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Biologia 63/6: 799—805, 2008 Section DOI: 10.2478/s11756-008-0101-4

Siderocelis irregularis (, ) in Lake Tanganyika (Africa)*

Maya P. Stoyneva1, Elisabeth Ingolič2,WernerKofler3 &WimVyverman4

1Sofia University ‘St Kliment Ohridski’, Faculty of Biology, Department of Botany, 8 bld. Dragan Zankov, BG-1164 Sofia, Bulgaria; e-mail: [email protected], [email protected]fia.bg 2Graz University of Technology, Research Institute for Electron Microscopy, Steyrergasse 17,A-8010 Graz, Austria; e-mail: [email protected] 3University of Innsbruck, Institute of Botany, Sternwartestrasse 15,A-6020 Innsbruck, Austria; e-mail: werner.kofl[email protected] 4Ghent University, Department Biology, Laboratory of and Aquatic Ecology, Krijgslaan 281-S8,B-9000 Gent, Belgium; e-mail: [email protected]

Abstract: Siderocelis irregularis Hindák, representing a genus Siderocelis (Naumann) Fott that is known from European temperate waters, was identified as a common phytoplankter in Lake Tanganyika. It was found aposymbiotic as well as ingested (possibly endosymbiotic) in lake , mainly Strombidium sp. and Vorticella spp. The morphology and ultrastructure of the species, studied with LM, SEM and TEM, are described with emphasis on the structure of the and the pyrenoid. Key words: Chlorophyta; cell wall; pyrenoid; symbiosis; ; Strombidium; Vorticella

Introduction ics of symbiotic species in general came into alignment with that of free-living and the term ‘zoochlorel- Tight partnerships between algae and aquatic inver- lae’ was abandoned as being taxonomically ambiguous tebrates, including symbiotic relationships, have long (e.g. Bal 1968; Reisser & Wiessner 1984; Taylor 1984; been of interest and a number of excellent reviews are Reisser 1992a). It was proposed to replace this obsolete available. In the context of modern biology, Reisser notion by the prefix ‘symbiotic’, and the exact species or (1992b, p. xii) defined ‘symbiosis’ as the ‘living together genus designation or, in cases of uncertainty, by ‘sym- in physical contact of organisms of different species’, biotic green alga’ (Reisser 1984; Reisser & Widowski while the interaction between heterotrophic cells and 1992). The terms ‘endosymbiotic’ and ‘endosymbiont’ ‘symbiotic’ derived from ingested algae was were further clarified by Reisser (1992a, p. 2) to be used mentioned by him as “twilight-zones” of symbiosis in- in a general sense as ‘living within genetically different cluded there by tradition. organism... which will be called “host” without any Many symbiotic genera and species appear closely implications as to mutual harm or benefit. related to, or fall within, recognized free-living assem- Heterotrophic hosts seem to be very fastidious blages. However, by strong contrast with the free-living in choosing a potential autotrophic partner. Although (aposymbiotic) algae the descriptions of most of the the freshwater habitat offers a plethora of diverse symbiotic forms are still quite rudimentary and often cyanoprokaryotes and algae, they pick up exclusively contradictory (Reisser 1984). Following the studies of asexual green coccoid species (Reisser 1986). Due to Brandt (1882) the most commonly applied term to their simple morphology, classification by light mi- the green autotrophic partners was ‘zoochlorellae’. This croscopy alone is not easy. It has commonly been stated term, without any taxonomic value and arbitrarily ex- that the predominant symbiotic algal partners of fresh- tended to every green algal cell that lives in associa- water associations belong to the genus (with tion with a heterotrophic organism, was characteristic some preference to the -sorokiniana of the confused state of knowledge on symbiotic forms cluster) and its representatives do not differ principally (Reisser 1984). After many discussions on whether exis- by morphology or cytology from free-living chlorellae, tence in a symbiotic association was a sufficient reason but are distinguished from them mainly by physiolog- to place these organisms in separate taxa, the systemat- ical characteristics (Reisser & Widowski 1992). More

* Presented at the International Symposium Biology and of V, Smolenice, June 26–29, 2007, Slovakia.

