Evolution of Thoracosphaeroideae (Peridiniales, Dinophyceae) and a case of atavism in taxonomically clarified Chimonodinium lomnickii var. wierzejskii from the Polish Tatra Mountains

ABSTRACT

Character evolution in calcareous dinophytes and their relatives is poorly understood at present, particularly regarding the transformations of the epitheca. The precise taxonomic identity of Chimonodinium lomnickii var. (≡ Peridinium) wierzejskii is unclear, but two different arrangements of the epithecal plate pattern have been reported. We studied dinophyte material collected across Central Europe, including the type localities of Peridinium wierzejskii (Polish Tatra) and Peridinium lomnickii var. punctulatum (Berlin), and investigated the morphology of eight monoclonal strains in detail. We further obtained rRNA sequences of the strains, including 27 new GenBank entries, for a molecular phylogenetic study using a representative taxon sample of the Thoracosphaeroideae. Five ITS ribotypes could be distinguished in Chimonodinium, but neither the distribution nor morphological differentiation seems to correlate with these ribotypes. An evolutionary transformation of the epitheca is inferred from the phylogenetic tree, with the predominant plate pattern found in C. lomnickii var. wierzejskii exemplifying the derived character state. However, the rare epithecal plate pattern of C. lomnickii var. wierzejskii represents the ancestral character state today found in, for example, Peridinium and Scrippsiella. This is an indication of an atavism, of which only very few cases are known from the microbial domain. The name Peridinium wierzejskii is taxonomically clarified by epitypification.

HIGHLIGHTS

• Rare documentation of atavism in the microbial domain• Deep morphology of strain established from type locality• Molecular phylogenetics inferred from concatenated rRNA sequence data

KEYWORDS:

• Character evolution
• dinoflagellate
• molecular phylogenetics
• niche
• protist
• taxonomy
• Wołoszyńska

Acknowledgements

We thank Corinna Romeikat and Christine Tietze (both Munich) for establishing strains that are documented in the present study.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary material

The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2021.2002950

Supplementary table S1: Voucher list. All names are given under the rules of the ICN, the author standard forms follow (Brummitt & Powell, 1992). Abbreviation: n. inf., no information; rt, ribotype. If ‘holotype’ or ‘epitype’ is noted for a species name, then it refers to material, from which the type was prepared.

Supplementary figures S1–S7: Flagellated thecate and immotile stages of Chimonodinium cf. lomnickii (GeoM^*733: ribotype E; glutaraldehyde–fixed material; light microscopy; all at the same scale). S1–S4: flagellated thecate cells showing variation in size and shape. S5–S7: immotile coccoid cells (with theca remnant) showing variation in size and shape. Abbreviation: n: nucleus.

Supplementary figures S8–S18: Flagellated thecate and immotile coccoid stages of Chimonodinium cf. lomnickii (S8–S14, S16 GeoM^*733: ribotype E; S15, S7–S18 GeoM^*686: ribotype E; scanning electron microscopy; all at the same scale). S8: flagellated cell in ventral view (asterisks indicate the sulcal plate Sm). S9–S12: epitheca. S9: left lateral view showing pentagonal anterior intercalary plates 1a and 2a and the precingular plate 3’ as key stone plate. S10: lateral–dorsal view showing pentagonal anterior intercalary plates 1a and 2a and the precingular plate 3’ as key stone plate (note that the height of the precingular plates is greater than in S9). S11–S12: apical view showing pentagonal anterior intercalary plates 1a and 2a and hexagonal intercalary plate 3a. S13: flagellated cell in lateral–dorsal view showing pentagonal anterior intercalary plates 1a and 2a. S14–S15: hypotheca in antapical view showing variation in number and size of the knobs. S16–S17. hypothecae in antapical view showing unusual plate pattern. S16: presence of only one antapical plate. S17: presence of only four postcingular plates. S18: immotile coccoid cell showing a smooth surface. Abbreviations: n′: apical plate, n″: precingular plate, n′′′: postcingular plate, n′′′′: antapical plate, na: anterior intercalary plate, nC: cingular plate, Sa: anterior sulcal plate, Sd: right sulcal plate, Sm: median sulcal plate, Sp: posterior sulcal plate, Ss: left sulcal plate.

Supplementary figures S19–S30: Flagellated thecate and immotile stages of Chimonodinium cf. lomnickii (GeoM^*936: ribotype C; light microscopy; autofluorescence in S22, S26; all at the same scale; arrowheads indicate the position of an eyespot). S19–S22: flagellated cells showing variation in size and shape. S20–S22: same flagellated thecate cell at different foci showing an eyespot (S21) and chloroplast(s) through autofluorescence (S22). S23–S30: immotile coccoid cells showing variation in size and shape. S24: immotile coccoid cell with theca remnant. S25–S26: same cell showing an eyespot (S25) and chloroplast(s) through autofluorescence (S26). S27–S29: same immotile coccoid cell at different loci showing eyespot (S28) and chloroplast(s) (S29). S30. dividing coccoid cell. Abbreviation: n: nucleus.

Supplementary figures S31–S36: Flagellated thecate and immotile coccoid stages of Chimonodinium cf. lomnickii (GeoM^*936: ribotype C; scanning electron microscopy; all at the same scale). S31–S32: flagellated thecate cells in ventral view showing variation in size and shape. S33: lateral–dorsal view showing pentagonal anterior intercalary plates 1a and 2a and the precingular plate 3’ as key stone plate. S34: lateral–dorsal view showing the precingular plate 3’ as key stone plate. S35–S36: hypotheca in antapical view (asterisks indicate the sulcal plate Sm). S35: symmetric arrangement of the hypothecal plates, with a pentagonal postcingular plate 3′′′. S36: slightly asymmetric arrangement of the hypocone plates, with an extension of the postcingular plate 2′′′ connecting the antapical plate 2′′′′ and a quadrangular postcingular plate 3′′′. Abbreviation: n′: apical plate, n″: precingular plate, n′′′: postcingular plate, n′′′′: antapical plate, na: anterior intercalary plate, nC: cingular plate, Sa: anterior sulcal plate, Sd: right sulcal plate, Sm: median sulcal plate, Sp: posterior sulcal plate, Ss: left sulcal plate.

Supplementary figures S37–S42: Flagellated thecate and immotile stages of Chimonodinium cf. lomnickii (GeoM^*825: ribotype B and reference material of Peridinium lomnickii var. punctulatum; light microscopy; all at the same scale; arrowheads indicate the position of an eyespot). S37–S40: flagellated cells showing variation in size and shape. S41–S42: immotile coccoid cells showing variation in size and shape. Abbreviation: n: nucleus.

Supplementary figures S43–S51: Flagellated thecate and immotile coccoid stages of Chimonodinium cf. lomnickii (GeoM^*825: ribotype B and reference material of Peridinium lomnickii var. punctulatum; scanning electron microscopy; all at the same scale). S43–S48: flagellated thecate cells showing variation in size and shape. S43. ventral view. S44. theca in ventral view showing an unusual plate pattern

Author contributions

J. Kretschmann: original concept, light and electron microscopy, drafting and editing manuscript; Anže Žerdoner Čalasan: obtaining molecular sequence data, editing manuscript; J. Knechtel: strain establishment; P.M. Owsianny: original concept, fieldwork; E. Facher: electron microscopy; M. Gottschling: original concept, analysis of molecular data, drafting and editing manuscript.

Additional information

Funding

Financial support was provided by the Deutsche Forschungsgemeinschaft (grant GO 1459 10-1).