Multiple microalgal partners in symbiosis with the acantharian Acanthochiasma sp. (Radiolaria)

Symbiosis

Volumn 58, Issue 1-3, 2012, Pages 233-244

  Decelle, Johan ^a,b   Siano, Raffaele ^c   Probert, Ian ^a   Poirier, Camille ^a,b   Not, Fabrice ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c IFREMER   (France)

Author keywords

Acantharia; Microalgae; Photosymbiosis; Plankton; Protists; Radiolaria

Indexed keywords

DINOFLAGELLATE; ENDOSYMBIONT; FORAMINIFERA; HETEROTROPHY; MARINE ECOSYSTEM; MICROALGA; NINETEENTH CENTURY; RADIOLARIA; SYMBIOSIS;

EID: 84872260338     PISSN: 03345114     EISSN: 18787665     Source Type: Journal    
DOI: 10.1007/s13199-012-0195-x     Document Type: Conference Paper

References (58)

1. Anderson OR (1983) Radiolaria. Springer, New York
2. Annenkova NV, Lavrov DV, Belikov SI (2011) Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 162:22-236
3. Baker AC, Romanski AM (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: Comment on Goulet (2006). Marine Ecology Progress Series 335:237-242
4. Brandt K (1881) Über das Zusammenleben von Algen und Tieren, Biologisches Zentrallblatt 1:524-527
5. Bråt J et al (2012) Radiolaria associated with large diversity of marine alveolates. Protist 163:767-777
6. Carlos AA, Baillie BK, Maruyama T (2000) Diversity of dinoflagellate symbionts (Zooxanthellae) in a host individual. Marine Ecology Progress Series 195:93-100
7. Cienkowski L (1871) Über Schwarmer-Bildung bei Radiolarien. Archiv für Mikroskopische Anatomie 7:372-381
8. Coleman AW (2007) Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Research 35:3322-3329
9. de Bary AH (1878) Vortrag: Uber Symbiose. Tagblatt der 51. Versammlung Deutscher Naturforscher und Aerzte in Cassel. Baier & Lewalter, Kassel, pp. 121-126.
10. Decelle J et al (2012a) An original mode of symbiosis in open ocean plankton. PNAS. Early edition 15 oct. doi: 10.1073/pnas.1212303109
11. Decelle J, Suzuki N, Mahé F, de Vargas C, Not F (2012b) Molecular phylogeny and morphological evolution of the Acantharia (Radiolaria). Protist 163:435-450
12. Douglas AE (1998) Evolution of mutualistic symbiosis without vertical transmission in symbiosis. Heredity 81:599-603
13. Douglas AE, Smith DC (1989) Are endosymbioses mutualistic? TREE 4:350-352
14. Edvardsen B, Imai I (2006) The ecology of harmful flagellates within Prymnesiophyceae and Raphidophyceae. In: Granéli E, Turner JT (eds) Ecology of harmful algae, ecological studies, Vol. 189. Springer, Berlin, pp 67-79
15. Edvardsen B et al (2011) Ribosomal DNA phylogenies and a morphological revision provide the basis for a revised taxonomy of the Prymnesiales (Haptophyta). European Journal of Phycology 46:202-228
16. Faber WW Jr, Anderson OR, Lindsey JL, Caron DA (1988) Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis: I. Occurrence and stability of two mutually exclusive chrysophyte endosymbionts and their ultrastructure. Journal of Foraminiferal Research 18:334-343
17. Febvre J, Febvre-Chevalier C (1979) Ultrastructural study of zooxanthellae of three species of Acantharia (Protozoa: Actinopoda), with details of their taxonomic position in the prymnesiales (prymnesiophyceae, Hibberd, 1976). Journal of Marine Biological Association UK 59:215-226
18. Foster RA, Collier JL, Carpenter EJ (2006a) Reverse transcription PCR amplification of cyanobacterial symbiont 16S rRNA sequences from single non-photosynthetic eukaryotic marine planktonic host cells. Journal of Phycology 42:243-250
19. Foster RA, Carpenter EJ, Bergman B (2006b) Unicellular cyanobionts in open ocean dinoflagellates, radiolarians, and tintinnids: ultrastructural characterization and immuno-localization of phycoerythrin and nitrogenase. Journal of Phycology 42:453-463
20. Franck SA (1996) Host symbiont conflict over the mixing of symbiotic lineages. Proceedings of the Royal Society of London - Series B: Biological Sciences 263:339-344
21. Gast RJ, Caron DA (1996) Molecular phylogeny of symbiotic dinoflagellates from planktonic foraminifera and radiolaria. Molecular and Biological Evolution 13:1192-1197
22. Gast RJ, Caron DA (2001) Photosymbiotic associations in planktonic foraminifera and radiolaria. Hydrobiologia 461:1-7
23. Gast RJ, McDonnell TA, Caron DA (2000) srDNA-based taxonomic affinities of algal symbionts from a planktonic foraminifer and a solitary radiolarian. Journal of Phycology 36:172-177
24. Gottschling M et al (2005) A molecular phylogeny of Scrippsiella sensu lato (Calciodinellaceae, Dinophyta) with interpretations on morphology and distribution. European Journal of Phycology 40:207-220
25. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular and Biological Evolution 27(2):221-224
26. Guillou L et al (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to syndiniales (Alveolata). Environmental Microbiology 10:3349-3365
