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Article

Morphological and Molecular Characterization of the Unarmored Dinoflagellate Gymnodinium trapeziforme (Dinophyceae) from Jiaozhou Bay, China

by
Menghan Gao
1,2,
Zhangxi Hu
1,2,3,4,*,
Zhaohe Luo
5,
Yunyan Deng
3,4,
Lixia Shang
3,4,
Yuanyuan Sun
6 and
Yingzhong Tang
3,4,*
1
College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China
2
Guangdong Laboratory of Marine Ecology Environment Monitoring and Warning, Zhanjiang 524088, China
3
CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
4
Functional Laboratory of Marine Ecology and Environmental Science, Laoshan Laboratory, Qingdao 266237, China
5
Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China
6
CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
*
Authors to whom correspondence should be addressed.
Diversity 2023, 15(12), 1186; https://doi.org/10.3390/d15121186
Submission received: 30 October 2023 / Revised: 25 November 2023 / Accepted: 26 November 2023 / Published: 29 November 2023
(This article belongs to the Special Issue Diversity of Phytoplankton and Their Associated Microbiomes in the Changing Marine Environment)
Browse Figures
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Abstract

:
The genus Gymnodinium contains more than 230 extant species, approximately 30% of which have not been reported since their original description. Approximately eight Gymnodinium species have been reported or described in the coastal waters of China. This work reports the presence of Gymnodinium trapeziforme from Jiaozhou Bay, China, in 2020, and its morphological and phylogenetic characterization by using light and scanning electron microscopy and systematic analysis based on partial LSU rDNA sequences. We observed the typical diagnostic features of G. trapeziforme, including a small size, biconical to ovoid shape, and a sulcal extension intruded to the epicone and connected to the horseshoe-shaped apical structure complex (ASC). Additionally, we firstly observed that the ASC consisted of three parallel series of vesicles, with the central one possessing knobs, and having more than 10 amphiesmal vesicles within the ASC. The nucleus was cucurbit-shaped, and the amphiesmal vesicles covering the cell surface, which would be peeled off for the cells in stress. While our molecular phylogeny inferred with the maximum likelihood (ML) and Bayesian inference (BI) confirmed the conspecificity of our isolate with the holotype G. trapeziforme (accession No. EF192414), we found a difference of 14 bases in the D1–D6 domains of the LSU rDNA sequences between the two entities, which indicates a detectable speciation of the two populations. Our work provides a detailed morphological and molecular characterization of G. trapeziforme that was isolated from the coastal water of China, which also broadens the geographical distribution of this species.

