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A microtubular basket in the armoured dinoflagellate Prorocentrum micans (Dinophyceae)
Arch. Protistenkd. 138 (1990): 89-91 VEB Gustav Fischer Verlag lena
Zellenlehre, Fakultat fiir Biologie, University of Heidelberg, F.R.G.
A Microtubular Basket in the Armoured Dinoflagellate Prorocentrum micans (Dinophyceae) By E. SCHNEPF & SUSANNE WINTER With 4 Figures Key words: Annoured dinoflagellate; Prorocentrum micans; Microtubular basket
Summary The existence of a microtubular basket in Prorocentrum micans is described. It ends at the flagellar pit with a sphincter.
Introduction Prorocentrum species are extensively investigated dinoflagellates (for recent ultrastructural studies see e.g. FRITZ & TRIEMER 1983; PREVOT & SOYER 1985; KLUT et al. 1986; MALCOLM & WETHERBEE 1987). They are autotrophic. We, nevertheless, observed in Prorocentrum micans a microtubular basket, i.e., a structure which indicates that it might also feed on living prey.
Material and Methods Prorocentrum micans EHRENBERG was kindly supplied by Dr. G. DREBES, Biologische Anstalt Helgoland, Litoralstation ListlSylt, cultivated in the f/2 sea water medium (McLACHLAN 1973), fixed with glutaraldehyde and OS04 (usually simultaneously at 4°C; 1.25 % glutaraldehyde plus 0.4 % OS04 dissolved in the culture medium) and embedded in SPURR'S medium.
Resnlts and Discussion Unexpectedly we found a structure not described or identified as yet. It begins at the flagellar pit (Figs. 1, 2), close to another pit which is surrounded by mucilage vesicles ("mucilage pit") (Figs. 1, 2) and consists of rows of microtubules forming a cylinder (Figs. 3, 4). It runs nearly parallel to the surface of the cell (Fig. 1), and extends some micrometers into the cell. Its distal end is surrounded by a collar of electron dense material (sphincter, Figs. 1, 2, 3). It is accompanied by small, round vesicles with electron transparent contents (Fig. 4) and oblong vesicles which are filled with electron dense material (Figs. 1, 2, 3). The position of the structure, the arrangement of microtubules, the distal sphincter and the two types of characteristic vesicles clearly show that it is a microtubular basket, i.e. a non-emerged feeding tube (SPERO 1982; SPECTOR 1984; SCHNEPF et al. 1985; BROWN et al. 1988; LARSEN 1988). A feeding tube was detected in various heterotrophic dinophytes (see SCHNEPF et a1. 1985 and LARSEN 1988 for references); it is generally used to suck out prey organisms (myzocytosis, SCHNEPF & DEICHGRABER 1984). A microtubular basket had been observed in the armoured,
90
E.
SCHNEPF
& S.
WINTER
Figs. 1-4. Prorocentrum micans; F = flagellum outside the cell; f = flagellum in the flagellar pit; m pit; p = pusule; s = sphincter; T = apical tooth; V = mucilage vesicles.
= mucilage
Fig. 1. Longitudinal section through the cell apex with apical tooth , mucilage pit, flagellar pit and a microtubular basket in longitudinal section. Fig. 2. As Fig. 1, higher magnification. Fig. 3. Microtubular basket with oblong, dense vesicles. Fig. 4. Microtubular basket with round, electron transparent vesicles.
A Microtubular Basket in the Annoured Dinoflagellate
91
autotrophic Ceratium hirundinella (DODGE & CRAWFORD 1970). A similar structure was found by FAUST (1974) in Prorocentrum mariae-lebouriae, but not identified as a microtubular basket. Obviously it has been overlooked in other studies on Prorocentrum micans. Its occurrence suggests that Prorocentrum species, at least P. micans and P. mariae-lebouriae, do not exclusively live autotrophically but can also feed myzocytolically, confirming that this kind of nutrition is found among armoured dinoflagellates as well. The present results show that microtubular baskets (and therewith peduncles or feeding tubes) are not restricted to highly "advanced" dinoflagellates, but occur in "primitive" ones 100 (see FRITZ & TRIEMER 1983). We thank Mr. W. WINTER for correcting the text. With support of the Deutsche Forschungsgemeinschaft.