c 2008 Institute of Botany, Slovak Academy of Sciences 800 M.P. Stoyneva et al. recently, the first molecular phylogeny based on 18S for a tropical coloured lake with abundance of ciliates rRNA sequences was reported and revealed paramae- up to 250 000 L−1. This suggests that mixotrophic cili- cian symbionts which were genetically close to so-called ates may play a substantial role in plankton photosyn- Chlorella vulgaris group (Hoshina et al. 2004, 2005). Oc- thesis. casionally, other green algae (species of Scenedesmus, The considerable role of ciliates is especially valid Ankistrodesmus, Pleurococcus, , , for the ancient, large tropical oligotrophic Lake Tan- , Symbiococcum and a few prasino- ganyika (Hecky & Kling 1981, 1987; Pirlot et al. 2005). phyceans) have been reported to occur in freshwater There ‘the biomass of Strombidium cf. viride nearly symbiotic systems (for references consult Reisser 1984; equaled or exceeded the phytoplankton biomass dur- Rahat 1992; Reisser & Widowski 1992; Nakahara et al. ing much of the stably stratified period; this protozoan 2004). However, these data, based mainly on field ob- probably has a symbiotic relationship with zoochlorel- servations, need careful corroboration by modern tax- lae, which were always present in it’ (Hecky & Kling onomic methods applied to material grown under lab- 1981, p. 548). More recently, ciliates are still found to oratory conditions in order to exclude the possibility be an abundant group in the lake (Descy et al. 2005) that the observed algae have only been taken as a food and in 2002, total autotrophic carbon was partly sus- (Reisser 1986; 1992a; Reisser & Widowski 1992). tained by the endosymbionts in Strombidium (Pirlot The hosts of freshwater endosymbiotic associations et al. 2005). When fixed phytoplankton samples were can be assigned to different groups but among them processed during the same study of Lake Tanganyika, the overwhelming are chromalveolate , predom- it was observed that this abundant contained inantly ciliates. This fact has long been linked with their numerous coccoid green algal cells. Similar green cells ability to feed via (Reisser 1992a). Ciliates were detected in the samples in different quantities as are commonly considered as herbivores, but they are ac- free-living or inside other zooplankters (e.g. Vorticella tually composed of more or less distinct trophic guilds spp.). Using light microscopy the alga was identified (Dolan 1991). The key role that ciliates may play in as Siderocelis irregularis Hindák, a first record for the food webs in lakes was stressed by many authors dur- lake (Descy et al. 2005). For the present study, selected ing the last few decades. These studies have revealed samples were prepared for scanning (SEM) and trans- that ciliate communities are composed of a high num- mission electron microscopy (TEM). Here we describe ber of species with different sizes that reflect a diverse the cell morphology, cytological peculiarities and repro- range of feeding strategies, ranging from phagotrophic duction mode of Siderocelis irregularis and we discuss ingestion of particles (including nanoplanktonic algae) its taxonomic position. to photosynthetic fixation of organic carbon. The pho- tosynthetic capability can be acquired by sequestration Material and methods of chloroplasts from ingested prey or by possession of photosynthetic cells as endosymbionts (Modenutti et al. The material was collected from the large deep ancient tec- 2000; Endo & Taniguchi 2006; Summerer et al. 2007). tonic tropical Lake Tanganyika. In 2002–2004, standard bi- This mixed nutrition, termed mixotrophy, may improve weekly phytoplankton sampling at a depth of 20 m was access to scarce nutrients since by excretion of carbohy- conducted in the regions of Kigoma and Mpulungu. Ad- drates host metabolism could be sustained (e.g. Stabell ditional samples through a longitudinal transect of the lake were collected during a cruise in July 2003. A Zeiss Ax- et al. 2002). Therefore mixotrophy can be viewed as a iovert 135 inverted microscope was used for phytoplankton kind of symbiosis and also as an adaptive strategy that counting. Detailed investigations on non-permanent slides provides greater flexibility in the planktonic environ- were carried-out on a Leitz Diaplan microscope with Differ- ment and particularly strong advantage in oligotrophic ential Interference Contrast. Staining involved Indian ink, waters (Jones 1994; Schoonhoven 2000). These easily Methylene Blue, Gentiane Violet and Iodine. TEM method- explains why ciliates appear in quite different types of ology followed G¨artner & Ingoli´c (2003). Micrographs were waters (Stoecker 1998) but are especially common in taken with a FEI Tecnai 12 TEM microscope with a Gatan oligotrophic waters where a close nutrient cycle within CCD camera Bioscan. For SEM studies algal cells were the symbiotic association would confer advantages to washed with distilled water and dehydrated in a series of ethanol with gradually increasing concentrations (from 10% both symbiotic partners (Fenchel 1987; Modenutti et to 96%; 30 min. each). The material was then transferred to al. 2000). formaldehyde-dimethyl-acetal (FDA – Gerstberger & Leins Data on the ecology of freshwater symbiotic associ- 1978) for 24 hours, followed by FDA for 2 hours. The sample ations with algae are still scarce. The first measurement was critical-point dried with liquid CO2 using FDA as inter- of photosynthetic rates of natural, freshwater-ciliates medium, sputter-coated with gold-palladium and examined in situ at different water depths over a whole year was with a Philips XL20 SEM. done in a temperate, oligotrophic lake in North Patago- nia (Woelfl & Geller 2002). There the ciliate endosym- Results biotic algae accounted for up to 25% of the total au- totrophic biomass and of the total (op. Light microscopy: Strombidium sp. (S.cf.viride Stein cit.). The abundance of ciliates is also high in some acc. to Hecky & Kling 1981; Pirlot et al. 2005), Vor- tropical and subtropical lakes. Laybourn-Parry et al. ticella spp. and some other zooplankters containing (1997) estimated a contribution of ca. 40 µgChl-a L−1 green algal cells were observed in different quantities Siderocelis irregularis in Lake Tanganyika 801