1. Introduction

Dinoflagellate diversity has been estimated at about 2400 species belonging to 259 genera [1,2], and the numbers of species and genera are continuously growing as more novel taxa have been identified and described [3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19]. These species play essential roles in the ecosystem as important primary producers. Among them, many unarmoured dinoflagellates have been classified into the genus Gymnodinium F. Stein, established by Stein [20], which originally consisted of gymnodinioid species with a cingulum displacement less than 20% of the cell length [21], and was one of the largest dinoflagellate genera [22]. Takayama [23] found that the apical groove was present in many unarmoured species. Later, more dinoflagellate taxonomists found that the apical structure complex (syn. acrobase, apical groove) was a valuable taxonomic characteristic by which to differentiate unarmoured species [24,25,26,27,28].
For a long period, the taxonomic system of Gymnodinium has remained almost unchanged. Daugbjerg et al. [24] proposed three major morphological criteria for characterizing this important genus: nuclear chambers (NC), a nuclear fibrous connective (NFC), and an apical structure complex running in a counterclockwise direction around the apex. Based on these criteria, they redefined the genera Gymnodinium and Gyrodinium Kofoid & Swezy and erected the genera Akashiwo G. Hansen & Moestrup, Karenia G. Hansen & Moestrup, and Karlodinium J. Larsen. Subsequently, many new related genera have been erected, e.g., Paragymnodinium Kang, Jeong, Moestrup & Shin [29], Barrufeta N. Sampedro & S. Fraga [30], Gyrodiniellum N.S. Kang, H.J. Jeong & Moestrup [31], Levanderina (Levander) Ø. Moestrup, P. Hakanen, G. Hansen, N. Daugbjerg & M. Ellegaard [26], and Wangodinium Z. Luo, Zhangxi Hu, Yingzhong Tang & H.F. Gu [10]. Thessen et al. [22] conducted an extensive literature review and reported that there are 234 extant Gymnodinium species, and approximately 30% of them have never been recorded since their initial descriptions. These species, which are referred to as “oncers”, may be rare species, with very limited geographical distributions, or species in tightly defined niches. Therefore, discovery and quantification of the “oncers” of Gymnodinium may help to identify more morphological characteristics and increase the biodiversity of phytoplankton in the investigating area.
More than 350 dinoflagellate species have been observed, reported, or described in China [10,11,12,32,33,34,35], many of which currently lack morphological descriptions or molecular sequences [36]. So far, eight Gymnodinium species have been recorded in Chinese coastal waters. Gymnodinium catenatum H.W. Graham [37], G. dorsalisulcum (Hulburt, J.J.A. McLaughlin & Zahl) Shauna Murray, Salas & Hallegraeff [10], G. impudicum (S. Fraga & I. Bravo) Gert Hansen & Moestrup [10], G. inusitatum H. Gu [37], and G. microreticulatum C.J.S. Bolch & G.M. Hallegraeff [37] have been characterized based on their morphologies and molecular sequences, which undoubtedly confirmed the presence of the five Gymnodinium species in the coastal waters of China. In addition, the presence of G. aureolum (Hulburt) Gert Hansen [38], Gymnodinium cf. nolleri M. Ellegaard & Moestrup [39], and G. smaydae N.S. Kang, H.J. Jeong & Ø. Moestrup [40] in Chinese coastal waters has also been confirmed via high-throughput metabarcoding sequencing, however, the other two recorded species, G. bei H.J. Spero [39] and G. heterostriatum Kofoid & Swezy [39], have been reclassified as Pelagodinium bei (H.J.Spero) Siano, Montresor, Probert & Vargas, and Gyrodinium heterostriatum (Kofoid & Swezy) F. Gómez, Artigas & Gast. Most recently, we established a clonal culture of Gymnodinium species from the coastal water of Jiaozhou Bay, China in 2020, which provided further characterization of its morphology using light, scanning electron microscopy, and phylogenetic analysis based on partial LSU rDNA sequence. The identity of the isolate was confirmed as Gymnodinium trapeziforme Attaran-Fariman & Bolch, and here, we present the details of our characterization.

2. Materials and Methods

2.1. Sampling and Culture Establishment

A strain of Gymnodinium trapeziforme (strain JZBC3-2020-13) was isolated from a water sample collected at the coast of Qingdao, Shandong province, China (36.10° N, 120.25° E) in September 2020. The culture was maintained in natural seawater (with a salinity of 31) enriched with f/2-Si medium [41] at 21 °C, and 12:12 h light–dark at approximately 100 μmol quanta m−2 s−1 supplied by white fluorescent lights. An antibiotics solution (10,000 I.U. penicillin and 10,000 μg mL−1 streptomycin; Solarbio, Beijing, China) was added into the medium immediately before inoculation (final concentration 2%) to inhibit bacterial growth.

2.2. Light Microscopy

Live cells were observed and photographed with light microscopes (BX53 and IX73, Olympus, Tokyo, Japan) equipped with a DP80 digital camera (Olympus, Tokyo, Japan). For epifluorescence microscopy, cells were stained with SYBR Green (Solarbio, Beijing, China), viewed and photographed for chlorophyll-induced red autofluorescence and SYBR Green-induced green nuclear fluorescence. Cell sizes of G. trapeziforme for 50 live cells at the mid-exponential growth phase were measured at ×200 magnification using a DP80 digital camera (Olympus, Tokyo, Japan).

2.3. Scanning Electron Microscopy (SEM)

For SEM, specimens were prepared according to the method described by Hu et al. [34]. Specifically, cells in the mid-exponential growth stage were fixed in 2% OsO4 solution (final concentration) made up in natural seawater for 40–50 min at room temperature. Fixed cells were then gently filtered onto 11 μm pore size Millipore nylon membrane and dehydrated in an acetone series (10%, 30%, 50%, 70%, 90%, and three times in 100%, 15 min for each step). After that, cells were dried using a critical point dryer with liquid CO2 (EM CPD300, Leica, Vienna, Austria), and coated with platinum–palladium (EM ACE200, Leica, Vienna, Austria). The cells were observed using an S-3400N SEM (Hitachi, Hitachinaka, Japan) at 5-kV accelerating voltages.

