Morphology and molecular characterization of the epiphytic dinoflagellate Amphidinium massartii, isolated from the temperate waters off Jeju Island, Korea

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  • ABSTRACT

    Amphidinium massartii Biecheler is an epiphytic and toxic dinoflagellate. Prior to the present study, A. massartii has been reported in the waters off the Mediterranean, Australian, USA, and Canadian coasts. We isolated Amphidinium cells from the coastal waters of Jeju Island, Korea and their morphology and rDNA sequences indicated that they were A. massartii. Herein, we report for the first time the occurrence of A. massartii in the waters of the temperate region in the northwestern Pacific Ocean. The large subunit (LSU) rDNA sequences of the Korean strains were 0.7% different from those of an Australian strain of A. massartii CS-259, the closest species, but were 4.1-5.8% different from those of the other Australian strains and the USA strains of A. massartii and from those of Amphidinium sp. HG115 that was isolated from subtropical Okinawan waters. In phylogenetic trees based on LSU, internal transcribed spacer, small subunit rDNA, and cytochrome b sequences, the Korean strains belonged to the A. massartii clade, which was clearly divergent from the A. carterae clade. The morphology of the Korean A. massartii strains was similar to that of the originally described French strain and recently described Australian strain. However, we report for the first time here that scales were observed on the surface of the flagella. In conclusion, the Korean A. massartii strains have unique rDNA sequences, even though they have a very similar morphology to that of previously reported strains. This report extends the known range of this dinoflagellate to the temperate waters of the northwestern Pacific Ocean.


  • KEYWORD

    Amphidinium carterae , Amphidinium massartii , epiphytic dinoflagellate , molecular analysis , phylogenetic analysis

