Advertisement

Journal of Plant Research

, Volume 125, Issue 6, pp 705–711 | Cite as

Prasinoxanthin is absent in the green-colored dinoflagellate Lepidodinium chlorophorum strain NIES-1868: pigment composition and 18S rRNA phylogeny

  • Takuya Matsumoto
  • Masanobu Kawachi
  • Hideaki Miyashita
  • Yuji Inagaki
Regular Paper

Abstract

Green-colored plastids in the dinoflagellates Lepidodinium chlorophorum and L. viride have been widely believed as the remnant of an endosymbiotic prasinophyte. This hypothesis for the origin of the Lepidodinium plastids is solely based on an unpublished result quoted in Elbrächter and Schnepf (Phycologia 35:381–393, 1996) hinting at the presence of a characteristic carotenoid in prasinophytes, prasinoxanthin, in the L. chlorophorum cells. On the other hand, a recent work failed to detect prasinoxanthin in a culture of L. chlorophorum. Unfortunately, we cannot conduct any additional experiments to examine whether the two strains considered in the previous studies are truly of L. chlorophorum, as neither of the two strains is publicly available. We here investigated the pigment composition of L. chlorophorum strain NIES-1868 maintained as a mono-algal culture under laboratory conditions, and detected no sign of prasinoxanthin. The pigment composition of strain NIES-1868 is consistent with previous phylogenetic analyses based on plastid-encoded genes of the same strain, which successfully excluded prasinoxanthin-containing algae from the origin of the L. chlorophorum plastid. We also determined nucleus-encoded 18S ribosomal RNA (rRNA) genes from four Lepidodinium strains (including strain NIES-1868). Analyses of 18S rRNA sequences showed an extremely close relationship among strain NIES-1868 and other Lepidodinium cells/strains originating from different geological locations, suggesting that the cells/strains corresponding to these rRNA sequences lack prasinoxanthin.

Keywords

Plastid replacement Tertiary endosymbiosis Serial secondary endosymbiosis 

Notes

Acknowledgments

We thank Drs. R. Kamikawa (University of Tsukuba, Japan), T. Hashimoto (University of Tsukuba, Japan), and K. Takishita (JAMSTEC, Japan) for their critical comments on this manuscript. We also thank Dr. M. H. Noël (NIES, Japan) for providing Lepidodinium strains NIES-1867, 1868, and MH360. TM is a research fellow supported by the Japan Society for Promotion of Sciences (JSPS) for Young Scientists (No. 21508). This work was supported by grants from JSPS and the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 21370031 and 23117006) awarded to YI.