Figs 1–11. Siderocelis irregularis Hindák from Lake Tanganyika (LM). 1–9 – aposymbiotic cells (2 stained by Methylene Blue; 4 Stained by Gentian Violet; 5 stained by Indian ink; 7 pyrenoid starch plates after squashing; 8, 9 reproductive stages: 8 group of two connected cells; 9 cross-like group of two by two autospores of different size, stained by Gentian Violet); 10 – cells released from Strombidium sp.; 11 – cells in Vorticella sp. in the phytoplankton samples. Identical coccoid green the relatively invariant nature of this feature and to- cells were found as free-living in the same samples, gether with its relatively low values explains their sen- which, according to the observations based on qual- sitivity to grazing by zooplankters. There was not a sig- itative samples, were most abundant during the dry nificant difference between the dimensions of the cells season (May–September). In quantitative surface sam- inside the protozoans and the free-living cells. The cell ples from 30 September 2003 the same green alga was contents had a granular appearance without staining found among the phytoplankton dominants, after An- (Figs 1, 3, 5) and clearly warty after staining with abaenopsis tanganyikae (G. S. West) V. V. Mill., Lobo- Gentian Violet and with Methylene Blue (Figs 4, 9). cystis planctonica Tiffany et Ahlstrom and Gloeothece Staining with Indian ink did not reveal any sp. The LM observations revealed the presence of irreg- around the cells (Fig. 5). The was large, ularly shaped spherical to broad pyramidal and, more parietal, and mantle-shaped. Usually one single basal rarely, ellipsoidal coccoid cells with a width of (3.8)– or lateral pyrenoid was seen in each cell, but occasion- 5.1–9.5 µm and a length of (5.12)–8–12.7 µmor,when ally two pyrenoids were found (Fig. 6). The pyrenoid spherical, with a diameter of (4.8)–6.4–12.8 µm(Figs was always surprisingly large (e.g. 3.84 µmindiam- 1–6). The range of cell size during different periods and eter in a cell with dimensions 7.04 × 10.24 µm) and the change in average dimensions (Figs 12, 13) showed was clearly visible without staining (Figs 1–3, 5, 8, 10). 802 M.P. Stoyneva et al.

