Advertisement

Symbiosis

, Volume 57, Issue 1, pp 51–55 | Cite as

Ultrastructural and molecular characterization of cyanobacterial symbionts in Dictyocoryne profunda (polycystine radiolaria)

  • Tomoko Yuasa
  • Takeo Horiguchi
  • Shigeki Mayama
  • Atsushi Matsuoka
  • Osamu Takahashi
Article

Abstract

Cyanobacterial symbionts were detected in the extracytoplasm of the polycystine radiolarian Dictyocoryne profunda Ehrenberg. The bacterial symbionts were observed as numerous spherical bodies ~0.5–1.0 μm in diameter under transmission electron microscopy. They were present in a very restricted location close to the periphery of the host radiolarian shell, adjacent to the central capsular wall. Several cells of them may have been in the process of cell division or just divided. The symbionts had thylakoid-like structures, which ran around the cell periphery in two or three concentric layers. Based on the small subunit ribosomal DNA (16S rDNA) phylogenetic analyses, the intracellular symbiotic bacteria grouped with cyanobacteria belonging to the genus Synechococcus. Three sequences, one from each of three specimens of D. profunda, collected in March/October 2009 and March 2010 from the East China Sea, were the same and branched within Synechococcus clade II, that is characterized by strains with low amounts of phycourobilin (PUB).

Keywords

Cyanobacteria Dictyocoryne profunda Radiolaria Symbiont Synechococcus

Notes

Acknowledgments

We would like to acknowledge A. Takemura, Y. Nakano, and S. Nakamura of the University of the Ryukyus for their support and helpful discussions. We also wish to thank D. Honda of the Konan University for his valuable advice and suggestions. This study was financially supported by the grant-in-aid from JSPS Grants 19540491 and 23540545 to O. Takahashi.

References

  1. Anderson OR (1983) Radiolaria. Springer–Verlag, New YorkCrossRefGoogle Scholar
  2. Anderson OR, Matsuoka A (1992) Endocytoplasmic microalgae and bacteroids within the central capsule of the radiolarian Dictyocoryne truncatum. Symbiosis 12:237–247Google Scholar
  3. Brandt K (1881) Ueber das Zusammenleben von Thieren und Algen. Verh Physiol Ges Berlin 1881(1882):22–26Google Scholar
  4. Carpenter EJ, Foster RA (2002) Marine cyanobacterial symbioses. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer Academic Pub, Netherlands, pp 11–17Google Scholar
  5. Casey RE (1971) Distribution of polycystine Radiolaria in the oceans in relation to physical and chemical conditions. In: Funnell BM, Riedel WR (eds) The Micropalaeontology of oceans. Cambridge University Press, Cambridge, pp 151–159Google Scholar
  6. Choi DH, Noh JH (2009) Phylogenetic diversity of Synechococcus strains isolated from the East China Sea and the East Sea. FEMS Microbiol Ecol 69:439–448PubMedCrossRefGoogle Scholar
  7. Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853PubMedCrossRefGoogle Scholar
  8. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  9. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  10. Ferris MJ, Palenik B (1998) Niche adaptation in ocean cyanobacteria. Nature 396:226–228CrossRefGoogle Scholar
  11. 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. J Phycol 42:243–250CrossRefGoogle Scholar
  12. 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. J Phycol 42:453–463CrossRefGoogle Scholar
  13. Fuller NJ, Marie D, Partensky F, Vaulot D, Post AF, Scanlan DJ (2003) Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol 69:2430–2443PubMedCrossRefGoogle Scholar
  14. Gast RJ, Caron DA (1996) Molecular phylogeny of symbiotic dinoflagellates from planktonic foraminifera and radiolaria. Mol Biol Evol 13:1192–1197PubMedCrossRefGoogle Scholar
  15. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  16. Rambaut A (1996) Se-Al. Sequence Alignment Editor, version1.0a1. Distributed by the author, Department of Zoology, University of OxfordGoogle Scholar
  17. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212PubMedCrossRefGoogle Scholar
  18. Rocap G, Distel DL, Waterbury JB, Chisholm SW (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68:1180–1191PubMedCrossRefGoogle Scholar
  19. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  20. Swofford DL (2002) Phylogenetic Analysis Using Parsimony (PAUP*), ver 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
  21. Tai V, Palenik B (2009) Temporal variation of Synechococcus clades at a costal Pacific Ocean monitoring site. ISME J 3:903–915PubMedCrossRefGoogle Scholar
  22. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Tomoko Yuasa
    • 1
  • Takeo Horiguchi
    • 2
  • Shigeki Mayama
    • 3
  • Atsushi Matsuoka
    • 4
  • Osamu Takahashi
    • 1
  1. 1.Department of Astronomy and Earth SciencesTokyo Gakugei UniversityKoganeiJapan
  2. 2.Department of Natural History Sciences, Faculty of ScienceHokkaido UniversitySapporoJapan
  3. 3.Department of BiologyTokyo Gakugei UniversityKoganeiJapan
  4. 4.Department of Geology, Faculty of ScienceNiigata UniversityNiigataJapan

Personalised recommendations