Literature BROWN , D . L. , CACHON , I. , CACHON, M ., & BOILLOT , A . (1988): The cytoskeletal microtubular system of some naked dinoflagellates. Cell Motil. Cytoskel. 9: 361- 374. DODGE , 1. D., & CRAWFORD , R. M. (1970): The morphology and fine structure of Ceratium hirundinella (Dinophyceae). 1. Phycol. 6: 137-149. FAUST , M. A. (1974): Micromorphology of a small dinoflagellate Prorocentrum mariae-lebouriae (PARKE & BALLATINE) comb. nov. 1. Phycol. 10: 315-322. FRITZ, L., & TRIEMER, R. E. (1983): An ultrastructural study of mitosis in a marine dinoflagellate: Prorocentrum minimum. J. Protozool. 30: 437-444. KLUT , M. E. , BISALPUTRA, T.; & ANTIA , N . J. (1987): Some observations on the structure and function of the dinoflagellate pusule. Can. J. Bot. 65 : 736-744. MALCOLM, S. M. , & WETHERBEE, R. (1987): Serial reconstruction and behaviour during cytokinesis of the chondriome of ProrocenlrUIn minimum (PAVILLARD) SCHILLER (Pyrrhophyta) . Protoplasma 138: 32-36. McLACHLAN , J. (1973) : Growth media - marine. In: STEIN , J. R. (ed .), Handbook of phycological methods, culture methods and growth measurements, pp. 25-5\. Cambridge. PREVOT, P. , & SOYER, M.-O. , (1985): Action of the organophosphorous insecticide parathion on the free-living marine dinoflagellate Prorocelltrum micalls EHRBG. J. Protozool. 32: 626-633 . SCH NEPF , E., & DEICHGRABER, G . (1984): "Myzocytosis", a kind of endocytosis with implications 10 compartmcntation in endosymbiosis. Naturwissenschaften 71: 218. - DEICHGRABER, G., & DREBES, G. (1985) : Food uptake and the fine structure of the dinophyte Paulsenella sp. , an ectoparasite of marine diatoms. Protoplasma 124: 188-204. SPECTOR, D. L. (1984): Unusual inclusions . In: SPECTOR, D. L. (ed.), Dinoflagellates , pp. 365-390. New York. SPERO, H. (1982): Phagotrophy in Gymnodinium fungiforme (Pyrrhophyla): the peduncle as an organelle of ingestion. 1. Phycol. 18: 356-360 Address of the corresponding author : Prof. Dr. E. SCHNEPF, Zellenlehre, Fakultat fUr Biologie, University of Heidelberg , 1m Neuenheimer Feld 230, D - 6900 Heidelberg.
Zellenlehre, Fakultat fiir Biologie, University of Heidelberg, F.R.G.
A Microtubular Basket in the Armoured Dinoflagellate Prorocentrum micans (Dinophyceae) By E. SCHNEPF & SUSANNE WINTER With 4 Figures Key words: Annoured dinoflagellate; Prorocentrum micans; Microtubular basket
Summary The existence of a microtubular basket in Prorocentrum micans is described. It ends at the flagellar pit with a sphincter.
Introduction Prorocentrum species are extensively investigated dinoflagellates (for recent ultrastructural studies see e.g. FRITZ & TRIEMER 1983; PREVOT & SOYER 1985; KLUT et al. 1986; MALCOLM & WETHERBEE 1987). They are autotrophic. We, nevertheless, observed in Prorocentrum micans a microtubular basket, i.e., a structure which indicates that it might also feed on living prey.
Material and Methods Prorocentrum micans EHRENBERG was kindly supplied by Dr. G. DREBES, Biologische Anstalt Helgoland, Litoralstation ListlSylt, cultivated in the f/2 sea water medium (McLACHLAN 1973), fixed with glutaraldehyde and OS04 (usually simultaneously at 4°C; 1.25 % glutaraldehyde plus 0.4 % OS04 dissolved in the culture medium) and embedded in SPURR'S medium.
Resnlts and Discussion Unexpectedly we found a structure not described or identified as yet. It begins at the flagellar pit (Figs. 1, 2), close to another pit which is surrounded by mucilage vesicles ("mucilage pit") (Figs. 1, 2) and consists of rows of microtubules forming a cylinder (Figs. 3, 4). It runs nearly parallel to the surface of the cell (Fig. 1), and extends some micrometers into the cell. Its distal end is surrounded by a collar of electron dense material (sphincter, Figs. 1, 2, 3). It is accompanied by small, round vesicles with electron transparent contents (Fig. 4) and oblong vesicles which are filled with electron dense material (Figs. 1, 2, 3). The position of the structure, the arrangement of microtubules, the distal sphincter and the two types of characteristic vesicles clearly show that it is a microtubular basket, i.e. a non-emerged feeding tube (SPERO 1982; SPECTOR 1984; SCHNEPF et al. 1985; BROWN et al. 1988; LARSEN 1988). A feeding tube was detected in various heterotrophic dinophytes (see SCHNEPF et a1. 1985 and LARSEN 1988 for references); it is generally used to suck out prey organisms (myzocytosis, SCHNEPF & DEICHGRABER 1984). A microtubular basket had been observed in the armoured,
90
E.