14 or spine-like processes (Figs 14–19). The number of lay- 12 ers was variable (ca. 4–5) and included at least one that 10 was relatively thick (Figs 16–19). The cell walls of au- 8 tospores had a similar structure (Fig. 15). Additional 6 4 discrete dark precipitation granules were found on some 2 cell walls (Fig. 20). SEM studies (Figs 23–26) also re- 0 vealed the cell wall undulations and the occasional pres- Ap M Jn Jly Ag S ence of precipitation granules on cell walls. Fig. 12. Cell dimensions of Siderocelis irregularis Hindák in Lake Tanganyika (2003). Discussion

The results from this study revealed the similarity of 14 the cells of the green alga found free-living (aposym- 12 10 biotic) in the phytoplankton and ‘harbored’ inside dif- 8 ferent zooplankters, predominantly in two ciliates – the 6 oligotrich Strombidium sp. and the peritrich Vorticella 4 spp., both of which were abundant in Lake Tanganyika. 2 0 The first genus is a well known ‘green’ or ‘plastidic cil- Ap M Jn Jl As S O N iate’ from different localities especially from Lake Tan- ganyika, where its trophic role was postulated by Hecky Fig. 13. Average cell dimensions of Siderocelis irregularis Hindák in Lake Tanganyika in 2003 (bars indicate standard deviation). & Kling (1981, 1987), Pirlot et al. (2005) and by Descy et al. (2005). By contrast, green algae have only been reported infrequently in the freshwater ciliate Vorticella (Noland & Finley 1931; Graham & Graham 1978, 1980) The starch sheath composed of 2–10 granules was also and, as far as we know, never before for Lake Tan- clearly visible (Figs 1–5, 8, 10) as was demonstrated by ganyika. Since both species contribute substantially to the pyrenoid squash method of Ettl & G¨artner (1988) the plankton biomass of this tropical great lake, iden- (Fig. 7). Staining with iodine solutions revealed addi- tification of their ‘endosymbiont’ is important. tional starch granules in the cells. This investigation appears to support the opinion The samples contained mostly single cells but of different authors summarized in the review by Reisser rarely two connected cells were seen (Fig. 8) which & Widowski (1992, p. 34) that ‘there do not exist any could have arisen a result of cell division or represented major quantitative differences between symbiotic and just released autospores. Occasionally groups of four aposymbiotic algae’. Comparison of the morphological autospores were observed arranged in cross-like groups features of the cells found in our material with the de- of two by two cells that differed in size (Fig. 9) or groups scription of Siderocelis irregularis Hindák from temper- of four of equal size enclosed by a tight mother cell wall. ate freshwaters (Hindák 1980) allows us to refer the Starch-containing cells with undestroyed cell con- material to that species. The only morphological differ- tent were found free-living in the plankton as well as ence lies in the relatively larger range of dimensions of inside various zooplankton representatives, but mainly the vegetative cells observed in Lake Tanganyika (3–12 in the oligotrich ciliate Strombidium sp. and in per- µm) compared with the original description by Hindák itrichs like Vorticella spp. (Figs 10, 11). Cells inside (1980) (4–7 × 5–10 µm). Since the deviations were rela- the zooplankters and especially in Strombidium were tively small and towards both extremes, we do not find almost equal in dimensions, but cells with different di- them significant enough to justify the description of a ameters (from 7.68 to 12.8 µm) were observed in the new taxon. same organism. The cells inside were single or, rarely, With respect to the morphology of reproductive appeared autospore-like: small cells arranged in groups structures, differently sized autospores have been found of 2 or 4 without an enclosing mother cell wall. In in our samples. To our knowledge, only autospores of most cases, the ‘granular’ coccoid cells were the only equal size have been depicted for the representatives particles seen in the protozoans, but occasionally they of S. irregularis and for the genus Siderocelis Fott. in were found together with other green coccoid algae and general. It is noted that in the closely related genus very rarely with empty cells. The other green Chlorella Beij. from Trebouxiophyceae (Tsarenko et alga seen inside the protozoans was Lobocystis planc- al. 2006) unequal autospores have been described for tonica, one of the most abundant green algae in the Chlorella trebouxioides Punčoch. (Punčochářová 1994). lake phytoplankton. Therefore, in our opinion, the presence of unequal au- Transmission and scanning electron microscopy: tospores or autospores of consecutive growth is not a TEM studies confirmed the presence of large pyrenoid valid reason for the description of a new taxon. covered by 2–10 starch plates (Figs 21, 22). The Autospores were observed inside the ciliates, but pyrenoid was traversed by a number of single undu- without proper experiments it is not possible to con- lating thyllakoids (Fig. 22). The cell walls were thick, clude that this alga is able to reproduce inside the hosts, multilayered and irregularly undulating, bearing wart or was ingested in this status. According to the dimen- Siderocelis irregularis in Lake Tanganyika 803

