Phagotrophy by a Plastidic Haptophyte, Prymnesium Pa Tellifer Urn
Total Page：16
File Type：pdf, Size：1020Kb
AQUATIC MICROBIAL ECOLOGY Vol. 14: 155-160, 1998 Published February 13 Aquat Microb Ecol Phagotrophy by a plastidic haptophyte, Prymnesium pa telliferurn Urban Tillmann* Forschungs- und Technologiezentrum Westkiiste, Universitat Kiel, D-25761 Biisum, Germany ABSTRACT: Observations and photographs of the previously unsuspected ingestion capacity of the phytoflagellate Prymnesiurn patelliferurn are presented. P. patelliferurn took up prey cells of different sizes by an elongated, U-shaped pseudopodium formed at the posterior part of the cells. While feeding, aggregates of several P. patelliferurn cells were formed in which their pseudopodia come in close con- tact. Motile prey cells were immobilised or probably killed before ingestion, but not all protistan species of ingestible size were immobilised or attacked. It is suggested that P. patelliferurn may secrete a toxin that serves as a killing agent for prey organisms. KEY WORDS: Prymnesiurn patelliferurn . Mixotrophy . Phagotrophy . Haptophyta INTRODUCTION 1936, Dietrich & Hesse 1990), Bulgaria (Valkanov 1964) and Norwegian coastal waters (Kaardtvedt et Phagotrophy by photosynthetic flagellates is a well- al. 1991). Because of its economic importance as an known phenomenon described in the phycological lit- ichthyotoxin-producing genus, Prymnesjum is an often- erature as early as the late 19th century. This process cultivated and well-studied organism. Nevertheless, has recently been 'rediscovered' and its potential eco- for a long time, the only documentation of phagotrophy logical significance addressed as part of the rapid within this genus was an anecdotal description by evolution in microbial food web ecology. Many higher Conrad (1941), who described particle ingestion by algal taxa have species with both photosynthetic and pseudopodia in amoeboid cells of P. saltans Massart. phagotrophic nutrition (mixotrophy). This is most Little detail was given in that report and confirmatory common in the dinoflagellates (Schnepf & Elbrachter observations were lacking (Green 1991). However, 1992), chrysophytes (Sanders & Porter 1988) and prym- Nygaard & Tobiesen (1993) recently showed that P. nesiophytes (Green 1991, Jones et al. 1994). In the parvum, among several other species of flagellates, latter group, descriptions of mixotrophic species are was able to ingest bacteria both in the field and in the nearly exclusively restricted to the genus Chrysochro- laboratory. In the present study, I show that particle mulina. In only 1 case has phagotrophy been recorded ingestion by Prymnesium is not restricted to bacteria in the coccolithophorids (Parke & Adams 1960). but that at least P. patelliferum is able to incorporate Prymnesium Conrad, the type genus of Prymnesio- different sized particles, sometimes even larger than phyceae, has a number of toxic bloom-forming species itself. separated morphologically only by the fine-structural details of body scales (Green et al. 1982) and is well known to cause extensive fish kills in brackish ponds MATERIALS AND METHODS in Israel (Reich & Aschner 1947), Denmark (Otterstrsm & Steemann Nielsen 1940), Germany (Lenz 1933, Hickel In 1992, Prymnesium patelliferum was isolated from a brackish pond near Biisum, northern Germany. From this isolate, unialgal cultures were obtained by the 'E-mail: [email protected] dilution technique and were grown in natural seawater 0 Inter-Research 1998 156 Aquat Microb Ecol14: 155-160, 1998 (S = 28%) enriched with nutrients (Guillard & Ryther Table 1 List of species tested for their suitability as prey for 1962). Species determination, based on TEM examina- Pryrnnesium patelliferum tion of the scales, was carried out by J. Green (Ply- mouth Marine Laboratories, UK). Cultures were main- Species Diameter Ingestion tained at 20°C under natural light in the laboratory. To (pm) observed study phagotrophy, senescent cultures were mixed Unknown Chlorococcales 5-10 with different species of other protists (Table 1). Live DunalieUa sp. 7 observations were made using an inverted microscope Cryptornonas sp. 10 (Zeiss Axiovert 35) equipped with a Nikon photomicro- Skeletonema costaturn (Greville) Cleve 10 graphy system and documented with a Panasonic Thalassiosira rotula Meunier 3 0 Oxyrrhis manna Dujardin 3 0 video system. From video tapes, single frames were Gyrodinium sp. 45 printed by a Sony video-printer. Unknown amoeba 12 RESULTS pseudopodium (Fig. 1). Presumably, the formation of the pseudopodium is chemically stimulated and not In exponentially growing cultures, Prymnesium patel- triggered by direct contact with the prey, because it liferum is elongate and slender with 2 chloroplasts was often observed in cells not surrounded by algal covering the whole cell in the longitudinal axis. In food. If P. patelliferum with a pseudopodium en- dense and senescent cultures, the cell shape changes countered a food particle, the particle was completely to a more rounded form. The chloroplasts are smaller