https://orcid.org/0000-0001-5061-9029
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Abstract
Recent molecular phylogenies that include species of Parvodinium revealed as its closest relatives the genera Peridiniopsis, Palatinus and Johsia. The clade containing these taxa is currently recognized as a family, Peridiniopsidaceae. The affinity between the members of Peridiniopsidaceae cuts across traditional boundaries based on features of the amphiesma, most notably the presence or absence of an apical pore complex. Detailed descriptions of the fine structure of Peridiniopsis and Palatinus are available from TEM studies of their type species. Here we provide a description in comparable detail of a species of the Parvodinium umbonatum–inconspicuum complex, which includes the type of the genus. The cells had an apical fibrous complex essentially similar to those described from other peridinioids prepared with comparable fixations. The pusular system was extensive and included areas with different aspects: an area with a sheet-like vesicle along the mid-right side of the cell, a ventral portion with ramified and anastomosed tubes and a somewhat flattened tube attached to the transverse flagellar canal. The most remarkable feature was the microtubular strand that extended from a ventral, protruding peduncle to the anterior part of the epicone, around an accumulation body, and came around along a more dorsal position toward the ventral side. This long microtubular strand of the peduncle (MSP) was reminiscent of the one described from Peridiniopsis borgei, both by its extension and looping path, and by the breaking up of the strand of microtubules into smaller portions with a wavy appearance; and contrasted with the reduced MSP of Palatinus apiculatus. The fine-structural features currently known from Peridiniopsidaceae are summarized. Members of the family include a flagellar apparatus with four microtubule-containing roots associated, the basal bodies inserted close to each other, nearly at right angles and a three-armed fibrous connective between root 1 and the transverse basal body.
HIGHLIGHTS
Detailed fine structure of Parvodinium (of P. umbonatum–P. inconspicuum complex).
Comparative analysis of the ultrastructure of Parvodinium and other Peridiniopsidaceae.
Summary of ultrastructural features of the family Peridiniopsidaceae.
Acknowledgments
Thanks to the Laboratory of Molecular Studies for Marine Environments (LEMAM), where the molecular work was done.
Disclosure statement
No potential conflict of interest was reported by the authors.
Supplementary information
The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2022.2091798
Supplementary figs S1–S4. LM and SEM of Parvodinium elpatiewskyi strain from Gafanha da Boavista, Ílhavo. Supplementary fig. S1. Ventral view of a living cell (LM). Nucleus (n), eyespot (e) and radiating chloroplast lobes (ch). Supplementary figs S2, S3. Superficial and deeper focus, from ventral to dorsal view, of an empty theca (LM). Supplementary fig. S4. Apical view of a cell showing the cingulum (c), the apical pore complex (apc) and plates marked in Kofoidean notation (SEM). Cells for SEM observation were fixed for 2 h 30 min in a mixture of 1:1 culture volume and 50% ethanol. Scale bars: Supplementary figs S1–S3, 10 mm; Supplementary fig. S4, 5 mm.
Supplementary figs S5–S7. Parvodinium strain from Buçaco, TEM. Supplementary fig. S5. Longitudinal section of a cell seen from the right-ventral side showing the chloroplast lobes (ch) with some thylakoid-free areas (short black arrows), oil droplets (O), starch grains (st) and trichocysts (t), scattered in the cell periphery. The eyespot (e) is visible in the sulcal region near pusular elements (pu). An almost transverse section of a peduncle (long black arrow) is present outside the cell. Supplementary fig. S6. Magnification of the peduncle displaying a strand of microtubules (thin arrows), and some electron-opaque vesicles (larger arrows). Supplementary fig. S7. Magnification of the eyespot-containing chloroplast lobe with two rows of globules (arrows) with the longitudinal microtubular root (LMR/r1) in the ventral side. Scale bars: Supplementary fig. S5, 2 mm; Supplementary figs S6, S7, 500 nm.
