DESCRIPTION OF THE PHYLUM OPALINATA (WENYON 1926)

EUKARYA> CHROMALVEOLATA> HETEROKONTAE> OPALINIDA

Opalinida (o-pa-LI-ni-da) means little opal and is derived from the Greek (opallios -οπάλλιος) or the Latin (opalus). The reference is to the tiny opaline trophozoites.

INTRODUCTION TO THE OPALINIDA The opalinids are gut commensals of amphibians, particularly anurans, and of some fish. They are covered by small short flagella (cilia) with parallel basal bodies (Figure 1). Thus, they superficially resemble ciliates. However, they do not have alveoli nor do they have dimorphic nuclei (Figure 2). Opalina is a commensal that has a life cycle that alternates between the mature frog and at least two different tadpoles (Opalina Life Cycle). Cysts are expelled by the adult frog and taken up by a feeding tadpole. After the cyst germinates in the gut, the cells (gamonts or gamete-producing cells) move to the cloaca where they undergo meiosis. In this case, the products of meiosis become gametes that look like the ciliated opalinid, but they are uninucleate and vary in size (microgamete and macrogamete), a condition called anisogamy. The fusion of gametes forms a zygote that encysts and leaves the host via the feces. The zygocyst is then taken up by a second tadpole where the cell excysts forming an agamont (a cell that does not undergo meiosis or gamete formation), which stays in the lower bowel and cloaca as a feeding stage, a trophozoite. The agamonts can form their own cysts which can, in turn, can be taken up by other tadpoles. As the tadpoles mature and metamorphose into frogs, the agamont trophozoites in them become larger and many times multinucleate (more than 2,000 nuclei). The large forms of the agamonts persist in the adult frogs until hormonal changes in the breeding season signals a change in the opalinids, which begin to divide without growth and mitosis, making the daughter cells successively smaller and with fewer nuclei with each cytokinesis. Finally, during the breeding season, the small cells with 2-12 nuclei encyst, are expelled, and the cycle continues. The proteromonads have a heterokont condition with a recurrent whiplash flagellum and an anterior flagellum that seems to have a paraflagellar rod in Proteromonas (Brugerolle and Mignot 1990, see Figure 3). The proteromonads have a pleated pellicle like that of Opalina. They are parasites/commensals in the lower bowls of vertebrates that include amphibians, reptiles, and mammals. They are especially common in rodents (Brugerolle and Mignot 1990). A sister genus, Karotomorpha, has two pairs of flagella. Blastocystis is very unlike the other taxa of this phylum and united only by molecular phylogenies (e.g. Perez-Brocal et al. 2010). The organism is a commensal in humans but can become parasitic in those with compromised immune systems. Originally, it was described as a kind of fungal yeast, but reclassified as a stramenopile only in 1996 (Silberman et al. 1996). The cell is amoeboid and not flagellated. It has an organelle that seems to be transitional between a mitochondrion and a hydrogenosome (Stechman et al. 2008). Margulis and Schwartz (1988) and Corliss (1990) consider this group to be part of a large, heterogeneous collection of flagellated organisms called the “Zoomastigina” (Pr-8). Since then, Margulis and Schwartz (1998) removed the amitochondriate taxa and renamed the new phylum Zoomastigota (Pr-30). We have raised the opalinids to the phylum level and are in agreement with Sleigh et al (1984). Older sources such as Kudo (1966) consider the opalinids to be primitive ciliates. However, Margulis and Schwartz (1988 and 1998), Grell (1973), and Lynn and Small (1990) consider that the opalinids only superficially resemble the ciliates. Patterson (1989) suggests that the opalinids have “suffered from taxonomic isolation” long enough and proposes an association with the Proteromonads (a group he considered allied to the Retortomonads). However, more recently, Patterson (1999) places the retortomonads, and therefore the opalinids, in the Stramenopliles (Heterokonts). Sogin and Patterson (Tree of Life Project) have placed them near the root of the heterokont tree (see Figure 5). Similarly, Baldauf (2003) in her synthesis have the opalinids clearly in the heterokont line, though at the base and near the divergence of the alveolates. In recognition of the association of the opalinids with the proteromonads, Patterson (1985) referred to this group as the Slopalinids (a contraction of Opalinida sensu latu). Slopalinida has become a technical term in the literature, but we prefer to use the more formal term Opalinata in a broader sense.