Figs 14–26. Siderocelis irregularis Hindák in Lake Tanganyika (TEM and SEM). 14–22 – ultrastructure of S. irregularis (TEM): arrows indicate remnants of mother cell wall (15), cell wall ‘spines’ (16, 18, 19) and precipitation granules (20); 23–26 – cell morphology of S. irregularis (SEM); arrows indicate precipitation granules. sions and general statements about the size of algae Since the first finding of sporopollenin in coccoid vulnerable to grazing, we assume that, most likely, the green algae by Atkinson et al. (1972) the role of this alga continues to reproduce after being ingested. This compound and other likely components (algaenans) was suggestion is in agreement with the results of Stabell widely interpreted as a mechanism to enhance grazing et al. (2002) who showed that the gross growth rate of resistance that was particularly important for endosym- algal endosymbionts in mixotrophic ciliates is always bionts. Different authors appear to hold differing views close to maximum. on this topic. According to Douglas & Huss (1986) and The TEM investigations, carried out for first time Reisser & Widowski (1992) sporopollenin is not a gen- on Siderocelis irregularis, allow us to enrich the infor- eral feature of cell walls of symbionts, and protection mation on the ultrastructure of the pyrenoid and cell against host digestive can be provided by fea- wall. The importance of these features in the systemat- tures other than a resistant cell wall structure. Due to ics of green algae is well established (e.g. Atkinson et al. lack of chemical analysis on Siderocelis irregularis,it 1972, Ingoli´c&G¨artner 2003). The large basal pyrenoid is possible only to compare data with its ‘close rela- of the studied specimens is penetrated by numerous sin- tives’. Sporopollenin and sporopollenin-like compounds gle undulating thyllakoids and is covered by 2–10 starch were detected in close relatives of Siderocelis in the plates. The ‘granulation’ of the cells, well visible under Trebouxiophyceae (e.g. Kalina & Punčochářová 1987; the light microscope even at 40× magnification, is obvi- G¨artner & Ingoli´c 1993). Therefore sporopollenin or its ously due to the abundant and irregular undulations of alike substances may also be present in S. irregularis.It the cell walls. The presence of additional precipitation is conceivable that the presence of sporopollenin, com- granules corroborates the findings of Crawford & Heap bined with the thick walls consisting of multiple layers, (1978) in another species of Siderocelis. are an effective defense mechanism against grazing by 804 M.P. Stoyneva et al. zooplankton. It could enable S. irregularis to survive Vyverman W., Cocguyt C., De Wever A., Stoyneva M.P., after ingestion by Strombidium, Vorticella or other zoo- Deleersnijder D., Naithani J., Chitamwebwa D., Chande A., plankters, and even to be released afterwards without Kimirei I., Sekadende B., Mwaitega S., Muhoza S., Sinyenza D., Makasa L., Lukwessa C., Zalu I. & Phiri H. 2005. Final visible damage. Report: Climate variability as recorded in Lake Tanganyika In conclusion, according to the morphological anal- (CLIMLAKE-EV/02). Belgian Science Policy, Brussels, 119 ysis and in the absence of molecular data, the taxo- pp. nomical identity of the specimens found in Lake Tan- Dolan J.R. 1991. Guilds of ciliate microzooplankton in the Chesa- peake Bay. Estuarine Coastal and Shelf Science 33: 137–152. ganyika is provisionally determined as Siderocelis ir- Douglas A.E. & Huss V.A.R. 1986. On the characteristics and regularis Hindák. It contributed to the phytoplankton taxonomic position of symbiotic Chlorella. Arch. Microbiol. biomass in a free-living state (aposymbiotic) as well as 145: 80–84. ingested (possibly endosymbiotic) by lake heterotrophs, Endo Y. & Taniguchi A. 2006. Method of chloroplast sequestra- tion and induction of encystment in the planktonic ciliate particularly the ciliates Strombidium sp. and Vorticella Strombidium conicum. Jpn. J. Protozool. 