Sorogena
Sorogena Bradbury & Olive (ref. ID; 3864 original paper)
Class Colpodea Small & Lynn, 1981: Subclass Colpodia Foissner, 1985: Order Sorogenida Foissner, 1985: Family Sorogenidae Bradbury & Olive, 1980 (ref. ID; 4366)
Family Sorogenidae (ref. ID; 3864 original paper)
[ref. ID; 3864]
Trophic stage with apical slit-like cytostomes, rhabdos type of pharyngeal apparatus, uniform ciliation, dikinetids in somatic kineties, and circumoral infraciliature; ciliates aggregating and forming aerial sorocarps, each consisting of a furrowed stalk bearing a round mass of sorocysts apically. (ref. ID; 3864)
Etymology; The species is named in honor of Miss Carmen Stoianovitch, who first observed the sorocarps of what is probably this organism on dead parts of corn plants. (ref. ID; 3864)
Type species; Sorogena stoianovitchae (ref. ID; 3864)
- Sorogena stoianovitchae Bradbury & Olive, 1972 (ref. ID; 3872), 1980 (ref. ID; 4116, 4366) or 1981 (ref. ID; 3864 original paper, 4107) reported author and year? (ref. ID; 191, 7118)
Sorogena stoianovitchae Bradbury & Olive, 1972 (ref. ID; 3872), 1980 (ref. ID; 4116, 4366) or 1981 (ref. ID; 3864 original paper, 4107) reported author and year? (ref. ID; 191, 7118)
Diagnosis
Trophic stage 40-75x23-55 um, usually with 22-24 meridional kineties curving slightly at the posterior end; pore of water-expulsion vacuole on posterior ventral surface; spherical macronucleus in middle of body and single micronucleus in macronuclear indentation; resting cysts on substrate 23-55 um diameter. Sorocarps apically tapered, with furrowed stalk sheath, 293-1,121 um tall; sori 98-488 um in diameter, containing up to several hundred sorocysts 18-32 um in diameter; sorocarps occasionally minute and with as few as 4 sorocysts. (ref. ID; 3864)
Descriptions
The newly excysted ciliate is slender, about half as wide as it is long, with a slight graceful curve to its somewhat flattened body. Even before growth has taken place it is possible, under a stereomicroscope, to distinguish Sorogena from the prey organism by its purposeful swimming and silvery refractile appearance. Most of its kineties curve around the dorso-ventrally flattened body, ending on the side opposite their origin. The slit-like cytostome is apical but displaced to the left and slanted posteriorly. It is surrounded by a naked lip that projects forward 1-2 um, and there is a shoulder or slight hump on the dorsal side that tilts the cytostome ventrally. The somatic kineties are separated from each other by projecting cytoplasmic crests, and their number and course are best seen in preparations stained with silver according to the Chatton-Lwoff method. Each kinety is a row of pairs of kinetosomes, the kinetosomes of the pair lined up one behind the other, and each pair spaced apart from the other pairs in the row, the spaces becoming longer toward the posterior pole of the organism. A single large, posterior, water-expulsion vacuole opens on the dorsal surface at the termination of the 4 shortest kineties. The 22-24 kineties are spaced almost equidistantly, but all converge at the cytostome, ending at the base of the lip. The shape and proportions of the ciliate are better preserved in preparations stained by the Chatton-Lwoff method than in those stained with protargol, perhaps because of the difference in the fixative (glutaraldehyde vs. Bouin's). The slit-like cytostome of the living or glutaraldehyde-fixed ciliate is pursed in protargol-impregnated preparations as if closed by a drawstring, and the height of the lip is doubled. With protargol the cytoplasm of the body stains light purple, while the lip remains a faint pink, the somatic kineties converge at the base of the lip, extra kinetosomes being inserted beside the anteriormost kinetosomes of the kineties to complete the ring. Two or 3 of the kineties appear to extend a very short distance up the lip; because of the pursing of the cytostome, their precise location in uncertain. They seem to be about mid-point on the ventral surface of the lip and sometimes stain more intensely than the terminations of adjacent kineties. The macronucleus also impregnates with protargol. It is located in the middle of the body, usually circular in outline, less frequently ovoid or elliptical. This ciliate is a voracious predator that feed on species of Colpoda, and, when the latter is depleted in numbers, aggregates to forms sorogens. Each sorogen rises into the air from the surface of the water, forming a secreted stalk with a sorus of cysts at its apex. (ref. ID; 3864)
[ref. ID; 4366]