Supplementary figs S8–S11. Parvodinium strain from Buçaco, TEM. Longitudinal serial sections through the apical pore complex, viewed from the right-ventral side of the cell. Slanted numbers indicate the section number in the series. Supplementary figs S8, S9. Several striated fibers (long arrows) and a round vesicle (short arrow) are seen under the pore plate (Po). The cover plate (cp) is seen on top of the Po. Supplementary figs S10, S11. Several round and elongated vesicles (short arrows) extend under the Po and converge toward the cp. Scale bars: 500 nm.
Supplementary figs S12–S16. Parvodinium strain from Buçaco, TEM. Pusular system and microtubular strand of the peduncle (MSP) in longitudinal serial sections proceeding toward the left-dorsal side, seen from the right-ventral side. Slanted numbers indicate the section number in the series. Supplementary figs S12, S13. The path of the MSP, breached up in several rows of microtubules and marked by arrows, is shown in two sections, the second one, 47 sections towards the left-dorsal side of the cell. In Supplementary fig. S12 the rows of microtubules are closer together and near the network of pusular tubes (PuN). The short arrow points to the apical pore. In Supplementary fig. S13 some rows are visible further up in the epicone, near an accumulation body (ab), while a single row of microtubules is present in the ventral area, near the PuN; the flat pusular vesicle (PuS) is visible on the right side of the cell. Supplementary fig. S14. Magnification of the microtubules and PuN from Supplementary fig. S12. Supplementary figs S15, S16. Magnification from Supplementary fig. S13, of four strands (marked 1–4) of microtubules visible near the ab (Supplementary fig. S15) and the microtubules in the ventral area (Supplementary fig. S16). Electron-opaque bodies are marked by short arrows (Supplementary fig. S15). c, cingulum; O, oil droplets; PuS, pusular sheet; s, sulcus; st, starch grains. Scale bars: Supplementary figs S12, S13, 5 mm; Supplementary figs S14–S16, 500 nm.
Supplementary Figs S17–S19. Parvodinium strain from Buçaco, TEM. Pusular system and microtubular strand of the peduncle (MSP); continuation of the series of sections shown in Figs 24, 25. Supplementary fig. S17. General view showing the descending path of the microtubular strand of the peduncle after inflecting to the left side of the cell (thin arrows). The pusular network (PuN) and pusular sheet (PuS) are visible on the ventral-right side of the cell. A transverse section through a detached peduncle (short arrow) is visible outside the cell, on the ventral side, near the sulcus (s). Supplementary fig. S18. Magnification of Supplementary fig. S17 showing four rows of microtubules from the MSP and electron-opaque bodies (short arrows). Supplementary fig. S19. Magnification of the PuS from Supplementary fig. S17 containing electron-opaque bodies (black arrows) and a tubular portion with dot-like contents reminiscent of the pusular tube associated with the TFC (white arrow). c, cingulum; e, eyespot; O, oil droplets; s, sulcus; st, starch grains. Scale bars: Supplementary fig. S17, 5 mm; Supplementary figs S18, S19, 500 nm.
Supplementary Fig. S20. Concatenated phylogeny based on 3923 base pairs of large subunit rDNA, internal transcribed spacers, 5.8S rDNA and small subunit rDNA of 12 genera of Dinophyceae (27 sequences) and inferred from Bayesian analysis. For this analysis Heterocapsa spp. were used as outgroup taxa. Branch support was evaluated from posterior probabilities (probabilities (PP ≥ 0.5) from Bayesian analyses and bootstrap (1000 replications, BS ≥ 50%) from maximum likelihood analyses, respectively. These support values are written at internodes. A hyphen (-) indicates values below 0.5 for PP and 50% for bootstrap. GenBank accession numbers are written after the species epithet. Sequences determined in this study were bold faced. The branch lengths are proportional to the number of character changes, see scale bar below the phylogenetic tree.
Author contributions
M.S. Pandeirada: LM, TEM and SEM preparation and analysis, molecular analyses, drafting manuscript; S.C. Craveiro: TEM preparation, molecular analyses, drafting manuscript; N. Daugbjerg: phylogenetic analyses, drafting and editing manuscript; Ø. Moestrup: editing manuscript; A.J. Calado: original concept, TEM analysis, editing manuscript.