39: 53–57. spp. According to the drawing provided by Hecky & Ettl H. & G¨artnerG. 1988. Eine einfache Methode zur Darstellung Kling (1987 – Fig. 42) it is assumed that this species der Struktur der St¨arkeh¨ullen von Pyrenoiden bei Gr¨unalgen was recorded earlier (in 1975) as symbiotic in Strombid- (Chlorophyta). Arch. Protistenknd. 135: 179–181. Fenchel T. 1987. Ecology of . The biology of free-living ium cf. viride. The identification of the species, based phagotrophic protests. Springer Verlag, New York, 197 pp. on LM, SEM and TEM, has provided additional infor- G¨artner G. & Ingoli´c E. 1993. Zur Morphologie und Tax- mation on the morphology, , ecology and onomie einiger Bodenalgen (Unterfamilie Scotiellocystoideae, distribution of the representatives of the genus Sidero- ) aus der Algensammlung in Innsbruck (ASIB, 143: celis (Naumann) Fott. It was previously known mainly Austria). Arch. Protistenknd. 101–112. G¨artner G. & Ingoli´c E. 2003. Further studies on from temperate waters of Europe and was reported Brand emend. Vischer (Chlorophyta, Trebouxiophyceae) and from large lakes of Africa with the species S. kolkwitzii a new species Desmococcus spinocystis sp. nov. from soil. (Naumann) Fott (Cocquyt et al. 1993). Just recently, S. Biologia 58: 517–523. irregularis was found in a free-living status in another Gerstberger P. & Leins P. 1978. Rasterelektronenmikroskopische Untersuchungen an Bl¨utenknospen von Physalis philadelph- lake from the same system of African great rift lakes ica (Solanaceae) – Anwendung einer neuen Pr¨aparationsme- – as a very rare species in Lake Kivu (Sarmento et al. thode. Ber. Deutsch. Bot. Ges. 91: 381–387. 2007). Graham L.E. & Graham J.M. 1978. Ultrastructure of endosym- biotic Chlorella and Vorticella.J.Protozool.25: 207–210. Graham L.E. & Graham J.M. 1980. Endosymbiotic Chlorella in Acknowledgements a species of Vorticella (Ciliophora). Trans. Am. Microsc. Soc. 99: 160–166. Hecky R.E. & Kling H.J. 1981. The phytoplankton and protozoo- The authors are grateful to Prof. RNDr. F. Hindák, DSc. plankton of the euphotic zone of Lake Tanganyika: Species for the invitation to present this paper at the V Interna- composition, biomass, chlorophyll content, and spatio-tem- tional Symposium Biology and Taxonomy of Green Algae. poral distribution. Limnol. Oceanogr. 26: 548–564. Part of this study was carried out in the framework of the Hecky R.E. & Kling H.J. 1987. Phytoplankton ecology of the CLIMLAKE project, supported by the Federal Science Pol- great lakes in the rift valleys of Central Africa. Arch. Hydro- icy Office of Belgium, which also granted a research fellow- biol. Beih. Ergebn. Limnol. 25: 197–228. ship to the first author. The first author thanks Prof. Dr J.- Hindák F. 1980. Studies on the chlorococcal algae (Chloro- P. Descy for the invitation to participate in the CLIMLAKE phyceae). II. Bratislava, Veda, Biol. Práce 26 (6): 1–196. project. Special acknowledgement is due to Univ.-Prof. Dr Hoshina R., Kamako S.-I. & Imamura N. 2004. Phylogenetic po- sition of endosymbiotic green algae in Paramaecium bursaria G. G¨artner for his help in organizing the SEM and TEM Ehrenberg in Japan. Biology 6: 447–453. studies and for his comments during the preparation of the Hoshina R., Kato Y., Kamako S. & Imamura N. 2005. Genetic manuscript. We thank Dr H. 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