2.4. DNA Extraction, PCR Amplification, and Sequencing

Genomic DNA of Gymnodinium trapeziforme (strain JZBC3-2020-13) was extracted using a Tiangen plant extraction kit (Beijing, China) following the manufacturer’s protocol. Approximately 1500 bp of 28S (large subunit [LSU]) rDNA (D1–D6) was amplified using primer pair D1R (forward, 5′-ACCCGCTGAATTTAAGCATA-3′) [42] and 28-1483R (reverse, 5′-GCTACTACCACCAAGATCTGC-3′) [24]. Polymerase chain reaction (PCR) reactions were conducted using a PCR Master Cycler nexus gradient (Eppendorf, Hamburg, Germany), and performed with a final volume of 25 μL, containing 9.5 μL ddH2O, 12.5 μL 2 × Taq PCR MasterMix, 1 μL of each PCR primer (10 mM), and 1 μL of the DNA template. The thermal condition of PCR was as follows: an initial denaturation at 94 °C for 5 min, 35 cycles at 94 °C for 20 s, 55 °C for 30 s, and 72 °C for 2 min, and a final elongation step of 10 min at 72 °C. The amplification was confirmed by 1% agarose gel electrophoresis and visualized with ultraviolet light. The PCR product was purified using an agarose gel DNA fragment purification kit (GENEray Biotechnology, Shanghai, China) following the protocol, ligated with pMD18-T cloning vector (TaKaRa, Tokyo, Japan) and then sequenced (Sangon, Shanghai, China). DNA sequence determined in this study was deposited in GenBank with accession number ON399089.

2.5. Phylogenetic Analyses

The newly obtained LSU rDNA sequence was incorporated into those of closely related species available in the GenBank and those of outgroup taxa were first aligned using MAFFT v7.511 [43] online program (http://mafft.cbrc.jp/alignment/server/; accessed on 21 October 2023) with default settings, and alignments were manually checked with BioEdit v7.2.5 [44]. The final alignments of the LSU sequences of G. trapeziforme consisted of 39 taxa and contained 1000 positions (including gaps introduced from alignment), and the sequences of Alexandrium leei (AY959942) and Alexandrium taylorii (AB607263) were used as the outgroups, respectively. The program jModelTest 2.1.4 was used to select the most appropriate model of molecular evolution with Akaike information criterion (AICc) [45], model TrN + G was selected as the best-fit model for the LSU rDNA dataset of G. trapeziforme. Phylogenetic trees were constructed using Bayesian inference (BI) and maximum likelihood (ML) analyses. Bayesian inference (BI) was performed with MrBayes 3.2.6 [46] with the best-fitting substitution model (TrN + G). Four independent Markov chain Monte Carlo simulations were run simultaneously for 10,000,000 generations and trees were sampled every 1000 generations. The first 10% trees were discarded as burn-in. The convergence was judged based on the average standard deviation of split frequencies (all less than 0.01). The remaining trees were used to generate a consensus tree and calculate the posterior probabilities of all branches using a majority-rule consensus approach. Maximum likelihood (ML) analyses were conducted with raxmlGUI v1.3.1 [47,48] using the model GTR + G (the model GTR + G ranked second, and the score of this model was close to model TrN + G).) Node support was assessed with 1000 bootstrap replicates. FigTree (v1.4.4) was used to view and edit trees for publication.

3. Results

3.1. Morphology

The vegetative cells of Gymnodinium trapeziforme were biconical to ovoid, 24.4–38.9 µm (31.6 ± 3.0 µm, n = 50) in length, and 19.0–29.8 µm (24.3 ± 3.1 µm) in width (Figure 1 and Figure 2). Many amphiesmal vesicles (AVs) of different shapes (polygonal or rectangular) covered the cell surface (Figure 2). The hypocone was slightly larger than the epicone (Figure 1 and Figure 2), the epicone was conical, and the hypocone was hemispherical to round (Figure 1 and Figure 2). The cingulum was wide, deeply incised, and made a displacement approximately one cingular width (Figure 2a). The sulcus was wider below the end of the cingulum than between the two ends of the cingulum (Figure 1a,b and Figure 2a). The sulcal extension intruded to the epicone and its end connected to the apical structure complex (ASC, Figure 2a). The ASC was horseshoe-shaped, consisting of three parallel series of vesicles, the central one possessing knobs (Figure 1a,e–i). There were more than 10 AVs within the ASC, and their morphology was similar to the ones in the epicone and hypocone (Figure 1e–i). The nucleus was large, and cucurbit shaped (Figure 1h,i). Numerous yellow-brown and irregular to ribbon-like chloroplasts distributed peripherally (Figure 1a,c,g,h). A red-orange accumulation body was observed in the hypocone or just below the cingulum of some cultures (Figure 1d). Amphiesmal vesicles peeled off the cell surface when culture was transferred to fresh medium or in stress (Figure 1e,f). A diagrammatic reconstruction of G. trapeziforme is presented in Figure 3.

