Structure of Protistan Parasites Found in Bivalve Molluscs

W&M ScholarWorks VIMS Books and Book Chapters Virginia Institute of Marine Science 1988 Structure of Protistan Parasites Found in Bivalve Molluscs Frank O. Perkins Follow this and additional works at: https://scholarworks.wm.edu/vimsbooks Part of the Marine Biology Commons, and the Parasitology Commons American Fisheries Society Special Publication 18:93- 111 , 1988 CC> Copyrighl by !he American Fisheries Sociely 1988 PARASITE MORPHOLOGY, STRATEGY, AND EVOLUTION Structure of Protistan Parasites Found in Bivalve Molluscs 1 FRANK 0. PERKINS Virginia In stitute of Marine Science. School of Marine Science, College of William and Mary Gloucester Point, Virginia 23062, USA Abstral'I.-The literature on the structure of protists parasitizing bivalve molluscs is reviewed, and previously unpubli shed observations of species of class Perkinsea, phylum Haplosporidia, and class Paramyxea are presented. Descriptions are given of the flagellar apparatus of Perkin.His marinus zoospores, the ultrastructure of Perkinsus sp. from the Baltic macoma Maconw balthica, and the development of haplosporosome-like bodies in Haplosporidium nelsoni. The possible origin of stem cells of Marreilia sydneyi from the inner two sporoplasms is discussed. New research efforts are suggested which could help elucidate the phylogenetic interrelationships and taxonomic positions of the various taxa and help in efforts to better understand life cycles of selected species. Studies of the structure of protistan parasites terization of the parasite species, to elucidation of found in bivalve moll uscs have been fruitful to the many parasite life cycles, and to knowledge of morphologist interested in comparative morphol- parasite metabolism. The latter, especially, is ogy, evolu tion, and taxonomy. A diversity of important for determining the effects of prophy- species and higher taxa contain a great range of laxis and therapy. structures and developmental stages of consider- In most cases, the parasitic state, its pathogenic- able complexity. The most intensive studies have ity, or both cannot be directly transmitted experi- centered on pathogens of commercially important mentally. In cases of successful direct transmission, hosts, and the results have contributed to the for example, of Perkinsus marinus or (perhaps) management of these valuable hosts, primarily Bonamia ostreae, host specificity of the parasite is oysters, by identifying the agent causing mortal- often not known because morphologically distin- ity. Thus, the investigator can identify the caus- guishing structures are lacking and transmission ative agent and conduct epizootiological studies experiments with a single population of parasites in to determine (I) geographical range, (2) frequency several host species have not been attempted. Be- and periodicity of disease expression, and (3) cause infections of bivalves with most parasites controlling physical factors such as salinity and cannot be transmitted, investigations should be con- temperature. Then managers and users of the ducted on host defense mechanisms, identification hosts can be advised how to avoid the disease and of intermediate hosts, and whether the organisms how to minimize the impact of the disease. Unless are truly parasitic or merely opportunistic. protistan pathogens can be di stinguished from one The availability of transmission electron micro- another, the ecological relationships of parasite to scopes beginning in the early 1960s was a major host may be misi nterpreted. advance for protistologists. Most cell stages are Morphologists have not always been successful 2-10 µ.m in size, and distinguishing structures in their attempts at species characterization, be- were often impossible to find by light microscopy. cause the protists within genera have relatively Electron microscopes have provided the ability to few di stinguishing structures. The problem is distinguish major taxa, for example, coccoid uni- compounded by the inability to establish pure cells of the thraustochytriacean protists from the cultures of all but a very few parasitic protista or species of class Perkinsea. of host cell s that could serve as the culture In this presentation, I shall provide an overview medium. The lack of cultures is the greatest of the major groups of protistan parasites with barrier to more complete morphological charac- emphasis on their structure, phylogeny, and geographical distribution. Literature citations wi ll 'Contribution 14 14 VIMS/SMS of the College of direct readers to published descriptions and mi- Wil liam and Mary. crographs of morphological structures. 