Lateromyxa

1. Lateromyxa gallica Hulsmann, 1993 (ref. ID; 7275 original paper)

Lateromyxa gallica Hulsmann, 1993 (ref. ID; 7275 original paper)

Descriptions

• Light microscopy: The general shape of the freely floating or crawling specimens of Lateromyxa gallica resembles that of other isodiametrical vampyrelids. The uni- or multinucleated cells or syncytia (= trophozoites) are differentiated into a peripheral colourless zone (the cortical cytoplasm) and an inner more compact zone of bright orange-red or brick-red cytoplasm (the central cytoplasm). The diameters reach (without filopodia) from 26 to more than 150 um, depending on the number of previous confluence processes with conspecific individuals. Due the dense matrix of the central cytoplasm, the attempt to discriminate between distinct organelles is rather ineffectual. In the more transparent cortical region, the presence of regularly pulsating contractile vacuoles cannot be ascertained. The slender filopodia originate from the frontal region and, in smaller individuals, very often in clusters from the left and right flank of the frontal region. They radiate from the ventral as well as from the dorsal surface. All filopodia are rigid, with bases that are slightly thickened in comparison with the terminal region. In addition to individual filopodia, ramified one with common bases also occur. The filopodial surface is smooth, and membranosomes (a kind of membrane whorl visible throughout the filopodia of other reddish vampyrellids (Hulsmann 1985)) occur rarely. During normal movement, they very rapid and mostly invisible formation of the filopodia at the front is followed by affixing the tips for distal regions to the locomotion substrate. During and after shortening, a shifting of the base relative to the body region is demonstrable. After reaching an extreme lateral position, filopodia lose contact with the substrate, bend at their bases and, within a few seconds, are completely confluent with the caudal zone of the specimen. This characteristic behaviour gives the impression of a paddle-like crawling motion. In older cultures, larger syncytia appear that are the results of dozens or hundreds of fusions between smaller and formerly independent uni- or oligonucleated individuals. These syncytia, with diameters of up to 0.8 mm or more, are visible with the naked eye. They spread normally over the bottom of the culture vessel or investigation chamber and are immobile but not immotile as they exhibit body contractions that are obviously uncoordinated. The filopodia radiate from all sides and remain rather inactive, but sometimes they show rotating movements leading to screw-like outlines. Such syncytia normally undergo degeneration, but when exposed experimentally to intact Oedogonium filaments they initiate vampyrellid attacks as normal. Uninucleate cells and multinucleate syncytia start the attack by flattening the cell bodies and retracting the pseudopodia. The smaller multinucleated individuals, which are strongly attached to the algal surface, secrete a very delicate, short-persisting and sometimes undetectable cover, the pseudocyst. This covering is only visible after the cell has left the pseudocyst and seems to be nondemonstrable in fixed material. During the next 8 to 15 min, the lateral cell wall of Oedogonium is penetrated by an unknown physico-chemical process. The penetration results in a fenestration of the algal cell wall and leads to a circular hole with a diameter of about 6-8 um and to a corresponding operculum. After penetration the entire cell body of Lateromyxa gallica enters the lumen of the affected Oedogonium cell and engulfs the protoplasmic content. During this stage, the rather common and dramatic osmotic consequences that are observed in other vampyrellids (i.e. plant cell explosion, or plasmoptysis, with resulting injuries to the aggressor cell) (Hulsmann 1982) cannot be recorded. Depending on cell size and therefore on the number of nuclei of Lateromyxa gallica, the following attacks are directed against only one or against both of the adjacent plant cells. When both plant cells are involved, the invader divides into two individuals. In all cases, the cross wall is penetrated in the same way as the lateral wall during the initial attack. Under the better optical conditions inside the filament, the different aspects of the cellular assault can be analyzed in more detail. The attacking area appears to be more homogeneous; and the operculum is clearly seen to be pressed by the turgor into the cell body of Lateromyxa gallica. Within the next minutes, the affected plant cell collapses under the loss of turgor, and the shrunken protoplast is englufed by a bell-shaped ingestion pseudpodium, the calyculopodium. Several subsequent attacks are possible. The trophozoite enters the emptied cell and migrates through the filament to the next cross wall. However, only the frontal regions are involved in this kind of phagotrophy. The caudal parts, filled with green food vacuoles, are separated by division from the rest of the syncytium and are left behind. One or two daughter cells remain in the emptied algal cell. They round up and undergo encystation, while the frontal region, which becomes smaller from attack to attack, continues feeding. At the end of this phase, which lasts for up to about 2 h, the peripheral parts also undergo encystation. The result is a row of normally 2-8 but sometimes up to 15 cysts lying inside the Oedogonium filament, one or two per plant cell. The cysts are globular or ovoid. Inside the natural Oedogonium species, they possess normally the maximal possible width (about 25 um) which corresponds to the inner diameter of the algae. Up to the next day or the day after that, the food is digested and the typical bright orange-red colour of the species reappears. In mature digestive cysts, the food vacuoles with dark-brown egesta are arranged peripherally. As in most vampyrelids (Gobi 1915; Hulsmann 1982, 1985), excystation occurs preferentially in the late afternoon. The cytoplasmic contents of