3.2. Phylogeny

We compared our 1509 bp LSU rDNA sequence (accession No. ON399089) of G. trapeziforme with other Gymnodiniaceae species and found that it was 98.7% (926 b/938 bp) identical to the holotype sequence of G. trapeziforme (EF192414), while it was 82.1–95.5% identical to Gymnodinium spp., 85.5% (882 bp/1032 bp) to Lepidodinium chlorophorum (Elbrächter & Schnepf) Gert Hansen, Botes & Salas (AY331681), 85.5% (508 bp/594 bp) to Wangodinium sinense Z. Luo, Zhangxi Hu, Yingzhong Tang & H.F. Gu (MH732681), 79.9% (591 bp/740 bp) to Barrufeta bravensis N. Sampedro & S. Fraga (FN647674), 83.0% (356 bp/429 bp) to Levanderina fissa (Levander) Moestrup, Hakanen, Gert Hansen, Daugbjerg & M. Ellegaard (EF192407), and 86.3% (341 bp/395 bp) to Akashiwo sanguinea (K. Hirasaka) Gert Hansen & Moestrup (AF260397), respectively, in GenBank (Table 1), indicating our isolate is conspecific to G. trapeziforme (EF192414). However, there was a difference of 14 base pairs between them, in which 3 bases were in the D2 domain of the LSU rDNA sequences (Figure 4). There were nine degenerate bases (H (A/C/T), W (A/T), N (A/T/C/G), S (G/C), V (G/A/C), and Y (C/T)) in the holotype sequence of G. trapeziforme (EF192414), indicating they might be 25%, 33%, or 50% identical to the corresponding positions of our sequences (ON399089) (Figure 4).
Phylogenetic analyses using maximum likelihood (ML) and Bayesian inference (BI) generated similar trees based on LSU rDNA sequences (Figure 5). The Gymnodiniaceae clade comprised Gymnodinium, Lepidodinium Watanabe, Suda, Inouye, Sawaguchi & Chihara, Wangodinium, Barrufeta, and Akashiwo (Figure 5). The two entities of G. trapeziforme from China (ON399089) and Iran (EF192414) formed a coherent clade with maximal support (100 BS/1.00 PP), and this clade branched together with other Gymnodiniaceae species (Figure 5).