93 94 PERKINS Class Perkinsea anterior end and tapers to a pointed posterior end (Plate I, Figure I) . The anterior flagellum emerges Perkinsus marinus from a groove located about one-third of the way Levine ( 1978) establi shed the class Perkinsea for from the anterior end toward the posterior end. The the phylum Apicomplexa to accommodate the ob- posterior flagellum emerges from a cul-de-sac in the servations of Perkins (1976c), who found that the cell surt'ace at right angles to the anterior flagellum. fl agell ated cells of Dermocystidium marinum, the The kinetosome and base of the flagellum are name then given to a pathogen of the eastern oyster complex. There are no cartwheels in the kineto- Crassostrea virginica, have organelles very similar some lumen; however, a large electron-dense to those of other species in the Apicomplexa. The inclusion body is found in the lumen with cross phylum essentially includes protistan species for- bridging to the A and B microtubules of the triplet merly classified in the Sporozoa. Perkins (1974) blades (Plate I, Figure 2 [d]) . Each triplet blade is noted that flagellated cells are not formed in Der- linked to the adjacent blade by a si ngle bridge. mocystidium sp. from salmon, nor have other The proximal end of the kinetosome is blocked by cyst-forming species of Dermocystidium in fish an electron-dense plate; however, there is no and amphibia been observed to form flagellated basal plate in the interfacial zone between the cell s. Therefore, Levine (1978) created a new ge- kinetosome and flagellum (Plate I, Figure 2). An nus for the pathogen of the eastern oyster and electron-dense, hollow cylinder is present at the renamed the species Perkinsus marinus. base of the flagellum; it is closed at the distal end but This systematic revision has stimulated debate on the validity of the Apicomple xa and Perkinsea may be partially open or closed at the proximal end. by several workers, notably Vivier ( 1982) and A secondary, thin-walled cylinder is found outside myself as related by Canning (1986). Until more is the primary one (Plate I, Figures 2, 2 [b]). known about Perkinsea and other Protista with The central doublet of flagellar microtubules ter- apicomplexan characteristics, the validity of the minates on a plate which is free in the flagell ar class will remain unsettled. However, it appears lumen and located close to the cylinders mentioned that the eastern oyster pathogen is not properly above. At right angl es to the plate and extending placed in the genus Dermocystidium. distally is a structure that is either a stack of rings or The structures found in the flagellated cells a helically wound filament (Plate I, Figures 2, 2 [aj). (zoospores) of Perkins 11 .1· spp., which are similar Two or more structures, perhaps microtubules, to those found in the Apicomplexa, particularly coated with electron-dense material, extend at the Coccidi a , are the apical complex, micropores, right angles to the long axis of the cell body (Plate rhoptries, micronemes, and subpellicular complex I, Figure 2). They originate from a wedge-shaped, described in detail in Perkinsus marinus by Per- electron-dense structure located at the base of the kins (1976c). They have also been observed in two kinetosomes and between them. If this fila- Perkin.I'll.I' sp. found in Macoma balthica (my mentous extension were shown to be homologous unpublished data) and in Tridacna sp. (R. J. G. to the presumptive vestigal flagella of the micro- Lester, University of Queensland , unpublished gametes of Toxop/asma gondii and Eimeria magna data). Unlike those of other known Protista, the (Pelster and Piekarski 1971; Speer and Danforth anterior flagellum of Perkin.rns spp. has a row of 1976) , the evidence for including P . marinus in the long, filamentous mastigonemes and a row of Apicomplexa would be strengthened and questions short, spurlike structures along the full length of would be raised as to whether or not the zoospores the flagellum. The repeating units are one spur of P. marinus are isogametes. and five clustered mastigonemes grouped together The complement of the kinetosomal-flagellar (Perkins 1987) . The posterior flagellum lacks structures in Perkinsus spp. has also been ob- mastigonemes. served in the Perkinsus sp. found in Macoma The cell body (2-3 x 4- 6 µm) is rounded at the balthica (Perkins 1968; unpublished data). Fur- PLATE 1.- Flage ll ar apparatus of Perkin.1·11 .1· marinus zoospores. FIGURE 1.-Phase-contrast micrograph of .... Perkin.1·11 .1· 111ari1111.1· zoospore. A = anterior flagellum; P = posterior flagellum. Bar = 3 µm. FIGURE 2.- Kinetosome and base of anterior flagellum of P. marinus. Bar = 0.5 µm. Lines a-d indicate the sites of cross sections of flagella illustrated in in serts a-d; in sert bar = 0.1 µm. E = electron-dense core in lumen of kinetosome; C = hollow cylinder in flagellar base; P = plate at base of central pair of flagell ar axonemes; Fi = heli cal filament(?); F = bundle of filaments or microtubules. STRUCTURE OF PROTISTAN PARASITES OF BIVALVES 95 ® 96 PE RKINS thermore, the electron-dense cylinder in the prox- rations of eastern oyster tissue observed in bright imal end of the kinetosome lumen has been ob- fie ld microscopy because it has characteristic served in the thraustochytriaceous-labyrinthulid Brownian movement and is refringent. It has protists (Perkins 1974). The phylogenetic affinity cytochemical characteristics similar to volutin as between Perkin.rns spp. and the latter group and found in yeast cells.

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