The Dancing Star: Reinvestigation of Artodiscus Saltans (Variosea, Amoebozoa) Penard 1890
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Protist, Vol. 170, 349–357, August 2019 http://www.elsevier.de/protis Published online date 21 June 2019 ORIGINAL PAPER The Dancing Star: Reinvestigation of Artodiscus saltans (Variosea, Amoebozoa) Penard 1890 a b a a,1 Efthymia Ntakou , Ferry Siemensma , Michael Bonkowski , and Kenneth Dumack a University of Cologne, Terrestrial Ecology, Institute of Zoology, Zülpicher Str. 47b, 50674 Köln, Germany b Julianaweg 10, 1241VW Kortenhoef, Netherlands Submitted November 12, 2018; Accepted June 13, 2019 Monitoring Editor: Alastair Simpson Artodiscus saltans, first described by Penard (1890), has a unique morphology. Without genetic data it could not yet been reliably placed into a wider taxonomical context. We present morphological data for A. saltans from different aquatic habitats of four European countries. We subjected three cells of one strain from Germany to molecular analyses and, interestingly, obtained six different rDNA sequences. Phylogenetic analyses of these SSU rDNA sequences revealed that A. saltans branches close to the amoebozoan Multicilia marina (Variosea, Amoebozoa). © 2019 Elsevier GmbH. All rights reserved. Key words: Ribosomal genes; amoebae; Conosa; Multicilia; flagellate; Paramphitrema. Introduction 2016, Spain, as well as the records that are the subject of this publication (Table 1)). Penard (1890) described A. saltans as a reddish, Artodiscus saltans was discovered and described spherical cell, being very plastic (hence its generic by Penard in 1890 after he collected some spec- name; the prefix arto is derived from the Greek word imens from a flooded pasture near Wiesbaden, ␣ o for a piece of dough) with fast and contin- Germany. He found similar specimens in subse- uous changes of its shape during locomotion. He quent years in Lake Geneva; along its shore and noticed that, although difficult to see, the cells were in up to 30 m water depth (Penard 1905). However, surrounded by a layer of very fine ‘mucus’ in which since Penard’s description, records have been very very small plates were embedded. It was, in his scarce. In the last century it was found by Rainer words, one of the most interesting species he ever (1968), Siemensma (1973, unpubl.) and De Groot had observed, because of its ‘extraordinary mobile’ (1979). Only recently have reports of A. saltans flagella-like ‘pseudopodia’ by which the ‘animals’ increased (e.g. Frouz 2013, Czech Republic, sev- were ‘dancing vividly’ and sometimes ‘swimming eral photomicrographs and videos available online as fast as a flagellate’. In 1903 he emended his by Revello 2012, Uruguay; Opitz 2013, Austria; description, writing that the cell body usually was Voelcker and Clauß 2015, Germany, and Capilla spherical, but with a tendency to become uneven and angular, being surrounded by a distinct mem- 1 Corresponding author; fax +49 221 470 5038 branous envelope that followed every deformation e-mail [email protected] (K. Dumack). https://doi.org/10.1016/j.protis.2019.06.002 1434-4610/© 2019 Elsevier GmbH. All rights reserved. 350 E. Table 1. Sampling spots of A. saltans, morphological characters and reference to figures. Ntakou Sampling Coordinates Observation n Diameter Length of position of theca Fig. Habitat spots date cell body in flagella in nucleus * ** et m m al. Wipperfürth, 51.127368, May, 2018 1 13 × 10 34 ± 1 (n = 4) centric smooth 1 F small stream, running Germany 7.380871 water, approx. depth 15–20 cm Spiegelplas, 52.274259, 1973 1 NA NA eccentric xenosomes lake shore, sandy Netherlands 5.071945 bottom, CSSW Gaasterland, 52.885363, May, 2012 3 20–24 41 eccentric xenosomes 1D,E ditch, thick layer of Netherlands 5.561656 organic sediment, CSSW Spiegelplas, 52.261307, Jan., 2013 20 19–21 45 ecc./centric smooth/xeno. 1H lake shore, sandy Netherlands 5.067952 bottom, CSSW Sankt Ulrich, 47.534666, June, 1 9 32 centric smooth river, backwater, thin Austria 12.573009 2013 layer of organic sediment, CSSW River Saar, 49.621619, Oct., 2014 2 9–13 34–37 centric smooth 1A river, turbid running Germany 6.564232 water, between green algae on rock Laegieskamp, 52.277634, April, 2014 3 5–10 27–31 centric smooth 1C ditch, with Chara sp. Netherlands 5.136724 and Sphagnum, CSSW Naardermeer, 52.282330, Jan., 2015 5 13–15 39–47 centric smooth ditch, thick layer of Netherlands 5.119572 organic sediment, CSSW Castricum, 52.548240, Sept. 2015 2 10–15 41–52 centric smooth 1 G artificial dune pond, Netherlands 4.617177 sandy bottom, CSSW Île-Grande, 48.795937, June, 2 10–11 27–30 centric smooth old washing basin, France 3.585810 2015 brackish water, CSSW IJsselmeer, 53.074981, July, 2015 1 12 26–30 centric smooth 1B lake shore, sandy Netherlands 5.344705 bottom, CSSW CSSW = optically clear stagnant and shallow water. NA = No data available. * measured from photomicrographs; as the cells have a constantly changeable shape, we tried to estimate the diameter of a spherical cell. ** measured from photomicrographs; we only measured projections