4. Discussion

The genus Gymnodinium was characterized based on the following morphological traits: lacking a theca, a cingulum displacement less than 20% of the cell length, a horseshoe-shaped apical groove, a nuclear envelope with vesicular chambers, and a nuclear fibrous connective (NFC) [21,24,49,50,51,52,53]. Our isolate has the typical characteristics of Gymnodinium: it lacks a theca, the cingulum creates a displacement approximately one cingular width (less than 20% of the cell length), the sulcal extension intrudes to the epicone, and its end connects to the horseshoe-shaped apical structure complex (ASC), and is 98.7% identical to the entity of G. trapeziforme (EF192414), the type material of G. trapeziforme. In addition, it has a small size and is bi-conical to ovoid outline contour. Together, these attributes lead us to conclude that our isolate is conspecific with the entity annotated as G. trapeziforme.
Gymnodinium trapeziforme was described by Attaran-Fariman et al. [54], and the general cell characteristics of this species are very similar to a variety of other small cell-sized photosynthetic gymnodinoid dinoflagellates [24,50,51,55,56], in which G. trapeziforme differentiated G. microreticulatum, G. nolleri, G. catenatum, and G. aureolum mainly in terms of the cingulum displacement, morphologies of nucleus and resting cysts, and color of accumulation body [51,54]. Additionally, we first observed the fine structure of ASC, which consisted of three rows of vesicles in G. trapeziforme, and within the ASC, there were more than 10 amphiesmal vesicles, which is very similar to the ASC observed in G. catenatum [57], Kirithra asteri Boutrup, Tillmann, Daugbjerg & Moestrup [9], Kirithra sigma Z.X. Hu, Zhun Li, H.H. Shin & Y.Z. Tang [12], Levanderina fissa [26], and Torquentidium flavescens (Kofoid & Swezy) H.H. Shin, Zhun Li & Matsuoka [58]. We also observed that the nucleus was cucurbit-shaped, which is different from the observations made by Attaran-Fariman et al. [54]. The new observed morphological information will help us to better identify this species.
Vegetative cells of G. trapeziforme have rarely been reported after its initial description; however, its resting cysts have been recorded in the southeast coast of Iran [59,60], the Cap Blanc (NW Africa) and Gotland Basin (Baltic Sea) [61], and the upper Gulf of California, Mexico [62], which indicates that G. trapeziforme is distributed in a very limited number of regions or is difficult to identify accurately. In 2020, we isolated a strain of G. trapeziforme from Jiaozhou Bay, China, where the phytoplankton community has been intensively investigated in the past 40 years [38]; however, vegetative cells and resting cysts of G. trapeziforme have not been recorded there in the literature or in public reports [36,63,64,65,66]. We confirm that this is the first record and report of G. trapeziforme in China coasts [36,63,64,65,66], which indicates that this species is present in very low abundance or is an alien species. The molecular data obtained in this study also confirmed the presence of G. trapeziforme in the Jiaozhou Bay, China, based on a 1509-bp LSU rDNA sequence analysis and the phylogenetic inference of the strain JZBC3-2020-13. The phylogenetic tree inferred from LSU rDNA sequences shows that our strain of G. trapeziforme forms a coherent with the strain GYPC102 reported from Iran (Figure 5; [54]), and they are closely related to G. microreticulatum, G. nolleri, and G. catenatum, which is in accordance with the result of Attaran-Fariman et al. [54]. However, there are 14 bases difference between them, which indicates a detectable speciation of the two populations. In conclusion, the combinations of features, such as the general morphology, morphology of ASC, and the phylogeny, led us to confirm that G. trapeziforme is distributed on the Chinese coast.

5. Conclusions

Together, our morphological observations and phylogenetic analyses confirmed the presence of G. trapeziforme in the coastal water of China, which broadens the geographical distribution of G. trapeziforme in the world. We also identified more morphological characteristics of G. trapeziforme: the ASC consists of three parallel series of vesicles, the central one possessing knobs, and the nucleus is cucurbit-shaped.