globular cysts are normally expelled as undivided cell, whereas two (or four) trophozoites are released from the ovoid cysts. Exocytosis of debris takes place during excystation. Most of the excysted cells are uninucleate. The young trophozoites behave differently: those from cysts beside intact plant cells continue to feed, others migrate along the interior of the filament and leave the filament through the initial opening or through new penetration holes. After emigration they have the same features of trophozoites as described above. They form larger syncytia whenever they come into contact with conspecific partners. In older cultures, or under unfavourable conditions, as well as in the reddish algal wads isolated from Lac Pavin, a second type of cyst can be found. Instead of leaving the cystic envelope as others do, some specimens excrete the debris and secrete and additional cystic wall around the cytoplasm. Such cysts serve as resting stages; they are able to withstand desiccation and freezing. Under laboratory conditions, excystment of 3-yr-old resting cysts takes place after transferring them to fresh medium or to growing algal cultures. (ref. ID; 7275)
  • Trophozoites. Living individuals without filopodia between 26 um and 35 um (uninucleate cells) and up to 800 um and more (multinucleate syncytia). Obligatory fusion of cells and syncytia after contact with conspecific individuals. Cell body and smaller syncytia radially symmetrical, others bilaterally symmetrical with width as greatest dimension, or variable. Cortical cytoplasm hyaline and colourless, in larger individuals often vacuolated central cytoplasm compact granular and of bright red-orange or brick-red colour. Filopodia mostly unbranched, stiff and slender, up to 40 um in length, originating from the frontal or frontolateral regions and disappearing at the caudal zone by lateral fusion with the cell surface. Pseudopodia with axial filament bundles. Nuclei 3.1-5.1 um in diameter and surrounded by one additional cisterna of the endoplasmic reticulum. Chromosomes compact and discernible during interphase. One or two compact nucleoli in peripheral location. Mitochondria with conspicuous ribosomal (polysomal) aggregates and with tubular cristae terminating in dilated sacs. Dictyosomes with 3-5 lacunae in all cell regions. Feeds exclusively on Oedogonium species, penetrating their lateral cell walls and engulfing the cytoplasmic contents. Attacks performed from a semiencysted stage without filopodia. Invades the algal interior and attacks other cells by penetrating the cross walls. During invasion of the algal filament, normally divides into daughter cells or daughter syncytia, combined with the formation of digestive and reproductive cysts. (ref. ID; 7275)
  • Digestive-reproductive cysts. Formation exclusively inside Oedogonium filaments. Dimensions normally limited in width by the inner diameter of the algal specimen (23-28 um), but not depending on it is broader algal filaments. Globular or ovoid. Initially green or brown-green, later on with the red-orange colour of trophozoites. One filamentous cystic wall. Excystation after one or two days, performed by one undivided or two or four divided individuals. Nuclei larger (diameter 7.2-8.9 um) without additional cisternal envelope, but with condensed chromosomes affixed to the inner nuclear membrane. Mitochondria with conspicuous DNA-like threads, but without ribosomal aggregates. (ref. ID; 7275)
  • Resting cysts. Reddish and without inclusions visible by light microscopy. Diameters about half that of digestive cysts. Formation exclusively inside Oedogonium filaments. Initiated from digestive cysts after exocytosis of undigested remnants and then formed by the secretion of one additional cystic wall. Resistant against drying and freezing for several years. (ref. ID; 7275)
• Electron microscopy: The cell membranes of cells and syncytia of Lateromyxa are completely naked and exhibit no pronounced mucous layes or any other extracellular deposits. The cortical cytoplasm contains an elaborated network of vacuoles, smooth endoplasmic reticulum, membranous sacs of cisternae and more or less dense membranosomes as constitutive parts of other membrane systems. As in Vampyrella lateritia, some of these membranosomes communicate with the cell membrane (Hulsmann 1985). They are lacking in regions in which larger vacuoles dominate. Beside these organelles, other electron-dense vesicles occur. They contain membranous remnants possibly representing undigested plastid material. In multinucleate syncytia, the cortical cytoplasm shows a greater number of vacuoles. Other constituents of the cortical cytoplasm are ribosomes, normally randomly distributed but sometimes also in paracrystalline arrays. Cytoplasmic microtubules are present during late stages of invasion. The filopodia are stiffened by a central core embedded within a dense amorphous matrix. The core consists of 7-nm filaments running parallel to the long axis. The central cytoplasm contains nuclei, lipid droplets, paracrystalline and conventional ribosomal aggregate, and vacuoles with amorphous of membranous remnants. Mitochondria and dictyosomes with 3-5 cisternae are distributed throughout the cell. No intracellular bacteria are detectable. The nuclei of trophozoites and cysts are characterized by chromatin areas condensed to discernable chromosomes. Chromatin layers can also be found beneath the inner nuclear membrane. The nuclear envelope is simple in cysts, but the nuclei of trophozoites are enveloped by an additional cisterna of endoplasmic reticulum. Mitochondria undergo changes during the life cycle. In the trophozoites of Lateromyxa gallica, they exhibit a central accumulation of clustered or spirally arranged polysomes. The cristae are tubular and terminate in vesicular swellings. Mitochondria of encysted stages are often accumulated in the periphery. Instead of mitochondrial ribosomes, putative DNA strands are now clearly visible and can be shown sometimes to accumulate to a so-called "mitochondrial nucleus". (ref. ID; 7275)

