Skip to main content
SpringerLink
Log in

Genetic diversity of Moestrupia oblonga (Dinophyceae) from coastal areas of Okinawa Island, Japan

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

The genetic diversity of marine benthic dinoflagellate strains morphologically identified as Moestrupia oblonga from the coastal areas of Okinawa Island, Japan, were investigated. All strains shared similar morphologies, such as unarmored cells with a rice grain-like shape, the cingulum displacing about one third of the body length, a distinctive ventral flange, and a conspicuous central pyrenoid, while the nucleus was positioned in the hypocone, conforming to the general morphology of M. oblonga (Larsen and Patterson) Hansen and Daugbjerg from Tenerife, Canary Island, Spain. Molecular phylogenetic analyses based on LSU rDNA D1-D3 and the concatenated dataset of SSU-ITS1-5.8S-ITS2-LSU rDNA sequences indicated that all strains are monophyletic, but separated into three genetically distinct clades; namely, Clade A, B, and C. Intraclade sequence divergence in the respective clades was less than 0.3 % for all molecular markers, excluding the ITS1-5.8S rDNA-ITS2 region of Clade B and Clade C that showed sequence divergence of 0.7 % and 1.75 % among its members, respectively. The mean interclade divergences between clades were about 1.2–3.7 % in SSU rDNA, but reached 18–26 % and 6.3–9.7 % for nucleotides in ITS and LSU rDNA sequences, respectively. Despite the link between the three Okinawan clades and M. oblonga (JF272764) from Spain showing close affinity in LSU rDNA D1-D3 phylogeny, they diverged about 7.5–12 % regarding base pairs from this sole representative of the genus. Moreover, the formation of these clades was somewhat consistent with morphological differentiation based on cell sizes, indicating that these clades may represent three pseudo-cryptic species in the genus, discreet from M. oblonga from Tenerife, Spain. This study reveals that the genus Moestrupia is much more complex than previous reports have suggested.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alpermann TJ, Tillmann U, Beszteri B, Cembella AD, John U (2010) Phenotypic variation and genotypic diversity in a planktonic population of the toxigenic marine dinoflagellate Alexandrium tamarense (Dinophyceae). J Phycol 46:18–32

    Article  CAS  Google Scholar 

  • Al-Qassab S, Le WJ, Murray S, Simpson AGB, Patterson DJ (2002) Flagellates from stromatolites and surrounding sediments in Shark Bay, Western Australia. Acta Protozool 41:91–144

    Google Scholar 

  • Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000) Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302–317

    Article  Google Scholar 

  • Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flø Jørgensen M, Murray S, Daugbjerg N (2004) Amphidinium revisited. I. Redefinition of Amphidinium (Dinophyceae) based on cladistics and molecular phylogenetic analyses. J Phycol 40:351–365

    Article  Google Scholar 

  • Grzebyk D, Sako Y, Berland B (1998) Phylogenetic analysis of nine species of Prorocentrum (Dinophyceae) inferred from 18S ribosomal DNA sequences, morphological comparisons, and description of Prorocentrum panamensis, sp. nov. J Phycol 34:1055–1068

    Article  CAS  Google Scholar 

  • Hallegraeff GM (2004) Taxonomic principles. In: Hallegraeff GM, Anderson DM, Cembella AD (eds) Manual on harmful marine microalgae. Monographs on oceanographic methodology, 2nd edn. UNESCO Publishing, Paris, pp 383–388

    Google Scholar 

  • Hansen G, Daugbjerg N (2009) Symbiodinium natans sp. nov.: a “free-living” dinoflagellate from Tenerife (Northeast-Atlantic Ocean). J Phycol 45:251–263

    Article  Google Scholar 

  • Hansen G, Daugbjerg N (2011) Moestrupia oblonga gen. & comb. nov. (syn.: Gyrodinium oblongum), a new marine dinoflagellate genus characterized by light and electron microscopy, photosynthetic pigments and LSU rDNA sequence. Phycologia 50:583–599

    Article  CAS  Google Scholar 

  • Hansen G, Daugbjerg N, Henriksen P (2000) Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov. (= Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. J Phycol 36:394–410

    Article  Google Scholar 

  • Herrera-Sepúlveda A, Medlin LK, Murugan G, Sierra-Beltrán AP, Cruz-Villacorta AA, Hernández-Saavedra NY (2015) Are Prorocentrum hoffmannianum and Prorocentrum belizeanum (Dinophyceae, Prorocentrales), the same species? An integration of morphological and molecular data. J Phycol 51:173–188

    Article  PubMed  Google Scholar 

  • Hoppenrath M, Elbrächter M, Drebes G (2009) Marine phytoplankton. Selected microphytoplankton species from the North Sea around Helgoland and Sylt. Kleine Senck. Reihe 49. Schweizerbart’sche Verlag., Sttutgart

  • Hoppenrath M, Chomérat N, Horiguchi T, Schweikert M, Nagahama Y, Murray S (2013) Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae) - a proposal and review. Harmful Algae 27:1–28

  • John U, Litaker RW, Montresor M, Murray S, Brosnahan ML, Anderson DM (2014) Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165:779–804

    Article  PubMed  PubMed Central  Google Scholar 

  • Kofoid CA, Swezy O (1921) The free-living unarmored Dinoflagellata. Mem Univ Calif 5:1–564

    Google Scholar 

  • Kohli GS, Neilan BA, Brown MV, Hoppenrath M, Murray S (2014) Cob gene pyrosequencing enables characterization of benthic dinoflagellate diversity and biogeography. Environ Microbiol 16:467–485