Author Contributions

Conceptualization, Z.H. and Y.T.; methodology, Z.H. and Y.S.; software, M.G. and Z.H.; validation, M.G., Z.H., Z.L., Y.D., L.S., Y.S. and Y.T.; formal analysis, M.G., Z.L. and Z.H.; investigation, M.G., Z.H., Z.L., Y.D., L.S., Y.S. and Y.T.; resources, Z.H. and Y.T.; data curation, M.G., Z.H., Z.L., Y.D., L.S., Y.S. and Y.T.; writing—original draft preparation, M.G. and Z.H.; writing—review and editing, M.G., Z.H., Z.L., Y.D., L.S., Y.S. and Y.T.; supervision, Z.H. and Y.T.; project administration, Z.H. and Y.T.; funding acquisition, Z.H. and Y.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Science & Technology Basic Resources Investigation Program of China, grant number 2018FY100200, the National Natural Science Foundation of China, grant number 41976134, the Program for Scientific Research Start-up Funds of Guangdong Ocean University, grant numbers 060302022201 and R17039, the Undergraduate Student Innovation and Entrepreneurship Training Program Project (S202210566010), and the Undergraduate Innovation Team of Guangdong Ocean University (CXTD2023002).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors greatly appreciate the constructive advice of the anonymous reviewers.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Micrographs (LM) of Gymnodinium trapeziforme strain JZBC3-2020-13. (a) surface of ventral view showing sulcus, cingulum and chloroplast (red arrow); (b) right ventro-lateral view showing sulcus, cingulum and longitudinal flagellum (lf); (c) surface focus of dorsal view showing cingulum, transverse flagellum (tf, black arrow) and chloroplast (red arrow); (d) surface focus of dorsal view showing an accumulation body (black arrowhead); (e) dorsal view showing the amphiesmal vesicles (yellow arrow) outside of the cell; (f) dorsal view showing the amphiesmal vesicles (yellow arrow) peeling off the cell surface; (g–i) bright-field and epifluorescence light microscopy observation on the same vegetative cell showing numerous yellow-brown and irregular to ribbon-like chloroplasts (red arrow) and a cucurbit-shaped nucleus (N) occupying one-third of the whole cell. Scale bars = 20 μm.
Figure 1. Micrographs (LM) of Gymnodinium trapeziforme strain JZBC3-2020-13. (a) surface of ventral view showing sulcus, cingulum and chloroplast (red arrow); (b) right ventro-lateral view showing sulcus, cingulum and longitudinal flagellum (lf); (c) surface focus of dorsal view showing cingulum, transverse flagellum (tf, black arrow) and chloroplast (red arrow); (d) surface focus of dorsal view showing an accumulation body (black arrowhead); (e) dorsal view showing the amphiesmal vesicles (yellow arrow) outside of the cell; (f) dorsal view showing the amphiesmal vesicles (yellow arrow) peeling off the cell surface; (g–i) bright-field and epifluorescence light microscopy observation on the same vegetative cell showing numerous yellow-brown and irregular to ribbon-like chloroplasts (red arrow) and a cucurbit-shaped nucleus (N) occupying one-third of the whole cell. Scale bars = 20 μm.
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Figure 2. SEM micrographs of Gymnodinium trapeziforme strain JZBC3-2020-13. (a) ventral view showing longitudinal and transverse flagella in sulcus and cingulum, respectively, sulcal intrusion connecting with apical structure complex, and displacement of cingulum; (b) dorsal view showing wide cingulum and amphiesmal vesicles on cell surface; (c) antapical–dosal view showing cingulum, and amphiesmal vesicles on cell surface; (d) antapical view showing amphiesmal vesicles on cell surface; (e) apical view showing apical structure complex; (f) apical–dosal view showing apical structure complex; (g,h) ventral view showing details of apical structure complex from one cell at different magnifications. (i) ASC is composed of three rows of vesicles: white arrow, upper row; yellow arrow, central row; black arrow, lower row. Within the ASC there are approximately 14 amphiesmal vesicles (yellow asterisks). Scale bars for (a–d) = 10 μm, (e–i) = 5 μm.
Figure 2. SEM micrographs of Gymnodinium trapeziforme strain JZBC3-2020-13. (a) ventral view showing longitudinal and transverse flagella in sulcus and cingulum, respectively, sulcal intrusion connecting with apical structure complex, and displacement of cingulum; (b) dorsal view showing wide cingulum and amphiesmal vesicles on cell surface; (c) antapical–dosal view showing cingulum, and amphiesmal vesicles on cell surface; (d) antapical view showing amphiesmal vesicles on cell surface; (e) apical view showing apical structure complex; (f) apical–dosal view showing apical structure complex; (g,h) ventral view showing details of apical structure complex from one cell at different magnifications. (i) ASC is composed of three rows of vesicles: white arrow, upper row; yellow arrow, central row; black arrow, lower row. Within the ASC there are approximately 14 amphiesmal vesicles (yellow asterisks). Scale bars for (a–d) = 10 μm, (e–i) = 5 μm.