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  • [Table 1.] Oligonucleotide primers and sequences used in this study to amplify the SSU, ITS1, 5.8S, ITS2, and LSU regions of rDNA and cytochrome b (mitochondrial gene) of Amphidinium massartii
    Oligonucleotide primers and sequences used in this study to amplify the SSU, ITS1, 5.8S, ITS2, and LSU regions of rDNA and cytochrome b (mitochondrial gene) of Amphidinium massartii
  • [Table 2.] List of Amphidinium species used to construct phylogenetic trees
    List of Amphidinium species used to construct phylogenetic trees
  • [Table 3.] Comparison of SSU, ITS1, 5.8S, ITS2, and LSU rDNA sequences of strains of Amphidinium massartii, A. carterae, and Amphidinium sp. isolated from the waters of Korea and other countries
    Comparison of SSU, ITS1, 5.8S, ITS2, and LSU rDNA sequences of strains of Amphidinium massartii, A. carterae, and Amphidinium sp. isolated from the waters of Korea and other countries
  • [Fig. 1.] Consensus Bayesian tree based on 929-bp aligned positions of large subunit rDNA region using the GTR + I + G model. A substitution rate matrix was used: A-C substitutions, 0.0820; A-G substitutions, 0.2400; A-T substitutions, 0.1100; C-G substitutions, 0.5000; C-T substitutions, 0.4450; G-T substitutions, 0.0740. The proportion of sites assumed to be invariable was 0.0470 and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 0.6334. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
    Consensus Bayesian tree based on 929-bp aligned positions of large subunit rDNA region using the GTR + I + G model. A substitution rate matrix was used: A-C substitutions, 0.0820; A-G substitutions, 0.2400; A-T substitutions, 0.1100; C-G substitutions, 0.5000; C-T substitutions, 0.4450; G-T substitutions, 0.0740. The proportion of sites assumed to be invariable was 0.0470 and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 0.6334. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
  • [Fig. 2.] Consensus Bayesian tree based on 461-bp aligned positions of internal transcribed spacer rDNA using the GTR + I + G model. A substitution rate matrix was used: A-C substitutions, 0.0770; A-G substitutions, 0.3000; A-T substitutions, 0.1400; C-G substitutions, 0.0950; C-T substitutions, 0.3000; G-T substitutions, 0.0900. The proportion of sites assumed to be invariable was 0.1240 and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 13.0030. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
    Consensus Bayesian tree based on 461-bp aligned positions of internal transcribed spacer rDNA using the GTR + I + G model. A substitution rate matrix was used: A-C substitutions, 0.0770; A-G substitutions, 0.3000; A-T substitutions, 0.1400; C-G substitutions, 0.0950; C-T substitutions, 0.3000; G-T substitutions, 0.0900. The proportion of sites assumed to be invariable was 0.1240 and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 13.0030. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
  • [Fig. 3.] Consensus Bayesian tree based on 1,640-bp aligned positions of small subunit rDNA using the GTR + I + G model. A substitution rate matrix was used: A-C substitutions, 0.0800; A-G substitutions, 0.2400; A-T substitutions, 0.1000; C-G substitutions, 0.0400; C-T substitutions, 0.4800; G-T substitutions, 0.0500. The proportion of sites assumed to be invariable was 0.4300 and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 13.1030. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
    Consensus Bayesian tree based on 1,640-bp aligned positions of small subunit rDNA using the GTR + I + G model. A substitution rate matrix was used: A-C substitutions, 0.0800; A-G substitutions, 0.2400; A-T substitutions, 0.1000; C-G substitutions, 0.0400; C-T substitutions, 0.4800; G-T substitutions, 0.0500. The proportion of sites assumed to be invariable was 0.4300 and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 13.1030. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
  • [Fig. 4.] Consensus Bayesian tree based on 371-bp aligned positions of a cytochrome b region of the mitochondrial DNA using the GTR + I + G model. The parameters were as follows: the assumed nucleotide frequency was empirical; substitution rate matrix: A-C substitutions, 0.1377; A-G substitutions, 0.2145; A-T substitutions, 0.1118; C-G substitutions, 0.3327; C-T substitutions, 0.1523; G-T substitutions, 0.0510; the proportion of sites assumed to be invariable was 0.1440; and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 1.4222. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
    Consensus Bayesian tree based on 371-bp aligned positions of a cytochrome b region of the mitochondrial DNA using the GTR + I + G model. The parameters were as follows: the assumed nucleotide frequency was empirical; substitution rate matrix: A-C substitutions, 0.1377; A-G substitutions, 0.2145; A-T substitutions, 0.1118; C-G substitutions, 0.3327; C-T substitutions, 0.1523; G-T substitutions, 0.0510; the proportion of sites assumed to be invariable was 0.1440; and the rate for variable sites was assumed to follow a gamma distribution with a shape parameter of 1.4222. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum liklihood bootstrap values (right). Posterior probabilities ≥0.5 are shown.