that were clearly visible. Most projections were partly out of focus. Molecular Characterization of Artodiscus saltans 351 of the cell and was covered with granules and very specimens from Spiegelplas had a centric and small plates (Penard 1903, 1904, 1905). smaller nucleus with a relatively large central nucle- Based on the unique morphological characters olus (diameters ∼4 m and ∼2 m respectively). of A. saltans it could not be reliably placed within Specimens from all other locations had a relatively a wider taxonomic context. Since the Thecofilosea small and more centric nucleus (diam. ∼3–5 m) (Cercozoa, Rhizaria) and the Variosea (Amoebo- with a relatively large central nucleolus (Fig. 1A, B). zoa) exhibit morphological characters common to Specimens isolated from the river Wupper in Wip- A. saltans, both represent taxa that could possibly perfürth had a length of ∼13 m, a width of ∼10 m, ± accommodate this species. Both taxa accommo- flagella-length of 34 1 m and a span width of ∼ date eukaryvorous and bacterivorous flagellates, 80 m (Fig. 1F). Measurements of all observed amoebae and amoeboid flagellates. Thecofilosean specimens are summarized in Table 1. species characteristically possess a more or All observed specimens had a flexible membra- less conspicuous organic theca, sometimes with nous theca that followed the constantly changing embedded or attached xenosomes (Dumack et al. outline of the cell. Some cells bore a theca with 2017), while variosean flagellates exhibit a protu- embedded small granules and/or rod-shaped ele- berate base from which the flagella emerge (Berney ments (Fig. 1D, E, H), while most cells had a et al. 2015). To ascertain the phylogenetic affiliation smooth theca (Fig. 1A, B, G). Only large cells of A. saltans, we obtained part of its SSU rDNA sometimes showed a small space between theca sequence and conducted phylogenetic analyses. and cytoplasm (Fig. 1E). The small elements were embedded in the membranous theca; we never observed these elements laying on the test. Results Individuals from all sampling locations had a vari- able number of flagella. Small specimens had about Ecological and Morphological 5–6 flagella and larger specimens up to 12, respec- Observations tively. However, the exact number was very difficult to count in living specimens. Although all flagella The observed and isolated specimens of A. were mobile, the cell usually had one or two flag- saltans were collected from different aquatic habi- ella that moved more actively, making slow rowing tats located in Austria, France, Germany and the movements. In fast locomotion the cell had one Netherlands (Table 1). All specimens were found leading flagellum with two trailing flagella behind in freshwater except one that occurred in slightly in the same plane, all three together shaped like a brackish water in an old fisherman’s washing pool Y (Supplementary Material Videos S1, S2). These on the French Atlantic coast, where Enteromorpha three flagella hardly moved, while the other flag- intestinalis was a dominant species. All but one ella made rowing movements in the direction of location had optically very clear water. Only the river the leading one. Despite the slow movements of Saar had turbid water; specimens there were col- the flagella, they propelled the organism relatively lected from sessile algae on a stone just below the quickly in the direction of the leading flagellum (see surface. All aquatic habitats were shallow with a Fig. 1C). Some specimens of A. saltans showed layer of organic sediment of variable thickness. The one short and stiff flagellum and at one occasion water bodies were stagnant or running. even two (Fig. 1G). When mechanically disturbed, A. saltans was never abundant in any sample. It the cells tended to swim actively to the water sur- was never found at first observation, but when wet face, making isolation a difficult task. mounts were left over for one or more days in a In larger specimens all flagella had a thickened wet chamber, specimens emerged from the debris and slightly tapering base. Using light microscopy and could be observed moving along the cover it was not possible to detect if this base was part of glass. We never found evidence that this species the flagellum or a tubular bulge of the theca (Fig. 1 multiplied in the wet mounts. Usually the cells dis- D, E, Supplementary Material Videos S1, S2). In appeared again after a few days. one specimen this base was covered by the same The cell body contained one nucleus with a kind of material as embedded in the theca. single small centric nucleolus and the cytoplasm In almost all specimens the flagella were more or appeared slightly greenish under phase con- less evenly distributed over the cell surface, but in trast. Specimens collected from Spiegelplas and material from Spiegelplas we observed some spec- Gaasterland had a relatively large, eccentrically imens that occasionally became spindle-shaped placed nucleus (diameter ∼9 m) with one or three within some minutes, with 1 to 4 flagella at each small nucleoli (∼2 m) (Fig.