SCHNEPF
& S.
WINTER
Figs. 1-4. Prorocentrum micans; F = flagellum outside the cell; f = flagellum in the flagellar pit; m pit; p = pusule; s = sphincter; T = apical tooth; V = mucilage vesicles.
= mucilage
Fig. 1. Longitudinal section through the cell apex with apical tooth , mucilage pit, flagellar pit and a microtubular basket in longitudinal section. Fig. 2. As Fig. 1, higher magnification. Fig. 3. Microtubular basket with oblong, dense vesicles. Fig. 4. Microtubular basket with round, electron transparent vesicles.
A Microtubular Basket in the Annoured Dinoflagellate
91
autotrophic Ceratium hirundinella (DODGE & CRAWFORD 1970). A similar structure was found by FAUST (1974) in Prorocentrum mariae-lebouriae, but not identified as a microtubular basket. Obviously it has been overlooked in other studies on Prorocentrum micans. Its occurrence suggests that Prorocentrum species, at least P. micans and P. mariae-lebouriae, do not exclusively live autotrophically but can also feed myzocytolically, confirming that this kind of nutrition is found among armoured dinoflagellates as well. The present results show that microtubular baskets (and therewith peduncles or feeding tubes) are not restricted to highly "advanced" dinoflagellates, but occur in "primitive" ones 100 (see FRITZ & TRIEMER 1983). We thank Mr. W. WINTER for correcting the text. With support of the Deutsche Forschungsgemeinschaft.
Literature BROWN , D . L. , CACHON , I. , CACHON, M ., & BOILLOT , A . (1988): The cytoskeletal microtubular system of some naked dinoflagellates. Cell Motil. Cytoskel. 9: 361- 374. DODGE , 1. D., & CRAWFORD , R. M. (1970): The morphology and fine structure of Ceratium hirundinella (Dinophyceae). 1. Phycol. 6: 137-149. FAUST , M. A. (1974): Micromorphology of a small dinoflagellate Prorocentrum mariae-lebouriae (PARKE & BALLATINE) comb. nov. 1. Phycol. 10: 315-322. FRITZ, L., & TRIEMER, R. E. (1983): An ultrastructural study of mitosis in a marine dinoflagellate: Prorocentrum minimum. J. Protozool. 30: 437-444. KLUT , M. E. , BISALPUTRA, T.; & ANTIA , N . J. (1987): Some observations on the structure and function of the dinoflagellate pusule. Can. J. Bot. 65 : 736-744. MALCOLM, S. M. , & WETHERBEE, R. (1987): Serial reconstruction and behaviour during cytokinesis of the chondriome of ProrocenlrUIn minimum (PAVILLARD) SCHILLER (Pyrrhophyta) . Protoplasma 138: 32-36. McLACHLAN , J. (1973) : Growth media - marine. In: STEIN , J. R. (ed .), Handbook of phycological methods, culture methods and growth measurements, pp. 25-5\. Cambridge. PREVOT, P. , & SOYER, M.-O. , (1985): Action of the organophosphorous insecticide parathion on the free-living marine dinoflagellate Prorocelltrum micalls EHRBG. J. Protozool. 32: 626-633 . SCH NEPF , E., & DEICHGRABER, G . (1984): "Myzocytosis", a kind of endocytosis with implications 10 compartmcntation in endosymbiosis. Naturwissenschaften 71: 218. - DEICHGRABER, G., & DREBES, G. (1985) : Food uptake and the fine structure of the dinophyte Paulsenella sp. , an ectoparasite of marine diatoms. Protoplasma 124: 188-204. SPECTOR, D. L. (1984): Unusual inclusions . In: SPECTOR, D. L. (ed.), Dinoflagellates , pp. 365-390. New York. SPERO, H. (1982): Phagotrophy in Gymnodinium fungiforme (Pyrrhophyla): the peduncle as an organelle of ingestion. 1. Phycol. 18: 356-360 Address of the corresponding author : Prof. Dr. E. SCHNEPF, Zellenlehre, Fakultat fUr Biologie, University of Heidelberg , 1m Neuenheimer Feld 230, D - 6900 Heidelberg.