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

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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 This hypothesis for the origin of the Lepidodinium plastids is solely based on an unpublished result quoted in Elbrächter and Schnepf (Phycologia 35:381–393, 1996) hinting at the presence of a characteristic carotenoid in prasinophytes, prasinoxanthin,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.

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References

  • 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 42:170–193

    Article  Google Scholar 

  • 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 39:1233–1246

    Article  Google Scholar 

  • Elbrächter M, Schnepf E (1996) Gymnodinium chlorophorum, a new, green, bloom-forming dinoflagellate (Gymnodiniales, Dinophyceae) with a vestigial prasinophyte endosymbiont. Phycologia 35:381–393

    Article  Google Scholar 

  • Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Horiguchi T, Takano Y (2006) Serial replacement of a diatom endosymbiont in the marine dinoflagellate Peridinium quinquecorne (Peridiniales, Dinophyceae). Phycol Res 54:193–200

    Article  Google Scholar 

  • 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 29:913–929

    Article  CAS  Google Scholar 

  • 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 60:68–72

    Article  PubMed  CAS  Google Scholar 

  • 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 162:268–276

    Article  PubMed  Google Scholar 

  • Meyer-Harms B, Pollehne F (1998) Alloxanthin in Dinophysis norvegica (Dinophysiales, Dinophyceae) from the Baltic Sea. J Phycol 34:280–285

    Article  CAS  Google Scholar 

  • 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 215–230

    Chapter  Google Scholar 

  • Noël MH, Kawachi M, Inouye I (2004) Induced dimorphic life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea (Prymnesiophyceae, Haptophyta). J Phycol 40:112–129

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Saldarriaga JF, Taylor FJR, Keeling PJ, Cavalier-Smith T (2001) Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53:204–213

    Article  PubMed  CAS  Google Scholar 

  • 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 53:217–224

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  PubMed  CAS  Google Scholar 

  • Suzuki R, Ishimaru T (1992) Characteristics of photosynthetic pigment composition of Gymnodinium mikimotoi Miyake et Kominami ex ODA. J Oceanogr 48:367–375

    Article  CAS  Google Scholar 

  • 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 47:257–262

    Article  Google Scholar 

  • Takishita K, Koike K, Maruyama T, Ogata T (2002) Molecular evidence for plastid robbery (kleptoplastidy) in Dinophysis, a dinoflagellate causing diarrhetic shellfish poisoning. Protist 153:293–302

    Article  PubMed  CAS  Google Scholar 

  • 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 410:26–36

    Article  PubMed  CAS  Google Scholar 

  • Tamura M, Shimada S, Horiguchi T (2005) Galeidinium rugatum gen. et sp. nov. (Dinophyceae), a new coccoid dinoflagellate with as diatom endosymbiont. J Phycol 41:658–671

    Article  CAS  Google Scholar 

  • Taylor FJR (1980) On dinoflagellate evolution. Biosystems 13:65–108

    Article  PubMed  CAS  Google Scholar 

  • 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 17:718–729

    Article  PubMed  CAS  Google Scholar 

  • 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 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • 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 23:382–389

    Article  CAS  Google Scholar 

  • 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 26:741–751

    Article  Google Scholar 

  • Withers N, Haxo FT (1975) Chlorophyll c 1 and c 2 and extraplastidic carotenoids in the dinoflagellate, Peridinium foliaceum Stein. Plant Sci Lett 5:7–15

    Article  CAS  Google Scholar 

  • Withers NW, Cox ER, Tomas R, Haxo FT (1977) Pigments of the dinoflagellate Peridinium balticum and its photosynthetic endosymbiont. J Phycol 13:354–358

    CAS  Google Scholar 

  • 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 195:29–45

    Article  CAS  Google Scholar 

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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.

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Authors and Affiliations

  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Takuya Matsumoto & Yuji Inagaki

  2. National Institute for Environmental Studies, Tsukuba, Ibaraki, 305-8506, Japan

    Masanobu Kawachi

  3. Department of Interdisciplinary Environment, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Kyoto, 606-8501, Japan

    Hideaki Miyashita

  4. Center for Computational Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8577, Japan

    Yuji Inagaki

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  1. Takuya Matsumoto
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  2. Masanobu Kawachi
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  3. Hideaki Miyashita
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  4. Yuji Inagaki
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Correspondence to Yuji Inagaki.

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Matsumoto, T., Kawachi, M., Miyashita, H. et al. Prasinoxanthin is absent in the green-colored dinoflagellate Lepidodinium chlorophorum strain NIES-1868: pigment composition and 18S rRNA phylogeny. J Plant Res 125, 705–711 (2012). https://doi.org/10.1007/s10265-012-0486-6

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  • DOI: https://doi.org/10.1007/s10265-012-0486-6

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