A young theront of S. stoianovitchae recently escaped from a sorocarp cyst and not yet filled with too many food vacuoles measures 30-40x20-30 um in vivo. The cell is more or less reniform and compressed laterally. The outline of its ventral side is sigmoid whereas the dorsal side is slightly convex. The trophic stage of S. stoianovitchae is almost circular in cross section. Depending on the degree of food intake the trophont measures 50-70x30-45 um. In both stages, the theront and the trophont, the elliptical cytostome is located on a domed elevation in a subapical position. In living cells (this holds also for fixed cells) the oral ciliature at the base of the oral dome is difficult to distinguish from the somatic ciliature. The cell has an almost spherical macronucleus, 15-18 um in diameter and a single separate micronucleus, 2.5-3 um in diameter. Both nuclei are located in the middle of the cell and may be difficult to detect in living trophonts due to the numerous food vacuoles. There is one subterminal contractile vacuole with a single excretory pore on the right-ventral side near the posterior end of the cell as well as a slit-like cytoproct near the excretory pore two kineties to the left. The position of the contractile vacuole and the cytoproct are shown in a camera lucida drawing of a silver nitrate impregnated cell. When swimming the ciliate rotates about its longitudinal axis. On the bottom of the culture dish Sorogena creeps. When slightly compressed under a cover slip, the cell shows a high degree of flexibility, performing an almost amoeboid movement. The somatic cortex shows 18-21 kineties composed exclusively of dikinetid. The kineties on the right side of the cell are slightly shorter than those on the left side and terminate in front of the pore of the contractile vacuole. The somatic cilia measure 7-8 um in length. As seen clearly in the scanning micrographs, two adjacent kineties are separated by a cytoplasmic crest as described by Bradbury & Olive (1980). The somatic kineties take a spiral course. Seen from outside of the cell, and from the anterior to the posterior pole, the kineties take a counterclockwise turn. The drawing of S. stoianovitchae given by Bradbury & Olive (1980) is incorrect in showing the somatic kineties running in a clockwise orientation, a mistake that is easily made by focusing to the "inappropriate" plane. Our figure shows a clockwise orientation of the somatic kineties. In this particular case it had to be focused through the cell to picture the oral apparatus, which was lying "underneath the cell'. Only when seen from inside the cell the somatic kineties run in a clockwise orientation. Sorogena stoianovitchae has a colpodid silverline system. Vertical silverlines connect the somatic dikinetids. At higher magnification an elliptical silverline is visible around every dikinetid. It is mostly from these dikinetid territories that highly wavy horizontal silverlines pass to the neighboring vertical silverlines. In small irregularly placed areas of the somatic cortex short semimedian silverlines are seen in addition. The oral ciliature is located around the outer base of the naked oral dome seen most clearly in freeze-fracture replicas. The paroral ciliature consists of a double row of fairly short cilia about 5 um in length, and arranged in a C-shape, thus encompassing the dorsal and the ventral part of the oral dome. On the left side of the oral dome there are 3-5, but most often 4 adoral organelles. Silver-stained specimens show that the adoral organelles consist of 6-8 kinetosomes, but as seen in freeze-fracture replicas only 4-5 of these kinetosomes are ciliated. (ref. ID; 4366)
Morphogenesis: Vegetative reproduction in S. stoianovitchae takes place by bipartition. Contrary to colpodid ciliates s. str., cell division in S. stoianovitchae does not occur in a division cyst but in the free swimming condition. It is only during the last stage of division immediately prior to the separation of the two daughter cells that the dividing cell rest motionless on the bottom of the culture dish. It is now widely recognized that a comprehensive understanding of ciliate morphogenesis from light microscopy is an absolute prerequisite for the study of this process by electron microscopy. As the first step we have undertaken a careful study of stomatogenesis and cell division of S. stoianovitchae using pyridinated silver carbonate impregnated cells. The Fernandez-Galiano method is a powerful technique to disclose every single kinetosome, but it should also be noted that owing to compression by the coverslip, the cell shape is often distorted in photographs. The entire process, shown in a series of camera lucida drawings is describe as follows. As the first sign of a beginning cell division a proliferation of kinetosomes is seen in 5-6 right lateral somatic kineties close above the excretory pore of the contractile vacuole. These zones of kinetosomes