27. Haeckel E (1888) Die Radiolarien (Rhizopoda Radiolaria). Eine Monographie, Dritter Teil, Die Acantharien oder Actinopyleen-Radiolarien. Verlag von Georg Reimer, Berlin, p 33
28. Hollande A, Carré D (1974) Les xanthelles des radiolaires sphaerocollides, des acanthaires et de Velella velella: infrastructure - cytochimie - taxonomie. Protistologica 4:573-601
29. Jeong HJ, Yoon JY, Kim JS, Yoo YD, Seong KA (2002) Growth and grazing rates of the prostomatid ciliate Tiarina fusus on red-tide and toxic algae. Aquatic Microbial Ecology 28:289-297
30. Kamiyama T (2000) Application of a vital staining method to measure feeding rates of field ciliate assemblages on a harmful alga. Marine Ecology Progress Series 197:299-303
31. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. Journal of Phycology 23:633-638
32. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a "species" level marker. Journal of Phycology 37:866-880
33. Lee JJ, Correia M (2005) Endosymbiotic diatoms from previously unsampled habitats. Symbiosis 38:251-260
34. Litaker RW et al (2002) Seasonal niche strategy of the bloom-forming dinoflagellate Heterocapsa triquetra. Marine Ecology Progress Series 232:45-62
35. Liu H et al (2009) Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. PNAS 106:12803-12808
36. Lundgren V, Granéli E (2011) Influence of altered light conditions and grazers on Scrippsiella trochoidea (Dinophyceae) cyst formation. Aquatic Microbial Ecology 63:231-243
37. McDonald SM, Sarno D, Scanlan DJ, Zingone A (2007) Genetic diversity of eukaryotic ultraphytoplankton in the Gulf of Naples during an annual cycle. Aquatic Microbial Ecology 50:75-89
38. Michaels AF (1988) Vertical distribution and abundance of Acantharia and their symbionts. Marine Biology 97:559-569
39. Michaels AF, Caron DA, Swanberg NR, Howse FA, Michaels CM (1995) Planktonic sarcodines (acantharia, radiolaria, foraminifera) in surface waters near Bermuda - abundance, biomass and vertical flux. Journal of Plankton Research 17:131-163
40. Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light- and shade- adapted colonies of the symbiotic coral Stylophora pistillata. Proceedings of the Royal Society of London - Series B: Biological Sciences 222:181-202
41. Pawlowski J et al (2012) CBOL Protist Working Group: Barcoding eukaryotic richness beyond the animal, plant and fungal kingdoms. PLos Biology. In press.
42. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Molecular Phylogenetics and Evolution 38:20-30
43. Saldarriaga JF, Taylor FJR, Cavalier-Smith T, Menden-Deuer S, Keeling PJ (2004) Molecular data and the evolutionary history of dinoflagellates. European Journal of Protistology 40:85-111
44. Schewiakoff WT (1926) The Acantharia. Fauna e Flora del Golfo di Napoli 37:1-755
45. Shaked Y, de Vargas C (2006) Pelagic photosymbiosis: rDNA assessment of diversity and evolution of dinoflagellate symbionts and planktonic foraminiferal hosts. Marine Ecology Progress Series 325:59-71
46. Siano R, Montresor M, Probert I, Not F, de Vargas C (2010) Pelagodinium gen. nov and P-béii comb. nov., a dinoflagellate symbiont of planktonic Foraminifera. Protist 161:385-399
47. Siano R et al (2011) Distribution and host diversity of Amoebophryidae parasites across oligotrophic waters of the Mediterranean Sea. Biogeosciences 8:267-268
48. Spero HJ (1987) Symbiosis in the planktonic foraminifer, Orbulina universa, and the isolation of its symbiotic dinoflagellate, Gymnodinium béii sp. nov. Journal of Phycology 23:307-317
49. Stern R et al (2012) The ribosomal internal transcribed spacer (ITS) as a candidate dinoflagellate barcode marker. PLoS One 7(8):e42780. doi: 10.1371/journal.pone.0042780
50. Stoecker DK, Gustafson DE, Verity PG (1996) Micro- and mesoprotozooplankton at 140 W in the equatorial Pacific: heterotrophs and micotrophs. Aquatic Microbial Ecology 10:273-282
51. Stoecker DK, Johnson MD, de Vargas C, Not F (2009) Acquired phototrophy in aquatic protists. Aquatic Microbial Ecology 57:279-310
52. Swanberg NR, Caron DA (1991) Patterns of feeding in epipelagic oceanic plankton. Journal of Plankton Research 13:287-312
53. Tamura K et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular and Biological Evolution 28:2731-2739
54. Tillman U, Elbrächter M, Krock B, John U, Cembella A (2009) Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. European Journal of Phycology 44:63-79
55. Wooldridge SA (2010) Is the coral-algae symbiosis really "mutually beneficial" for the partners? Bioessays 32:615-625
56. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrates hosts. Plant, Cell & Environment 31:679-694
57. Yuasa T, Horiguchi T, Mayama S, Matsuoka A, Takahashi O (2012) Ultrastructural and molecular characterization of cyanobacterial symbionts in Dictyocoryne profunda (polycystine radiolaria). Symbiosis. doi: 10.1007/s13199-012-0174-2
58. Zwirglmaier K et al (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environmental Microbiology 10(1):147-161