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. 2022 Mar;12(3):210325.
doi: 10.1098/rsob.210325. Epub 2022 Mar 16.

On the origin of TSAR: morphology, diversity and phylogeny of Telonemia

Denis V Tikhonenkov  1 , Mahwash Jamy  2 , Anastasia S Borodina  1   3 , Artem O Belyaev  1   4 , Dmitry G Zagumyonnyi  1 , Kristina I Prokina  1   5 , Alexander P Mylnikov  1 , Fabien Burki  2   6 , Sergey A Karpov  7   8
Affiliations

On the origin of TSAR: morphology, diversity and phylogeny of Telonemia

Denis V Tikhonenkov et al. Open Biol. 2022 Mar.

Abstract

Telonemia is a poorly known major phylum of flagellated eukaryotes with a unique combination of morphological traits. Phylogenomics recently revealed the phylogenetic position of telonemids as sister to SAR, one of the largest groups of eukaryotes, comprising Stramenopiles, Alveolata and Rhizaria. Due to this key evolutionary position, investigations of telonemids are of critical importance for elucidating the origin and diversification of an astounding diversity of eukaryotic forms and life strategies. To date, however, only two species have been morphologically characterized from Telonemia, which do not represent this genetically very diverse group. In this study, we established cultures for six new telonemid strains, including the description of five new species and a new genus. We used these cultures to update the phylogeny of Telonemia and provide a detailed morphological and ultrastructural investigation. Our data elucidate the origin of TSAR from flagellates with complex morphology and reconstruction of the ancestral structure of stramenopiles, alveolates and rhizarians, and their main synapomorphic characters. Since telonemids are a common component of aquatic environments, the features of their feeding, behaviour and ecological preferences observed in clonal cultures and the results of global metabarcoding analysis contribute to a deeper understanding of organization of microbial food webs.

Keywords: 18S rDNA; evolution; microbial diversity; protists; telonemids; ultrastructure.

