Advertisement

Symbiosis

, Volume 58, Issue 1–3, pp 233–244 | Cite as

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

  • Johan DecelleEmail author
  • Raffaele Siano
  • Ian Probert
  • Camille Poirier
  • Fabrice Not
Article

Abstract

Acantharia (Radiolaria) are widespread and abundant heterotrophic marine protists, some of which can host endosymbiotic eukaryotic microalgae. Although this photosymbiotic association was first described at the end of the 19th century, the diversity of the symbiotic microalgae remains poorly characterized. Here, we examined the identity of the microalgae associated with the acantharian species Acanthochiasma sp. by sequencing partial 18S and internal transcribed spacer (ITS) ribosomal DNA genes from cultured symbionts and directly from isolated holobiont specimens. Single Acanthochiasma cells contained multiple symbiotic partners, including distantly related dinoflagellates (Heterocapsa sp., Pelagodinium sp., Azadinium sp. and Scrippsiella sp.) as well as a haptophyte (Chrysochromulina sp.). This original association of multiple symbiotic microalgae within a single host cell raises questions about the specificity and functioning of the relationship. These microalgae exhibit the common ecological feature of being abundant and widely distributed in coastal and oceanic waters, some occasionally forming extensive blooms. Some of the microalgal genera found in association with Acanthochiasma (i.e. Pelagodinium and Chrysochromulina) are known to occur in symbiosis with other heterotrophic protists such as Foraminifera and other Radiolaria, whereas Heterocapsa, Scrippsiella and Azadinium have never previously been reported to be involved in putative symbiotic relationships. The unusual association unveiled in this study contributes to our understanding of the ecological and evolutionary significance of photosymbiosis in Acantharia and also provides new insights into the nature of such partnerships in the planktonic realm.

Keywords

Photosymbiosis Radiolaria Acantharia Protists Microalgae Plankton 

Notes

Acknowledgments

We thank the Laboratoire d’Océanographie de Villefranche-sur-Mer (LOV) for providing sampling facilities and Morgan Perennou and Gwen Tanguy from the GENOMER platform at the Station Biologique de Roscoff. This project was supported by the network “Bibliothèque du Vivant” funded by the CNRS, the Muséum National d’Histoire Naturelle, the INRA and the CEA (Centre National de Séquençage). This research was supported by the Region Bretagne (DIPHOPE 044763), the JST-CNRS program, and the EU FP7 I3 project ASSEMBLE and KBBE project MACUMBA.

Supplementary material

13199_2012_195_MOESM1_ESM.pdf (504 kb)
Supplementary Material (PDF 503 kb)