    Article  CAS  PubMed  Google Scholar 

  • 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. J Phycol 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53:305–319

    Article  Google Scholar 

  • Larsen J, Patterson DJ (1990) Some flagellates (Protista) from tropical marine sediments. J Nat Hist 24:801–937

    Article  Google Scholar 

  • Lilly EL, Halanych KM, Anderson DM (2007) Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J Phycol 43:1329–1338

    Article  CAS  Google Scholar 

  • Lin S, Zhang H, Jiao N (2006) Potential utility of mitochondrial cytochrome b and its mRNA editing in resolving closely related dinoflagellates: a case study of Prorocentrum (Dinophyceae). J Phycol 42:646–654

    Article  CAS  Google Scholar 

  • Litaker RW, Vandersea MW, Kibler SR, Reece KS, Stokes NA, Lutzoni FM, Yonish BA, West MA, Black MND, Tester PA (2007) Recognizing dinoflagellate species using ITS rDNA sequences. J Phycol 43:344–355

    Article  CAS  Google Scholar 

  • Moestrup Ø, Hakanen P, Hansen G, Daugbjerg N, Ellegaard M (2014) On Levanderina fissa gen. & comb. nov. (Dinophyceae) (syn. Gymnodinium fissum, Gyrodinium instriatum, Gyr. uncatenum), a dinoflagellate with a very unusual sulcus. Phycologia 53:265–292

    Article  Google Scholar 

  • Mohammad-Noor N, Moestrup Ø, Daugbjerg N (2007) Light, electron microscopy and DNA sequences of the dinoflagellate Prorocentrum concavum (syn. P. arabianum) with special emphasis on the periflagellar area. Phycologia 46:549–564

    Article  Google Scholar 

  • Murray S (2010) Benthic dinoflagellate. In: Hallegraeff GM, Bolch CJS, Hill DRA, Jameson I, Leroi J-M, McMinn A, Murray S, de Salas MF, Saunders K (eds) Algae of Australia: Phytoplanton of Temperate Coastal Waters, 1st edn. CSIRO Publishing, Collingwood, pp 213–259

    Google Scholar 

  • Murray S, Garby T, Hoppenrath M, Neilan BA (2012) Genetic diversity, morphological uniformity and polyketide production in dinoflagellates (Amphidinium, Dinoflagellata). PLoS ONE 7:e38253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagahama Y, Murray S, Tomaru A, Fukuyo Y (2011) Species boundaries in the toxic dinoflagellate Prorocentrum lima (Dinophyceae, Prorocentrales), based on morphological and phylogenetic characters. J Phycol 47:178–189

    Article  Google Scholar 

  • Nylander J (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden

  • Rambaut A (2014) Tree figure drawing tool: Figtree version 1.4.2 (downloaded from http://tree.bio.ed.ac.uk/software/figtree/)

  • Rambaut A, Suchard M, Drummond A (2013) MCMC trace analysis tool: Tracer v.1.6.0. http://beast.bio.ed.ac.uk/

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337

    Article  Google Scholar 

  • Stern RF, Andersen RA, Jameson I, Küpper FC, Coffroth MA, Vaulot D, Le Gall F, Véron B, Brand JJ, Skelton H, Kasai F, Lilly EL, Keeling PJ (2012) Evaluating the ribosomal internal transcribed spacer (ITS) as a candidate dinoflagellate barcode marker. PLoS ONE 7:e42780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takano Y, Horiguchi T (2006) Acquiring scanning electron microscopical, light microscopical and multiple gene sequence data from a single dinoflagellate cell. J Phycol 42:251–256

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor FJR, Hoppenrath M, Saldarriaga JF (2008) Dinoflagellate diversity and distribution. Biodivers Conserv 17:407–418

    Article  Google Scholar 

  • Zhang H, Bhattacharya D, Lin S (2005) Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J Phycol 41:411–420

Download references

Acknowledgments

We would like to thanks to two anonymous reviewers for constructive comments on the manuscript. This work was partly supported by Okinawa Intellectual Cluster Program, International Research Hub Project for Climate Change and Coral Reef/Island Dynamics of the University of the Ryukyus, and ‘Biodiversity and evolution of algae in the Indo-Pacific: a Japan-South Africa comparison’ (Strategic International Research Cooperative Program) of Japan Science and Technology Agency.

Author information

Authors and Affiliations

  1. Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    Danang Ambar Prabowo & Md. Mahfuzur Rahman Shah

  2. School of Environment and Energy, Peking University, University Town, Xili, Nanshan District, Shenzhen, 518055, People’s Republic of China

    Md. Mahfuzur Rahman Shah

  3. Department of Biological Sciences, Faculty of Science, Hokkaido University, North 10, West 8, Sapporo, 060-0810, Japan

    Takeo Horiguchi

  4. Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    Shoichiro Suda

Authors
  1. Danang Ambar Prabowo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Md. Mahfuzur Rahman Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takeo Horiguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shoichiro Suda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shoichiro Suda.

Additional information

Communicated by B. Leander

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prabowo, D.A., Shah, M.R., Horiguchi, T. et al. Genetic diversity of Moestrupia oblonga (Dinophyceae) from coastal areas of Okinawa Island, Japan. Mar Biodiv 46, 197–209 (2016). https://doi.org/10.1007/s12526-015-0351-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-015-0351-7

Keywords

Search

Navigation