References

  1. Bergholtz T, Daugbjerg N, Moestrup Ø, Fernandez-Tejedor M (2005) On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. J Phycol 42:170–193CrossRefGoogle Scholar
  2. De Salas MF, Bolch CJS, Botes L, Nash G, Wright SW, Hallegraeff GM (2003) Takayama gen. nov. (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. J Phycol 39:1233–1246CrossRefGoogle Scholar
  3. Elbrächter M, Schnepf E (1996) Gymnodinium chlorophorum, a new, green, bloom-forming dinoflagellate (Gymnodiniales, Dinophyceae) with a vestigial prasinophyte endosymbiont. Phycologia 35:381–393CrossRefGoogle Scholar
  4. Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239PubMedCrossRefGoogle Scholar
  5. Horiguchi T, Takano Y (2006) Serial replacement of a diatom endosymbiont in the marine dinoflagellate Peridinium quinquecorne (Peridiniales, Dinophyceae). Phycol Res 54:193–200CrossRefGoogle Scholar
  6. Laza-Martinez A, Seoane S, Zapata M, Orive E (2007) Phytoplankton pigment patterns in a temperate estuary: from unialgal cultures to natural assemblages. J Plankton Res 29:913–929CrossRefGoogle Scholar
  7. Matsumoto T, Ishikawa SA, Hashimoto T, Inagaki Y (2011a) A deviant genetic code in the green alga-derived plastid in the dinoflagellate Lepidodinium chlorophorum. Mol Phylogenet Evol 60:68–72PubMedCrossRefGoogle Scholar
  8. Matsumoto T, Shinozaki F, Chikuni T, Yabuki A, Takishita K, Kawachi M, Nakayama T, Inouye I, Hashimoto T, Inagaki Y (2011b) Green-colored plastids in the dinoflagellate genus Lepidodinium are of core chlorophyte origin. Protist 162:268–276PubMedCrossRefGoogle Scholar
  9. Meyer-Harms B, Pollehne F (1998) Alloxanthin in Dinophysis norvegica (Dinophysiales, Dinophyceae) from the Baltic Sea. J Phycol 34:280–285CrossRefGoogle Scholar
  10. Moestrup Ø, Daugbjerg N (2007) On dinoflagellate phylogeny and classification. In: Brodie J, Lewis J (eds) Unravelling the algae: the past, present, and future of algal systematics. CRC Press, Boca Raton, pp 215–230CrossRefGoogle Scholar
  11. Noël MH, Kawachi M, Inouye I (2004) Induced dimorphic life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea (Prymnesiophyceae, Haptophyta). J Phycol 40:112–129CrossRefGoogle Scholar
  12. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  13. Saldarriaga JF, Taylor FJR, Keeling PJ, Cavalier-Smith T (2001) Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53:204–213PubMedCrossRefGoogle Scholar
  14. Shalchian-Tabrizi K, Minge MA, Cavalier-Smith T, Nedreklepp JM, Klaveness D, Jakobsen KS (2006) Combined heat shock protein 90 and ribosomal RNA sequence phylogeny supports multiple replacements of dinoflagellate plastids. J Eukaryot Microbiol 53:217–224PubMedCrossRefGoogle Scholar
  15. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  16. Suzuki R, Ishimaru T (1992) Characteristics of photosynthetic pigment composition of Gymnodinium mikimotoi Miyake et Kominami ex ODA. J Oceanogr 48:367–375CrossRefGoogle Scholar
  17. Takishita K, Nakano K, Uchida A (1999) Preliminary phylogenetic analysis of plastid-encoded genes from an anomalously pigmented dinoflagellate Gymnodinium mikimotoi (Gymnodiniales, Dinophyta). Phycol Res 47:257–262CrossRefGoogle Scholar
  18. Takishita K, Koike K, Maruyama T, Ogata T (2002) Molecular evidence for plastid robbery (kleptoplastidy) in Dinophysis, a dinoflagellate causing diarrhetic shellfish poisoning. Protist 153:293–302PubMedCrossRefGoogle Scholar
  19. Takishita K, Kawachi M, Noël MH, Matsumoto T, Kakizoe N, Watanabe MM, Inouye I, Ishida K, Hashimoto T, Inagaki Y (2008) Origins of plastids and glyceraldehyde-3-phosphate dehydrogenase genes in the green-colored dinoflagellate Lepidodinium chlorophorum. Gene 410:26–36PubMedCrossRefGoogle Scholar
  20. Tamura M, Shimada S, Horiguchi T (2005) Galeidinium rugatum gen. et sp. nov. (Dinophyceae), a new coccoid dinoflagellate with as diatom endosymbiont. J Phycol 41:658–671CrossRefGoogle Scholar
  21. Taylor FJR (1980) On dinoflagellate evolution. Biosystems 13:65–108PubMedCrossRefGoogle Scholar
  22. Tengs T, Dahlberg OJ, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche CF, Jakobsen KS (2000) Phylogenetic analyses indicate that the 19′ hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol Biol Evol 17:718–729PubMedCrossRefGoogle Scholar
  23. 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
  24. Watanabe MM, Takeda Y, Sasa T, Inouye I, Suda S, Sawaguchi T, Chihara M (1987) A green dinoflagellate with chlorophylls a and b: morphology, fine structure of the chloroplast and chlorophyll composition. J Phycol 23:382–389CrossRefGoogle Scholar
  25. Watanabe MM, Suda S, Inouye I, Sawaguchi T, Chihara M (1990) Lepidodinium viride gen. et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with a chlorophyll a- and b-containing endosymbiont. J Phycol 26:741–751CrossRefGoogle Scholar
  26. Withers N, Haxo FT (1975) Chlorophyll c 1 and c 2 and extraplastidic carotenoids in the dinoflagellate, Peridinium foliaceum Stein. Plant Sci Lett 5:7–15CrossRefGoogle Scholar
  27. Withers NW, Cox ER, Tomas R, Haxo FT (1977) Pigments of the dinoflagellate Peridinium balticum and its photosynthetic endosymbiont. J Phycol 13:354–358Google Scholar
  28. Zapata M, Garrido JL, Rodríguez F (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195:29–45CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2012

Authors and Affiliations

  • Takuya Matsumoto
    • 1
  • Masanobu Kawachi
    • 2
  • Hideaki Miyashita
    • 3
  • Yuji Inagaki
    • 1
    • 4
  1. 1.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan
  2. 2.National Institute for Environmental StudiesTsukubaJapan
  3. 3.Department of Interdisciplinary Environment, Graduate School of Human and Environmental StudiesKyoto UniversityKyotoJapan
  4. 4.Center for Computational SciencesUniversity of TsukubaTsukubaJapan

Personalised recommendations