References

  1. Anderson OR (1983) Radiolaria. Springer, New YorkCrossRefGoogle Scholar
  2. Annenkova NV, Lavrov DV, Belikov SI (2011) Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 162:22–236CrossRefGoogle Scholar
  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 335:237–242CrossRefGoogle Scholar
  4. Brandt K (1881) Über das Zusammenleben von Algen und Tieren, Biologisches Zentrallblatt 1:524-527Google Scholar
  5. Bråt J et al (2012) Radiolaria associated with large diversity of marine alveolates. Protist 163:767–777CrossRefGoogle Scholar
  6. Carlos AA, Baillie BK, Maruyama T (2000) Diversity of dinoflagellate symbionts (Zooxanthellae) in a host individual. Marine Ecology Progress Series 195:93–100CrossRefGoogle Scholar
  7. Cienkowski L (1871) Über Schwarmer-Bildung bei Radiolarien. Archiv für Mikroskopische Anatomie 7:372–381CrossRefGoogle Scholar
  8. Coleman AW (2007) Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Research 35:3322–3329PubMedCrossRefGoogle Scholar
  9. de Bary AH (1878) Vortrag: Uber Symbiose. Tagblatt der 51. Versammlung Deutscher Naturforscher und Aerzte in Cassel. Baier & Lewalter, Kassel, pp. 121–126.Google Scholar
  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 163:435–450PubMedCrossRefGoogle Scholar
  12. Douglas AE (1998) Evolution of mutualistic symbiosis without vertical transmission in symbiosis. Heredity 81:599–603CrossRefGoogle Scholar
  13. Douglas AE, Smith DC (1989) Are endosymbioses mutualistic? TREE 4:350–352PubMedGoogle Scholar
  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 67–79CrossRefGoogle Scholar
  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 46:202–228CrossRefGoogle Scholar
  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 18:334–343CrossRefGoogle Scholar
  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 59:215–226CrossRefGoogle Scholar
  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 42:243–250CrossRefGoogle Scholar
  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 42:453–463CrossRefGoogle Scholar
  20. Franck SA (1996) Host symbiont conflict over the mixing of symbiotic lineages. Proceedings of the Royal Society of London - Series B: Biological Sciences 263:339–344CrossRefGoogle Scholar
  21. Gast RJ, Caron DA (1996) Molecular phylogeny of symbiotic dinoflagellates from planktonic foraminifera and radiolaria. Molecular and Biological Evolution 13:1192–1197CrossRefGoogle Scholar
  22. Gast RJ, Caron DA (2001) Photosymbiotic associations in planktonic foraminifera and radiolaria. Hydrobiologia 461:1–7CrossRefGoogle Scholar
  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 36:172–177CrossRefGoogle Scholar
  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 40:207–220CrossRefGoogle Scholar
  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):221–224CrossRefGoogle Scholar
  26. Guillou L et al (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to syndiniales (Alveolata). Environmental Microbiology 10:3349–3365PubMedCrossRefGoogle Scholar
  27. Haeckel E (1888) Die Radiolarien (Rhizopoda Radiolaria). Eine Monographie, Dritter Teil, Die Acantharien oder Actinopyleen-Radiolarien. Verlag von Georg Reimer, Berlin, p 33Google Scholar
  28. Hollande A, Carré D (1974) Les xanthelles des radiolaires sphaerocollides, des acanthaires et de Velella velella: infrastructure—cytochimie—taxonomie. Protistologica 4:573–601Google Scholar
  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 28:289–297CrossRefGoogle Scholar
  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 197:299–303CrossRefGoogle Scholar
  31. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. Journal of Phycology 23:633–638CrossRefGoogle Scholar
  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 37:866–880CrossRefGoogle Scholar
  33. Lee JJ, Correia M (2005) Endosymbiotic diatoms from previously unsampled habitats. Symbiosis 38:251–260Google Scholar
  34. Litaker RW et al (2002) Seasonal niche strategy of the bloom-forming dinoflagellate Heterocapsa triquetra. Marine Ecology Progress Series 232:45–62CrossRefGoogle Scholar
  35. Liu H et al (2009) Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. PNAS 106:12803–12808PubMedCrossRefGoogle Scholar
  36. Lundgren V, Granéli E (2011) Influence of altered light conditions and grazers on Scrippsiella trochoidea (Dinophyceae) cyst formation. Aquatic Microbial Ecology 63:231–243CrossRefGoogle Scholar
  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 50:75–89CrossRefGoogle Scholar
  38. Michaels AF (1988) Vertical distribution and abundance of Acantharia and their symbionts. Marine Biology 97:559–569CrossRefGoogle Scholar
  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 17:131–163CrossRefGoogle Scholar
  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 222:181–202CrossRefGoogle Scholar
  41. Pawlowski J et al (2012) CBOL Protist Working Group: Barcoding eukaryotic richness beyond the animal, plant and fungal kingdoms. PLos Biology. In press.Google Scholar
  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 38:20–30PubMedCrossRefGoogle Scholar
  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 40:85–111CrossRefGoogle Scholar
  44. Schewiakoff WT (1926) The Acantharia. Fauna e Flora del Golfo di Napoli 37:1–755Google Scholar
  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 325:59–71CrossRefGoogle Scholar
  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 161:385–399PubMedCrossRefGoogle Scholar
  47. Siano R et al (2011) Distribution and host diversity of Amoebophryidae parasites across oligotrophic waters of the Mediterranean Sea. Biogeosciences 8:267–268CrossRefGoogle Scholar
  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 23:307–317CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  50. Stoecker DK, Gustafson DE, Verity PG (1996) Micro- and mesoprotozooplankton at 140°W in the equatorial Pacific: heterotrophs and micotrophs. Aquatic Microbial Ecology 10:273–282CrossRefGoogle Scholar
  51. Stoecker DK, Johnson MD, de Vargas C, Not F (2009) Acquired phototrophy in aquatic protists. Aquatic Microbial Ecology 57:279–310Google Scholar
  52. Swanberg NR, Caron DA (1991) Patterns of feeding in epipelagic oceanic plankton. Journal of Plankton Research 13:287–312CrossRefGoogle Scholar
  53. Tamura K et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular and Biological Evolution 28:2731–2739CrossRefGoogle Scholar
  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 44:63–79CrossRefGoogle Scholar
  55. Wooldridge SA (2010) Is the coral-algae symbiosis really “mutually beneficial” for the partners? Bioessays 32:615–625PubMedCrossRefGoogle Scholar
  56. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrates hosts. Plant, Cell & Environment 31:679–694CrossRefGoogle Scholar
  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):147–161PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Johan Decelle
    • 1
    • 2
    Email author
  • Raffaele Siano
    • 3
  • Ian Probert
    • 4
  • Camille Poirier
    • 1
    • 2
  • Fabrice Not
    • 1
    • 2
  1. 1.UPMC University Paris 06RoscoffFrance
  2. 2.CNRSRoscoffFrance
  3. 3.IFREMER, Centre de Brest, DYNECO/PelagosPlouzanéFrance
  4. 4.UPMC University Paris 06RoscoffFrance

Personalised recommendations