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
The phylogeny of telonemids. Maximum-likelihood and Bayesian phylogenies of 18S rRNA sequences. Numbers at the nodes represent Ultrafast bootstrap (IQTree) and Bayesian support values, respectively. Names of the groups refer to clades that were recognized in Bråte et al. [11]. Only values above 50/0.50 are shown and black dots indicate strong statistical support (≥95/0.90). Taxa labels in blue indicate freshwater sequences.
Figure 2.
Figure 2.
Distribution of telonemids in the World Ocean. Metabarcoding data from 113 stations collected during the Tara Oceans expedition and corresponding to the V9 fragment of the 18S rRNA gene. (a) Telonemids were found to be enriched in the pico size fraction (0.8–5 µm), which is consistent with their cell sizes. (b) Percentage of telonemid metabarcodes recovered in the pico size fraction.
Figure 3.
Figure 3.
Phylogenetic placement of Tara Oceans and Malaspina expedition telonemid OTUs (a,b) and metabarcodes (c,d) on the Telonemia reference tree. The branch colours represent the distribution of OTU/metabarcode placement with darker branches indicating (a,b) that more OTUs were placed on them or (c,d) that those particular lineages are more abundant in the global ocean. TEL 1 is depicted in green, and TEL 2 in yellow. Specific clades in each TEL group are indicated with black lines.
Figure 4.
Figure 4.
External morphology of telonemids, differential interference contrast microscopy. Arpakorses versatilis, attached cell (a) and cell division (b). Arpakorses idiomastiga, typical cell (c) and cell division (d). Telonema papanine, typical cell (e) and cell with pseudopodium (f). Telonema tenere, typical cell (g) and cell division (h). Telonema rivulare, typical cells (i–k) and cell division (l). Scale bars: 5 µm. Abbreviations: c.v.—contractile vacuole; f—flagella; f.v.—food vacuole; gr—granules; pt—pit; ps—pseudopodium; rs—rostrum.
Figure 5.
Figure 5.
External morphology of telonemids, SEM. (a–d) Arpakorses versatilis, (e–g) Arpakorses idiomastiga, (h) Telonema subtile, (i–l) Telonema papanine, (m–n) Telonema tenere, (o) Telonema rivulare. Scale bars: (a,b,e,f,h,i,j,m,n,o)—5 µm; (c,d,g,k,l)—1 µm. Abbreviations: ac—acroneme; cm—cytostome; f—flagella; ma—mastigoneme; p—protrusion; p1,p2,p3—part 1,2,3 of mastigoneme.
Figure 6.
Figure 6.
General cell organization of (a,b,d,e) Arpakorses versatilis and (c,f) Arpakorses idiomastiga. (a) General view of the cell at LS. (b) Cell structures at its anterior end. (c) Mature mastigonemes in the dilation of perinuclear space at LS and transversal section (TS) of mastigoneme shafts showing their tubular structure (d, arrows). (e) Mitochondrion covered with ribosomal subunits. (f) Structure of extrusomes at TS (ts), tangential (tas) and longitudinal axial section (as). Scale bars: (a) 1 µm, (b) 400 nm, (c–f) 200 nm. Abbreviations: af—adhesive fibres; as—structure of extrusome at longitudinal axial section; b—bacteria; be—belt region; ca—anterior part of corset; cp—posterior part of corset; es—extrusomes; fv—food vacuole; k1—kinetosome of posterior flagellum; k2—kinetosome of anterior flagellum; m—mitochondria; ma—mastigonemes; mah—mastigoneme terminal hairs; mas—mastigoneme shafts; n—nucleus; pf—posterior fibre of corset; pl—r3-associated plate; pr—eukaryotic prey; rh—rhizoplast-like structure; rs—ribosomal subunits; tas—structure of extrusome at tangential section; ft—fibrillar tube associated with belt epiplasm; ts—structure of extrusome at transverse section.
Figure 7.
Figure 7.
Ultrastructural organization of (a–c) Arpakorses versatilis and (d) Arpakorses idiomastiga. (a) Sagittal section of the cell, ventral side to the left, anterior to the top. (b) TS of the cell posterior containing two food vacuoles with bacteria and eukatyotic prey. Dorsal side to the top. (c) Golgi apparatus by the nucleus at the middle of the cell. (d) orthogonal disposition of kinetosomes characteristic for A. idiomastiga. Scale bars: (a,b) 1 µm; (c) 400 nm; (d) 200 nm. Abbreviations: af—adhesive fibres; ag—axial granule underneath transversal plate of flagellum; be—belt region; ca—anterior part of corset; cp—posterior part of corset; cw—cart-wheel structure; es—extrusomes; fv—food vacuole; ga—Golgi apparatus; k1—kinetosome of posterior flagellum; k2—kinetosome of anterior flagellum; m—mitochondria; ma—mastigonemes; n—nucleus; pf—posterior fibre of corset; r3 and r4—microtubular roots of kinetosome 2.
Figure 8.
Figure 8.
Structure of the belt region and diaphragm of Arpakorses idiomastiga (a–c) and Arpakorses versatilis (d–f). Cell is oriented with anterior end to the top in all figures. (a) LS through the cell periphery, (b,c) belt region and diaphragm associated with AFs, (d–f) belt in anterior to posterior corset transition, (e,f) two consecutive tangential sections (60 nm) from surface (e) to the cell interior (f) direction. Black arrowheads in (e) and (f) show belt microtubules surrounded by epiplasm, which produce secondary microtubules of posterior part of corset (mtp) with intermediated epiplasmic bands. Scale bars: (a,b,d) 1 µm; (c) 500 nm; (e,f) 250 nm. Abbreviations: af—adhesive fibres; b—bacteria; be—belt region; ca—anterior part of corset; cp—posterior part of corset; di—diaphragm; ep—epiplasm of belt; m—mitochondria; mas—mastigoneme shafts; mta—microtubules of anterior part of the corset; mtp—microtubules of posterior part of the corset; n—nucleus; pf—posterior fibre of corset.
Figure 9.
Figure 9.
Kinetid structure of Arpakorses versatilis. (a–d) kinetid sections of separate cells, showing the roots and cytoskeletal elements. (e–k) consecutive serial TSs of kinetosome k1 from distal (e) to proximal (k) end. Cells oriented dorsal side to the right, anterior end to the top in all sections. Note: triplets of k1 are oriented counter clockwise, thus, our view is from flagellar tip to flagelar base. It means that the k1 gives rise to the left ‘posterior’ flagellum. Arrow on (a) shows a fibrillary sheath around posterior surface of k2. Scale bar: 200 nm. Abbreviations: af—adhesive fibres; ag—axial granule underneath transversal plate of flagellum; ax—axoneme; ca—anterior part of corset; ep—epiplasm of belt; ff—fibrillar foot of k2, initiating its microtubular roots r3 and r4; ft—fibrillar tube associated with belt epiplasm; k1—kinetosome of posterior flagellum; k2—kinetosome of anterior flagellum; pl—r3-associated plate; r1—ventral microtubular root of k1; r3 and r4—microtubular roots of kinetosome 2; tf—transition fibres; tp—transversal plate.
Figure 10.
Figure 10.
Kinetid structure and belt origin of the Arpakorses versatilis. (a–f) consecutive serial TSs of k2 from distal (a) to proximal (f) end. (a–l) consecutive serial sections of belt epiplasm origin (a) and its further enlargement (b–l) from the right to the left side of the cell. Dorsal side of the cell is to the right, anterior end to the top in all sections. Note: triplets of k2 are oriented clockwise; thus, our view is from flagelar base to flagellar tip. It means that the k2 gives rise to the right ‘anterior’ flagellum. Scale bar: 200 nm. Abbreviations: af—adhesive fibres; ag—axial granule underneath transversal plate of flagellum; ca—anterior part of corset; ep—epiplasm of belt; ff—fibrillar foot of k2, initiating its microtubular roots r3 and r4; ft—fibrillar tube associated with belt epiplasm; ft2—another fibrillary tube in kinetid vicinity; k1—kinetosome of posterior flagellum; k2—kinetosome of anterior flagellum; pl—r3-associated plate; r1—ventral microtubular root of k1; r3 and r4—microtubular roots of kinetosome 2.
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