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Figure 3. Diagrammatic reconstructions of Gymnodinium trapeziforme. (a) ventral view. (b) dorsal view. (c) detail of the apical structure complex (ASC).
Figure 3. Diagrammatic reconstructions of Gymnodinium trapeziforme. (a) ventral view. (b) dorsal view. (c) detail of the apical structure complex (ASC).
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Figure 4. Sequence variation in the partial LSU rDNA sequences among G. trapeziforme strains JZBC3-2020-13 (ON399089) and GYPC102 (EF192414).
Figure 4. Sequence variation in the partial LSU rDNA sequences among G. trapeziforme strains JZBC3-2020-13 (ON399089) and GYPC102 (EF192414).
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Figure 5. Phylogeny of Gymnodinium trapeziforme and other Gymnodiniaceae species inferred from partial large subunit rDNA (LSU rDNA) sequences using maximum likelihood (ML) with Alexandrium leei Balech (AY959942) and A. taylorii Balech (AB607263) as outgroups. New sequence of G. trapeziforme (ON399089) is indicated in bold. Numbers on branches are statistical support values to clusters to their right (ML bootstrap support/Bayesian posterior probability). Bootstrap values > 50% and posterior probabilities > 0.5 are shown. Solid dots indicate maximal support (ML bootstrap support: 100/Bayesian posterior probability: 1.00).
Figure 5. Phylogeny of Gymnodinium trapeziforme and other Gymnodiniaceae species inferred from partial large subunit rDNA (LSU rDNA) sequences using maximum likelihood (ML) with Alexandrium leei Balech (AY959942) and A. taylorii Balech (AB607263) as outgroups. New sequence of G. trapeziforme (ON399089) is indicated in bold. Numbers on branches are statistical support values to clusters to their right (ML bootstrap support/Bayesian posterior probability). Bootstrap values > 50% and posterior probabilities > 0.5 are shown. Solid dots indicate maximal support (ML bootstrap support: 100/Bayesian posterior probability: 1.00).
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Table 1. Comparisons in the rDNA sequences between Gymnodinium trapeziforme (1509 bp, GenBank accession No. ON399089) and that of the type specimen and other species in Gymnodiniaceae in NCBI database.
Table 1. Comparisons in the rDNA sequences between Gymnodinium trapeziforme (1509 bp, GenBank accession No. ON399089) and that of the type specimen and other species in Gymnodiniaceae in NCBI database.
SpeciesGenBank Accession NumberIdentityOrigin
G. trapeziformeEF19241498.7% (926/938)Pasabander, South coast of Iran
G. fuscum (Ehrenberg) F. SteinAF20067682.9% (819/988)La Trobe, Australia
G. fuscum var. rubrum Baumeister ex C.Romeikat, J. Knechtel & M. GottschlingMK40548985.5% (1260/1473)Seeon, Traunstein, Germany
G. microreticulatum ON39235694.6% (1427/1508)Yellow Sea, China
G. catenatum AY03607384.5% (594/703)Australia
G. inusitatum KF23407184.7% (609/719)Lianyungang, China
G. smaydae HG00513584.0% (771/918)Shiwha Bay, Korea
G. venator Flo Jørgensen & Shauna MurrayAY45568182.1% (1212/1477)-
G. plasticum KY68818495.5% (734/769)Plastic Lake, Canada
G. aureolum AF20067084.5% (843/998)Pettaquamscutt R., USA
G. corollarium A.M. Sundström, Kremp & DaugbjergFJ21138688.3% (1217/1378)Northern Baltic proper, Baltic Sea, Sweden
Levanderina fissa EF19240783.0% (356/429)-
Akashiwo sanguinea AF26039786.3% (341/395)-
Barrufeta bravensis FN64767479.9% (591/740)La Fosca, Cataluña
Lepidodinium chlorophorum AY33168185.5% (882/1032)-
Wangodinium sinense MH73268185.5% (508/594)Beihai, South China Sea, China
Note: “-” indicates not available.
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Gao, M.; Hu, Z.; Luo, Z.; Deng, Y.; Shang, L.; Sun, Y.; Tang, Y. Morphological and Molecular Characterization of the Unarmored Dinoflagellate Gymnodinium trapeziforme (Dinophyceae) from Jiaozhou Bay, China. Diversity 2023, 15, 1186. https://doi.org/10.3390/d15121186

AMA Style

Gao M, Hu Z, Luo Z, Deng Y, Shang L, Sun Y, Tang Y. Morphological and Molecular Characterization of the Unarmored Dinoflagellate Gymnodinium trapeziforme (Dinophyceae) from Jiaozhou Bay, China. Diversity. 2023; 15(12):1186. https://doi.org/10.3390/d15121186

Chicago/Turabian Style

Gao, Menghan, Zhangxi Hu, Zhaohe Luo, Yunyan Deng, Lixia Shang, Yuanyuan Sun, and Yingzhong Tang. 2023. "Morphological and Molecular Characterization of the Unarmored Dinoflagellate Gymnodinium trapeziforme (Dinophyceae) from Jiaozhou Bay, China" Diversity 15, no. 12: 1186. https://doi.org/10.3390/d15121186

APA Style

Gao, M., Hu, Z., Luo, Z., Deng, Y., Shang, L., Sun, Y., & Tang, Y. (2023). Morphological and Molecular Characterization of the Unarmored Dinoflagellate Gymnodinium trapeziforme (Dinophyceae) from Jiaozhou Bay, China. Diversity, 15(12), 1186. https://doi.org/10.3390/d15121186

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