proliferation become larger and while the macronucleus begins to elongate the split into an anterior and a posterior portion. Both portions will give rise to the oral ciliature of the opisthe. In the next step, which shows a dumbbell-shaped constriction of the macro- and the adjacent micronucleus, the future adoral dikinetids in front of their somatic kineties have become arranged in 4-5 compact adoral organelles. At the same time the anterior portion of the oral dikinetids is alinged in three or four broken rows, which lie perpendicular to the adoral organelles. A single bowed argentophilic structure is easily identified as the paroral ciliature of the opisthe. Meanwhile an oblique cleavage furrow appears in front of the oral ciliature of the opisthe. It cuts the parental cell into two daughter cells as soon as the nuclear division is finished. The divisions of the micronucleus is finished before the division of the macronucleus. The final separation of the daughter cells seems to be brought about by a kind of rotational movement of the proter relative to the opisthe about 45 degrees from the plane of division. In the latter stage of division the paroral dikinetids become visible as separate entities. No signs of reorganization are to be seen in the parental oral structures and in the silverline system. The mode of kinetosomes proliferation in the somatic cortex deserves an additional remark. The process starts with a separation of the two kinetosomes of a somatic dikinetid, then in front of the anterior kinetosome a new kinetosome appears, resulting in typical triads. A short time later a fourth kinetosome appears in front of the posterior parental kinetosomes, thus resulting in a quadrupling of kinetosomes that later separates to form two dikinetids. What we regard to be the new kinetosomes usually appear as smaller agentophilic dots compared to old kinetosomes. During kinetosome proliferation the new kinetosomes are not seen in straight with the course of the kinety, but are shifted slightly to the anterior left quarter in front of their parental inducer. Finally, the two new dikinetids, being the result of a "semi-conservative" mode of replication, separate further and arrange themselves in a straight line with the somatic kinety. Because of the restricted resolution of the light microscope not all the details of kinetosome proliferation could be detected, but it appears that more than one round of kinetosome replication takes place to cope with the demand for a high number of kinetosomes in the future oral apparatus. (ref. ID; 4366)
Remarks
Systematic position: In the original description of S. stoianovitchae the ciliate was regarded as a member of the Haptorida. Bradbury & Olive recognized that S. stoianovitchae did deviate in several aspects from typical haptorids even though it resembles the genus Enchelys in some respects (Bradbury & Olive 1980). There is the absence in S. stoianovitchae of toxicysts, extrusomes typically found in the voracious haptorids. It was noted that the numerous inclusion bodies located around the anterior part of the cytopharynx differed considerably from typical toxicysts, although they may be involved in the digestion of the prey as the authors suggested (Bradbury & Olive 1980). Mucocysts of exist in great number in S. stoianovitchae, but are extremely difficult to preserve. The majority of the foamy-looking areas described by Bradbury & Olive (1980) as "inflated cisternae of the endoplasmic reticulum" seem to be extrusomes, exploded within the cell. Mucocysts were found to play a central role in the process of sorocarp formation (Blanton & Olive 1982). Bradbury & Olive noticed the absence of a fibrous stratum, which in many haptorids separate the bulk of the endoplasm from a cortical layer of ectoplasm. Moreover, S. stoianovitchae lacks the clavate cilia typical for many haptorids. Although these and other features (e.g. the somatic dikinetids) did not fit with the diagnosis of the Haptorida , S. stoianovichae was regarded as an atypical member of the Haptorida placed in a new family, the Sorogenidae (Bradbury & Olive 1980). Bradbury & Olive regarded this ciliate as a proper gymnostome equipped with a continuous perioral ciliature. The naked lip, the comparatively simple cytopharynx and the circular array of nematodesmata seemed to justify the proposed systematic position. Now what are the characteristics that favor the assignment of S. stoianovitchae with the Colpodea? As first noticed by Small & Lynn (1981) somatic dikinetids of S. stoianovitchae do not show the haptorid, but instead show the typical colpodid pattern. The silverline pattern of the somatic cortex of S. stoianovitchae resembles the silverline pattern of the colpodid ciliates Cyrtolophosis (Foissner 1978), Sagittaria (Foissner et al. 1981), and Colpoda (Foissner 1985). The somatic and oral infraciliature of S. stoianovitchae is almost identical to the infraciliature of Sagittaria (Foissner 1978) and Platyophrya (Foissner 1978; Foissner et al. 1981). The similarity between Sorogena and Platyophrya is particularly pronounced. There is only a single characteristic that in vivo distinguishes the two genera; the domed oral area in Sorogena, which is lacking in Platyophrya. Otherwise the oral ciliature and minute details seen in freeze-fracture replicas are identical. Moreover, morphogenesis in the stomatic cortex of Sorogena, at least at the light microscopy level, is similar in every detail to the somatic morphogenesis in Platyophrya (Dragesco et al. 1977; Groliere 1975), Cyrtolophosis (Buitkamp 1977) and Microdiaphanosoma (Foissenr 1981, 1985). The general pattern of morphogenesis in Woodruffia, another cyrtolophosidid colpodid, is similar to Sorogena but differs in the detail of the reorganiziation of the paroral of the proter. The significance of this difference is hard to estimate until more detailed electron microscopy data on the stomatogenic events in the proter of other colpodid ciliates become available. In general, it is a shortcoming of many morphogenetic studies that comparatively little attention is paid to the developmental processes in the proter. This is based on the wide-spread but incorrect impression that the proter often takes over the seemingly unchanged oral apparatus of the parental cell. The Colpodea is remarkable among all groups of ciliates for the number of taxa transferred to it from other groups. These taxa include among others the genera Bryometopus, Kreyella, and Bursaria (Foissner 1984, 1985). The typical dikinetid pattern mentioned above with transverse ribbon arising from the posterior kinetosome is regarded as a characteristic feature of the colpodid ciliates. One may doubt that such a complex pattern developed more than once and thus all ciliates with such a pattern are regarded as a monophyletic group. Nevertheless, there are some differences in the somatic cortex of the "classical" colpodids, which encompasses Bresslaua, Colpoda, Tillina, and the "more recent acquisitions" to that group, such as Platyophrya, Woodruffia, and Sorogena. The latter genera have no ciliate plaques and usually one parasomal sac per dikinetid, while the former have ciliary plaques and three parasomal sacs per dikinetid. Because of the difference it the patterning of the particles in the proximal part of the ciliary membrane the senior author (Bardele 1981) still has some doubt that the colpodids form a a monophyletic group. It is recalled that the most of recent revision of the class Colpodea by Foissner (1985) recognized two subclasses, the Bryometopia with the order Bryometopida and the subclass Colpodia with the orders Sorogenida, Bryophryida, Cyrtolophosidida. Grossglocknerida, Colpodida, and Bursariomorphida. The establishement of the order Sorogenida at that time seemed justified by the quite different looking "haptorid" oral ciliature of Sorogena. Foissner's classification of the Colpodea was mainly based on the recongnition of three major silverline patterns: the kreyellid, the platyophryid, and the colpodid silverline pattern. But there exist mixtures of these, for instance the kreyellid and the platyophryid pattern in the Bryometopidae (Foissner 1985), and the silverline pattern may also change during morphogenesis, as in Cyrtolophosis (Foissner 1978). Other criteria were the oral ciliature and the mode of life. Now that it is realized that the oral ciliature of Sorogena is so similar to that of Platyophrya, one may consider an assignmnet of the Sorogenida to the order Cyrtolophosidida. But then what is the systematic value of the conspicuous union of both the micro- and the macronucleus within a common outer nuclear membrane, which is observed in the cyrtolophosidid genera Woodruffia, Kuklikophrya, Platyophrya, Cyrtolophosis, and probably Sagittaria, but not in Sorogena? Sorogena seems not to be closely related to the Colpodidae and the Grossglockneridae (Foissner & Didier 1983), which divide in cysts. For the time being the mosaic combination of so many features found in other colpodid orders as well as the "mycetozoan way of life" seems to justify a separate order Sorogenida. So far the genus Sorogena is monospecific, but since it is likely that further species may be found a more detailed redescription of S. stoianovitchae seemd neccessary. (ref. ID; 4366)
Habitat
On dead attached plant parts; coastal to western North Carolina, USA; Arles, France; Manila, Philippines; Wau Ecology Institute, Papua New Guinea (Type slide: PNG76-73). (ref. ID; 3864)