Remarks

• 1. The radial symmetry of smaller cell bodies, which is congruent with the morphology of the other type species (Gobi 1915; Hulsmann 1985; Old & Darbyshire 1980; Schepiatoff 1912; Zopf 1885), except Hyalodiscus (this widespread character, however, is found also in the possibly non-related genera Nuclearia and Vampyrellidium (Lee et al. 1985; Page & Siemensma 1991; Patterson 1983; Patterson et al. 1987; Zopf 1885));
• 2. The pseudopodia which do not show any indication of the presence of microtubules but do exhibit microfilaments as in other members of the vampyrellids (Hulsmann 1985) (but also in Vampyrellidium perforans (Patterson et al. 1987));
• 3. The obligatory fusion of conspecific individuals to larger and also amorphous syncytia which leads-if it happens extensively- to the formation of immobile organisms;
• 4. the ulrastructure of mitochondria with vesiculate cristae (Hausmann 1977; Old & Darbyshire 1980) and with ribosomal aggregates;
• 5. The reddish colour as a putative morphological remnant of the algal diet which is reported for all marine and freshwater vampyrellids living on Rhodophyta or Chlorophyta (Gobi 1915; Hoogenraad 1907; Hulsmann 1982, 1985; Poisson & Mangenot 1933; Schepiatoff 1912; Timpano & Pfiester 1986; Zopf 1885);
• 6. the manner of food uptake by penetrating cell walls of algae, and the following activity of one or two ingestion pseudopods (Gobi 1915; Hulsmann 1982, 1985; Old & Chakraborty 1986);
• 7. The method used to produce an aperture by cutting out opercula as described for Vampyrella closterii (Poisson & Mangenot 1933) and Arachnula (Old & Darbyshire 1980; Old & Chakraborty 1986) and noticed also for Vampyrella pendula and Gobiella borealis (N.H., pers. observ.);
• 8. The obligatory formation of digestive cysts immediately after food uptake as well as the ability to form resting cysts (Gobi 1915; Hulsmann 1985; Old & Darbyshire 1980; Old & Chakraborty 1986; Poisson & Mangenot 1933; Timpano & Pfiester 1986; Zopf 1885);
• 9. The presence of osmiophilic granules or membranosomes which function as membrane reservoirs in Vampyrella lateritia (Hulsmann 1985) are also typical constituents of the cytoplasm of Arachnula (Old & Darbyshire 1980), Hyalodiscus and Gobiella (N.H., pers. observ.);
• 10. The presence of cytoplasmic ribosomal aggregates in paracrystalline clusters (as seen in Vampyrella lateritia (Hausmann 1977) and Arachnula (Old & Darbyshire 1980) and which are typical also for Hyalodiscus, Vampyrella closterii and Gobiella borealis (N.H., pers. observ.)

• 1. The moving behavior of filopodia, especially the fusion of their flanks with the rear cell surface during the backward stroke;
• 2. The obligatory formation of a pseudocyst during penetration of the lateral cell wall;
• 3. The regular penetration of cross walls from inside the vanished plant cells as allusively found only in Hyalodiscus rubicundus (Hoogenraad 1907) or Arachnula impatiens (Old & Darbyshire 1980; Old & Chakraborty 1986);
• 4. The formation of digestive cysts and resting cysts exclusively within vanished cells of Oedogonium;
• 5. The presence of condensed chromatin having the appearance of individual chromosomes detectable during the whole cell cycle (similar characters are otherwise found in Euglenida and micronuclei of some Ciliophora (Lee et al. 1985));
• 6. The additional cisterna of the endoplasmic reticulum which surrounds the nucleus or trophozoites. From these unambiguous characters the establishment of a new taxon seems to be favourable. The first four signs, which are recognizable by contrast-enhancing light microscopic techniques, provide sufficient criteria to distinguish L. gallica with certainty from all other known sea- and freshwater vampyrellids. After fine structural investigations of new isolates, the chromosomal features and the nucleus-associated additional endoplasmic reticulum membranes can reveal further confirmation of identity. If the unique feature of the nuclear characters is not overinterpreted, the next relatives of Lateromyxa may be found in the genera Arachnula or Hyalodiscus. (ref. ID; 7275)

Etymology

Ecology

Type locality

Type specimens