIALES;

EID: 77954864594     PISSN: 14344610     EISSN: 16180941     Source Type: Journal    
DOI: 10.1016/j.protis.2010.01.002     Document Type: Article

References (59)

1. Anderson R., Bé A.W.H. The ultrastructure of a planktonic foraminifer, Globigerinoides sacculifer (Brady), and its symbiotic dinoflagellates. J Foram Res 1976, 6:1-21.
2. Apprill A.M., Gates R.D. Recognizing diversity in coral symbiotic dinoflagellate communities. Mol Ecol 2007, 16:1127-1134.
3. Arnold A.J., Parker W.C. Biogeography of Planktonic Foraminifera. Modern Foraminifera 1999, 103-122. Kluwer Academic Publishers, London. B.K.S. Gupt (Ed.).
4. Banaszak A.T., Iglesias-Prieto R., Trench R.K. Scrippsiella velellae sp. nov. (Peridiniales) and Gloeodinium viscum sp. nov (Phytodiniales), dinoflagellate symbionts of 2 hydrozoans (Cnidaria). J Phycol 1993, 29:517-528.
5. Caron D. Symbiosis and Mixotrophy among Pelagic Microorganisms. Microbial Ecology of the Oceans 2000, 495-523. Wiley-Liss, Inc., New York. D.L. Kirchman (Ed.).
6. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552.
7. Coffroth M.A., Santos S.R. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 2005, 156:19-34.
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. de Vargas C., Norris R., Zaninetti L., Gibbs S.W., Pawlowski J. Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proc Natl Acad Sci USA 1999, 96:2864-2868.
10. de Vargas C., Bonzon M., Rees N.W., Pawlowski J., Zaninetti L. A molecular approach to biodiversity and biogeography in the planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Mar Micropaleontol 2002, 45:101-116.
11. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M., Claverie J.M., Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36:465-469.
12. Dodge J.D. Fine structure of the dinoflagellate Aureodinium pigmentosum gen. et sp. nov. Br Phycol Bull 1967, 3:327-336.
13. Farmer M.A., Fitt W.K., Trench R.K. Morphology of the symbiosis between Corculum cardissa (Mollusca: Bivalvia) and Symbiodinium corculorum (Dinophyceae). Biol Bull 2001, 200:336-343.
14. A Classification of Fossil and Living Dinoflagellates 1993, Micropaleontology Press, Special Paper, no.7. R.A. Fensome, F.J.R. Taylor, G. Norris, W.A.S. Sarjeant, D.I. Wharton, G.L. Williams (Eds.).
15. Freudenthal H.D. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov; a Zooxanthella: taxonomy, life cycle and morphology. J Protozool 1962, 9:45-52.
16. Gast R.J., Caron D.A. Molecular phylogeny of symbiotic dinoflagellates from planktonic foraminifera and radiolaria. Mol Biol Evol 1996, 13:1192-1197.
17. Gast R.J., Caron D.A. Photosymbiotic associations in planktonic foraminifera and radiolaria. Hydrobiologia 2001, 461:1-7.
18. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
19. Hackett J.D., Anderson D.M., Erdner D.L., Bhattacharya D. Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 2004, 91:1523-1534.
20. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999, 41:95-98.
21. Hansen G., Daugbjerg N. Symbiodinium natans sp nov.: a free-living dinoflagellate from Tenerife (northeast-Atlantic Ocean). J Phycol 2009, 45:251-263.
22. Hansen G., Daugbjerg N., Henriksen P. Baldinia anauniensis gen. et sp. nov.: a 'new' dinoflagellate from Lake Tovel, N. Italy. Phycologia 2006, 46:86-108.
23. Hemleben C., Spindler M. Recent advances in research on living planktonic foraminifera. Utrecht Micropaleontol Bull 1983, 30:141-170.
24. Hoegh-Guldberg O., Mumby P.J., Hooten A.J., Steneck R.S., Greenfield P., Gomez E., Harvell C.D., Sale P.F., Edwards A.J., Caldeira K., Knowlton N., Eakin C.M., Iglesias-Prieto R., Muthiga N., Bradbury R.H., Dubi A., Hatziolos M.E. Coral reefs under rapid climate change and ocean acidification. Science 2007, 318:1737-1742.
25. Höhfeld I., Melkonian M. Amphiesmal ultrastructure of dinoflagellates: a revaluation of pellicle formation. J Phycol 1992, 28:82-89.
26. Hunter R.L., LaJeunesse T.C., Santos S.R. Structure and evolution of the rDNA internal transcribed spacer (ITS) region 2 in the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 2007, 43:120-128.
27. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-3066.
28. Keller M.D., Selvin R.C., Claus W., Guillard R.R.L. Media for the culture of oceanic ultraphytoplankton. J Phycol 1987, 23:633-638.
29. Kremp A., Elbrächter M., Schweikert M., Wolny J.L., Gottschling M. Woloszynskia halophyla (Biecheler) comb. nov.: a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J Phycol 2005, 41:629-643.
30. LaJeunesse T.C. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a species level marker. J Phycol 2001, 37:866-880.
31. LaJeunesse T.C., Lambert G., Andersen R.A., Coffroth M.A., Galbraith D.W. Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J Phycol 2005, 41:880-886.