FIGURE 1. Trophozoite of Opalina viewed with a DIC microscope. Note the cell covered with ciliary flagella. Image from http://www.k-state.edu/parasitology/625tutorials/FIGopalina.jpg	FIGURE 2. A photomicrograph of Opalina trophozoites from the gut of a frog. Note the multiple small nuclei in the larger cell. Image from http://www.tarleton.edu/~biology/InvLab1.html	FIGURE 3. A photomicrograph of Proteromonas lacertae trophozoite. Note the single nucleus and biflagellate condition. The anteriorly-directed flagellum is darker. Image from Perez-Brocal et al. (2010) Figure 1.	FIGURE 4. Cysts of Blastocystis hominis stained with Lugol’s Iodine in a fecal sample. Image from CDC.

FIGURE 5. A cladogram highlighting the relationships between the classes of the opalinids (in the shaded box) and their relationships with the heterotrophic heterokont taxa (in bold). The topology of the cladogram was informed by Perez-Brocal et al. (2010).

LITERATURE CITED Baldauf, S. L. 2003a. The deep roots of eukaryotes. Science. 300 (5626): 1701-1703. Brugerolle G and J. P. Mignot. 1990. Phylum Zoomastigina, class Proteromonadida. In: Margulis, L., J. O. Corliss, M. Melkonian, D. J. Chapman,eds. Handbook of Protoctista. Jones & Bartlett. Boston. pp. 246–251. Corliss, J.O. 1990. Opalinta. In: Margulis, L., J.O. Corliss, M. Melkonian, and D.J. Chapman, eds. 1990. Handbook of the Protoctista; the Structure, Cultivation, Habits and Life Histories of the Eukaryotic Microorganisms and Their Descendants Exclusive of Animals, Plants and Fungi. Jones and Bartlett Publishers. Boston. pp. 239-245. Grell, K. G. 1973. Protozoology. Springer-Verlag. New York. Kudo, R.R. 1966. Protozoology. 5th ed. Charles C. Thomas Publisher. Springfield. Lynn, D. H. and E. B. Small. 1990. Ciliophora. In: Margulis, L., J. O. Corliss, M. Melkonian, and D. J. Chapman, eds. 1990. Handbook of the Protoctista; the structure, cultivation, habits and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett Publishers. Boston. pp. 498-523. Margulis, L. and K. Schwartz. 1988. Five kingdoms, an illustrated guide to the phyla of life on earth. 2nd Edition. W.H. Freeman and Co. New York. Margulis, L. and K. Schwartz. 1998. Five kingdoms, an illustrated guide to the phyla of life on earth. 3rd Edition. W. H. Freeman and Company. New York. Patterson, D. J. 1989. Stramenopiles: chromophytes from a protistan perspective. In: Green, J. C., B. S. C. Leadbeater, and W. L. Diver, eds. The chromophyte algae, problems and perspectives. Systematics Association Special Volume No. 38. Clarendon Press. Oxford. pp. 357-379. Patterson, D. J. 1999. The diversity of eukaryotes. American Naturalist. 154 (Suppl.): S96–S124. Perez-Brocal, V., R. Shahar-Golan, and C. G. Clark. 2010. A linear molecule with two large inverted repeats: the mitochondrial genome of the stramenopile Proteromonas lacertae. Genome Biol. Evol. 2: 257-266. Silberman, J. D., M. L. Sogin, D. D. Leipe, and C. G. Clark. 1996. Human parasite finds taxonomic home. Nature 380: 398. [L] Sleigh, M.A., J.D. Dodge and D.J. Patterson. 1984. Kingdom Protista. In: Barnes, R.K.S., ed. A Synoptic Classification of Living Organisms. Sinauer Associates, Inc. Sunderland, Mass. Sogin, M. L. and D. J. Patterson. 1995. Stramenopiles. Version 01 January 1995 (under construction). http://tolweb.org/Stramenopiles/2380/1995.01.01 In: The Tree of Life Web Project, http://tolweb.org/ Stechman, A., K. Hamblin, V. Perez-Brocal, D. Gaston, G. S. Richmond, M. van der Giezen, C. G. Clark, and A. J. Roger. 2008. Organelles in Blastocystis that blur the distinction between mitochondria and hydrogenosomes. Current Biology. 18: 580-585. [C] Wenyon, C. M. 1926. Protozoology. Wm. Wood and Co. New York. pp.1563.

By Jack R. Holt. Last revised: 02/19/2013