  • [Fig. 5.] Micrographs of the Korean strain of Amphidinium massartii AMJJ1 under light microscopy (A-G) and epifluorescent microscopy (H). (A) Motile cells. (B) Cells embedded in mucilage. (C) Ventral view showing an almost ellipsoidal cell with a small epicone (EC) over a large hypocone (HC). The V-shaped cingulum (CI), transverse flagellum (TF), longitudinal flagellum (LF), and the sulcus (SU) are also shown. (D) Ventral view showing a pyrenoid (PY) located near the central region. (E) Lateral view. (F) Dorsal view showing the nucleus (NU) located in the hypocone and PY. (G) Cell division in a motile cell. (H) Lateral view a plastid (CP) radiating lobes (LO). Scale bars represent: C-H, 5 μm.
    Micrographs of the Korean strain of Amphidinium massartii AMJJ1 under light microscopy (A-G) and epifluorescent microscopy (H). (A) Motile cells. (B) Cells embedded in mucilage. (C) Ventral view showing an almost ellipsoidal cell with a small epicone (EC) over a large hypocone (HC). The V-shaped cingulum (CI), transverse flagellum (TF), longitudinal flagellum (LF), and the sulcus (SU) are also shown. (D) Ventral view showing a pyrenoid (PY) located near the central region. (E) Lateral view. (F) Dorsal view showing the nucleus (NU) located in the hypocone and PY. (G) Cell division in a motile cell. (H) Lateral view a plastid (CP) radiating lobes (LO). Scale bars represent: C-H, 5 μm.
  • [Fig. 6.] Micrographs of the Korean strain of Amphidinium massartii AMJJ1 taken using scanning electron microscopy. (A) Ventral view showing the tongue-shaped epicone (EC), cingulum (CI), transverse flagellum (TF), sulcus (SU), longitudinal flagellum (LF), and hypocone (HC). (B) Dorsal view showing EC, CI, and HC. (C) Lateral view showing the dorso-ventrally flattened EC, TF, SU, CI, and HC. (D) Ventral view showing EC, LF, TF, SU, HC, and ventral ridge (VR). (E) Enlargement of Fig. 2D showing EC, TF, and VR. Scale bars represent: A-E, 2 μm.
    Micrographs of the Korean strain of Amphidinium massartii AMJJ1 taken using scanning electron microscopy. (A) Ventral view showing the tongue-shaped epicone (EC), cingulum (CI), transverse flagellum (TF), sulcus (SU), longitudinal flagellum (LF), and hypocone (HC). (B) Dorsal view showing EC, CI, and HC. (C) Lateral view showing the dorso-ventrally flattened EC, TF, SU, CI, and HC. (D) Ventral view showing EC, LF, TF, SU, HC, and ventral ridge (VR). (E) Enlargement of Fig. 2D showing EC, TF, and VR. Scale bars represent: A-E, 2 μm.
  • [Table 4.] Comparison of the morphology of strains of Amphidinium massartii (AM) and A. carterae (AC) isolated from the waters of Korea and other countries
    Comparison of the morphology of strains of Amphidinium massartii (AM) and A. carterae (AC) isolated from the waters of Korea and other countries
  • [Fig. 7.] Micrographs of the Korean strains of Amphidinium massartii AMJJ1 (A & B) and AMJJ2 (C-F) taken using scanning electron microscopy. (A) A cell having amphiesmal vescicles (AV) on the surface of the outer membrane. (B) Enlarged part of Fig. 7A showing body scales (BS) on the outer membrane of the cell. (C) Lateral view showing the epicone (EC), longitudinal flagellum (LF), transverse flagellum (TF), and hypocone (HC). (D) Enlarged part of Fig. 7C showing flagellar scales (FS) on the LF. (E) Lateral view showing a cell with the outer membranes (OM) partially removed. (F) Enlarged part of Fig. 7E showing a thin plate (TP) layer, OM, and BS. Scale bars represent: A & C, 1 μm; E, 2 μm; B, D & F, 200 nm.
    Micrographs of the Korean strains of Amphidinium massartii AMJJ1 (A & B) and AMJJ2 (C-F) taken using scanning electron microscopy. (A) A cell having amphiesmal vescicles (AV) on the surface of the outer membrane. (B) Enlarged part of Fig. 7A showing body scales (BS) on the outer membrane of the cell. (C) Lateral view showing the epicone (EC), longitudinal flagellum (LF), transverse flagellum (TF), and hypocone (HC). (D) Enlarged part of Fig. 7C showing flagellar scales (FS) on the LF. (E) Lateral view showing a cell with the outer membranes (OM) partially removed. (F) Enlarged part of Fig. 7E showing a thin plate (TP) layer, OM, and BS. Scale bars represent: A & C, 1 μm; E, 2 μm; B, D & F, 200 nm.
  • [Fig. 8.] Micrographs of the Korean strains of Amphidinium massartii AMJJ1 taken using transmission electron microscopy. (A) Longitudinal section showing several organelles inside the protoplasm. PY, pyrenoid; PU, pusule, TR, trichocyst; GB, Golgi body; CP, chloroplast; MI, mitochondrion; NU, nucleus; ST, starch. (B) Enlarged part of Fig. 8A showing PU. (C) Enlarged part of Fig. 8A showing TR. (D) Transverse section showing PY and NU. Scale bars represent: A, 2 μm; B & C, 200 nm; D, 1 μm.
    Micrographs of the Korean strains of Amphidinium massartii AMJJ1 taken using transmission electron microscopy. (A) Longitudinal section showing several organelles inside the protoplasm. PY, pyrenoid; PU, pusule, TR, trichocyst; GB, Golgi body; CP, chloroplast; MI, mitochondrion; NU, nucleus; ST, starch. (B) Enlarged part of Fig. 8A showing PU. (C) Enlarged part of Fig. 8A showing TR. (D) Transverse section showing PY and NU. Scale bars represent: A, 2 μm; B & C, 200 nm; D, 1 μm.
  • [Fig. 9.] The global distribution of Amphidinium massartii. Closed stars indicate sampling locations of A. massartii strains for which both DNA sequences and morphology have been reported. Open stars indicate sampling locations of A. massartii strains for which only morphology has been reported.
    The global distribution of Amphidinium massartii. Closed stars indicate sampling locations of A. massartii strains for which both DNA sequences and morphology have been reported. Open stars indicate sampling locations of A. massartii strains for which only morphology has been reported.