32. Lee J.J. Nutrition and Physiology of the Foraminifera. Biochemistry and Physiology of Protozoa 1980, 43-66. Academic Press, Inc., London, New York. M. Levandowsky, S.H. Hunter (Eds.).
33. Leggat W., Marendy E.M., Baillie B., Whitney S.M., Ludwig M., Badger M.R., Yellowlees D. Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 2002, 29:309-322.
34. Lindberg K., Moestrup Ø, Daugbjerg N. Studies on woloszynskioid dinoflagellates I: Woloszynskia coronata re-examined using light and electron microscopy and partial LSU rDNA sequences, with description of Tovellia gen. nov. and Jadwigia gen. nov. (Tovelliaceae fam. nov.). Phycologia 2005, 44:416-440.
35. Loeblich A.R. The amphiesma or dinoflagellate cell covering. Proc North American Paleontol Convention II 1969, 867-929.
36. Loeblich A.R., Sherley J.L. Observations on the theca of the motile phase of free-living and symbiotic isolates of Zooxanthella microadriatica (Freudenthal) comb. nov. J Mar Biol Assoc UK 1979, 59:195-205.
37. Lopes R.M., Silveira M. Symbiosis between a pelagic flatworm and a dinoflagellate from a tropical area-structural observations. Hydrobiologia 1994, 287:277-284.
38. Manning M.M., Gates R.D. Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 2008, 53:1853-1861.
39. 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, Taylor and Francis Group, Boca Raton, FL. J. Brodie, J. Lewis (Eds.).
40. Moestrup Ø, Hansen G., Daugbjerg N. Studies on woloszynskioid dinoflagellates III: on the ultrastructure and phylogeny of Borghiella dodgei gen. et sp. nov., a cold-water species from Lake Tovel, N. Italy, and on B. tenuissima comb. Nov. (syn. Woloszynskia tenuissima). Phycologia 2008, 47:54-78.
41. Moestrup Ø, Lindberg K., Daugbjerg N. Studies on woloszynskioid dinoflagellates IV: The genus Biecheleria gen. nov. Phycol Res 2009, 57:203-220.
42. Moestrup Ø, Lindberg K., Daugbjerg N. Studies on woloszynskioid dinoflagellates V. Ultrastructure of Biecheleriopsis gen. nov., with description of Biecheleriopsis adriatica sp. nov. Phycol Res 2009, 57:221-237.
43. Moestrup Ø, Hansen G., Daugbjerg N., Flaim G., D'Andrea M. Studies on woloszynskioid dinoflagellates II: On Tovellia sanguinea sp. nov., the dinoflagellate responsible for the reddening of Lake Tovel. N. Italy. Eur J Phycol 2006, 41:47-65.
44. Montresor M., Procaccini G., Stoecker D.K. Polarella glacialis gen. nov., sp. nov. (Dinophyceae): Suessiaceae are still alive!. J Phycol 1999, 35:186-197.
45. Morard R., Quillevere F., Escarguel G., Ujiie Y., de Garidel-Thoron T., Norris R.D., de Vargas C. Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa. Mar Micropaleontol 2009, 71:148-165.
46. Schonberg C.H.L., Loh W.K.W. Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis. Mar Ecol Prog Ser 2005, 299:157-166.
47. Shaked Y., de Vargas C. Pelagic photosymbiosis: rDNA assessment of diversity and evolution of dinoflagellate symbionts and planktonic foraminiferal hosts. Mar Ecol Prog Ser 2006, 325:59-71.
48. Siano R., WHCF Kooistra, Montresor M., Zingone A. Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia 2009, 48:44-65.
49. Spero H.J. Symbiosis in the planktonic foraminifer, Orbulina universa, and the isolation of its symbiotic dinoflagellate Gymnodinium béii sp. nov. J Phycol 1987, 23:307-317.
50. Spindler M., Hemleben C.I.E. Symbionts in Planktonic Foraminifera (Protozoa). Endosymbiosis and Cell Biology 1980, 133-140. Walter de Gruyter & Co., Berlin-New York. W. Schwemmler, H.E.A. Schenk (Eds.).
51. Stat M., Morris E., Gates R.D. Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 2008, 105:9256-9261.
52. Stoecker D.K., Johnson M.D., de Vargas C., Not F. Acquired phototrophy in aquatic protists. Aquat Microb Ecol 2009, 57:279-310.
53. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
54. Tchernov D., Gorbunov M.Y., de Vargas C., Narayan Yadav S., Milligan A.J., Haggblom M., Falkowski P.G. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 2004, 101:13531-13535.
55. Thompson R.H. A new genus and new records of fresh-water Pyrrophyta in the Desmokontae and Dinophyceae. Lloydia 1951, 13:277-299.
56. Trench R.K. Microalgal-invertebrate symbioses - A review. Endocyt Cell Research 1993, 9:135-175.
57. Trench R.K., Blank R.J. Symbiodinium microadriaticum Freudenthal; S. goreauii sp. nov; S. kawagutii sp. nov. and S. pilosum sp. nov.: gymnodinioid dinoflagellate symbionts of marine invertebrates. J Phycol 1987, 23:469-481.
58. Trench R.K., Thinh L.V. Gymnodinium linucheae sp. nov.: the dinoflagellate symbiont of the jellyfish Linuche unguiculata. Eur J Phycol 1995, 30:149-154.
59. van Oppen M.J.H. Perspective: hidden diversity in coral endosymbionts unveiled. Mol Ecol 2007, 16:1125-1126.