enclosed by the pseudopodium and taken up into a and the posterior part of the cell is often filled with a food vacuole located at the posterior of the cell within large body of reserve metabolite, probably chrysolam- about 1 min (Figs. 2 & 3). inarin. The cells are often filled with small oil droplets. In cultures of motile protists mixed with Prymnesium In addition, cells with a large brownish pellet in the patelliferurn, a varying number of potential prey cells posterior occurred and sometimes excretion of this lost their motility. This effect was not due to observation body by the cells was observed. These cellular fea- handling (e.g. microscopic illumination) as determined tures, with hindsight, possibly resulted from cannibal- by prey-alone control cultures under the microscope. ism, i.e. the brown bodies strongly resembled 'faecal For example, Fig. 4a shows the immobilised and pellets', suggesting the occurrence of phagotrophy. rounded form of an amoeba. This species can then eas- After mixing senescent Prymnesium patelliferum ily be ingested by P. patelliferum, as shown in Fig. 4b, c. cultures with other protist cultures, some P. patel- Single prey cells were often attacked by several liferurn cells showed a swollen and transparent poste- Prymnesium patelliferum cells simultaneously. Some- rior, which afterwards formed an elongated U-shaped times, when multiple P. patelliferurn encountered a single prey, the membranous pseudopodia of P. patelliferum cells appeared to merge to enclose the prey between them. This process is illustrated with a series of sequential images taken from video (Fig. 5). Resulting feeding aggregates of the 2-cell type are most common (Figs. 4c & 6a-e), but 3 or more P. patelliferurn cells may be involved (Fig. 6f). P. patelliferum also aggregated around relatively large prey. Both the heterotrophic dinoflagellate Oxyrrhis marina (Fig. 7) and the phototrophic Gyro- dinium sp. (Fig. 8) were attacked. The pre- dator cells formed a more or less complete coat over the prey. In such cases, the shape of a single P. patelliferurn cell could be extremely deformed. Differences in suitability of protistan prey for Prymnesiurn patelliferurn were observed. Fig. 1. Prymnesium patelliferum forming elongated pseudopodia While the Chlorococcales and an amoeba (arrows) at the posterior part of the cell pnor to feedng activity. Scale were ingested (Figs. 2 to 4)e the slmilarl~sized bar = 10 p Cryptomonas sp. and Skeletonerna costaturn Tillmann: Phagotrophy by a plastidic haptophyte 157 Figs. 2 & 3. Time course of prey ingestion by Pryrnnesiurn patelliferurn. The drawings in the lower part give a schematic simpli- fied view of pseudopod action. Scale bars = 10 pm. Fig. 2. P. patelliferurn ingesting an unidentified chlorococcalean alga. Fig. P. patelliferurn ingesting Dunaljella sp. Fig. 4. Prymnesium patelliferurn ingesting an amoeba. (a) After addition to a P. patemerum culture, the amoebae lost their motility and became rounded. (b)After ingestion, the amoeba can be seen in a large food vacuole. (c) Two cells in close connec- tion with the food between them. Scale bars = 10 pm 158 Aquat Microb Ecol 14: 155-160, 1998 U .- 2 - II 2 2 -2C 2 9 2; c 0 aJ 2 2al 5W 9" -g 6 g L 2 U c 0) 0 8 '= Fig. 6. Pryrnnesium patelliferurn. Examples of communal phagotrophy by ,U U0) (a-e) pairs or (f) a triplet of P. patellderum cells feeding on (a,b) unknown c c aJ c chlorococcalean algae or (c-f) DunalieUa sp. Scale bars = 10 pm 8 5 $ 5 0 were not captured (Table 1). Although suitable prey 'S : =v) items were apparently immobilised, Cryptornonas sp. motility was unaffected by the presence of l? patel- cE L g 2 liferum. .-0 DISCUSSION &V)U W =W c u The mode of particle ingestion of Prymnesium patel- 2 CY uc liferum by means of pseudopodial development at aJ 0 5 5 the non-flagellar pole resembled that of Chrysochro- U n) h.4 -1 mulina kappa Parke & Manton and C. ericina Parke 0 2 & Manton. Parke et al. (1955, 1956) described how a c 5 '30 V colourless, slightly granular substance seemed to " E, flow out from the non-flagellar pole of C. kappa and Ug 52 enveloped the prey particles, which were then drawn 5aJ 5;;; quickly inside the cell. I did not observe involvement of z Q the haptonema in the feeding process of P. patel- a! a liferum. This is in contrast to C, hirta Manton, in which 2 * $2 the haptonema plays an important role in catching and tr U taking up particles (Kawachi et al. 1991) aJ"'U a, 0 c The observations from this study suggest that prey a S 5 g are immobilised or even killed by Prymnesium pa- .2 telliferurn before being ingested. Cells being ingested .2 were, in every case, immobilised and rounded. Al- 3- though the toxicity of the P. patelliferurn strain used Q, here has not been tested with standard toxicity tests, -0 the rapid immobilisation of prey suggests toxin pro- duction, especially since the toxicity of 2 strains of P. patelliferurn was demonstrated in a recent study by Larsen et al. (1993). Thus, it may be speculated that Tillmann: Phagotrophy by a plastidic haptophyte 159 Fig.