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FAU Institutional Repository FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1988 Springer. This manuscript is an author version with the final publication available at http://www.springerlink.com and may be cited as: Gustafson, R. G. & Reid, R. G. B. (1988). Association of bacteria with larvae of the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae). Marine Biology, 97(3), 389‐401. doi:10.1007/BF00397769 (JY \,.0 Marine Biology 97,389-401 (1988) Marine ,,,.~"o~,~"'"" on li!einOe<oano B-Iology and Coastal Wote", Cc) Springer-Verlag 1988 ,. Association ofbacteria with larvae ofthe gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae) R. G. Gustafson ':":' and R. G. B. Reid Department of Biology, University of Victoria, Victoria, British Columbia V8W 2Y2, Canada Abstract animals (Cavanaugh et al. 1981, Felbeck et al. 1981, 1983a, Cavanaugh 1983, 1985, Southward 1986). Rod-shaped bacteria were consistently observed by trans­ Chemoautotrophic symbionts have been localized both mission electron microscopy in the locomotory test of lar­ biochemically and ultrastructurally: in trophosome tissue vae and in the perivisceral cavity of post-larvae of Solemya of pogonophorans (Cavanaugh et al. 1981, Felbeck 1981, reidi, a gutless protobranch bivalve known to possess intra­ Southward et al. 1981, 1986, Southward 1982); in the sub­ cellular chemoautotrophic bacterial symbionts in the adult cuticular space of gutless marine oligochaetes of the genus gill. Bacteria develop within granular vesicles in the larval Phallodrilus (Felbeck et al. 1983b); and in the gills of bi­ test, where they either remain to be ingested at metamor­ valves of the family Lucinidae (Fisher and Hand 1984, phosis, or are released into the space separating the test Dando et al. 1985, 1986, Schweimanns and Felbeck 1985, and embryo, to be subsequently ingested through the lar­ Reid and Brand 1986), of the genera Solemya (Cavanaugh val mouth. In either case, bacteria lie within the periviscer­ 1983, Felbeck 1983, Felbeck et al. 1983a), Calyptogena al cavity following metamorphosis. Bacteria were not seen (Felbeck etal. 1981, Fiala-Medioni and Metivier 1986), either in or on gametes or in gills of juveniles. It is Thyasira (Dando and Southward 1986, Reid and Brand hypothesized that these bacteria represent a transmission 1986, Southward 1986), and in the vent mytilid Bathy­ stage of the gill symbionts present in adult S. reidi and are modiolus (Le Pennec and Hily 1984, Fiala-Medioni et al. not evident in gametes or gills of juveniles due to cryptic 1986). The question of whether symbionts are transmitted packaging within granular vesicles. Perpetuation of this through the sexual cycle of the host or are acquired from symbiosis would therefore be assured through vertical other sources has been determined only for the extracellu­ transmission, as is typical ofother marine invertebrate-bac­ lar marine oligochaete symbiosis (Giere and Langheld teria endosymbioses. 1987). Since the gutless protobranch bivalve Solemya reidi (Reid 1980, Reid and Bernard 1980), is used in studies of the association between chemoautotrophic endosymbionts and host animals from sulfide-rich habitats (Felbeck 1983, Felbeck et al. 1983a, Hand and Somero 1983, Powell and Introduction Somero 1985, 1986, Fisher and Childress 1986), it is impor­ tant to know the life-cycle of this symbiosis. In marine habitats where oxygen and reduced-sulfur com­ Sofemya reidi is found from Southern California to pounds are simultaneously available, such as beneath log­ southern Alaska at depths of 40 to 600 m (Bernard 1980) booming grounds, near sewage outfalls, in seagrass beds, near sewage outfalls (Felbeck 1983, Felbeck et al. 1983a) hypoxic marine basins, and around deep-sea hydrothermal and in the Pacific Northwest beneath log-booming grounds vents, certain invertebrate species maintain intracellular (Reid 1980). Transmission of endosymbionts in inverte­ chemoautotrophic bacteria which aid in oxidation of re­ brate-microorganism symbioses proceeds in one of three duced-sulfur compounds and provide energy to the host ways: by vertical transmission (transfer from parent to off­ spring, which may include incorporation in or on the egg * Harbor Branch Oceanographic Institution Contribution of the host); by horizontal transmission (involving the No. 602 spread of symbionts between contemporary hosts); or by ** Present address: Division of Applied Biology, Harbor Branch reinfection of the new host generation from an en­ Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946, USA vironmental stock of microorganisms (Andrewes 1957). 390 R. G. Gustafson and R. G. B.Reid: Bacteria-larvae association The present study provides evidence concerning the mech­ (Costerton 1979), in that they have a central region con­ anism by which chemoautotrophic endosymbionts found taining fibrillar material (chromatin) and a condensed "cy­ in adult gills ofS. reidi are transmitted to host offspring. toplasm". Most inclusions in ripe eggs of S. reidi can be identified as lipid spheres, yolk spheres, mucus containing granules, mitochondria, or multivesicular bodies (Figs. 4, Materials and methods 6). Adult Solemya reidi were collected from an average depth of 40 m with a Van Veen grab in the vicinity of Log-Boom­ Sperm ultrastructure ing Grounds Nos. 27 and 29 in Alberni Inlet on the west coast of Vancouver Island, British Columbia, Canada The spermatozoa of Solemya reidi are of the primitive type (Latitude 49° 12'N; Longitude 124°49'W). Spawning and (Franzen 1983, Anderson and Personne 1976), with four larval culture conditions have been described (Gustafson rounded mitochondria in the midpiece, a tail flagellum, and Reid 1986). Pericalymma larvae (see Gustafson and and an elongated conical nucleus surmounted by a cap­ Reid 1986) and post-larval specimens were cultivated shaped acrosome (Figs. 7, 8). No bacterial cells were seen through metamorphosis at Day 6 until 42 d after fertili­ in the testes. zation. Adult gill. ovary, testis, fertilized eggs, embryonic stages, larvae, and juveniles were prepared for transmis­ Bacteria - larvae association sion electron microscopy (lEM), and scanning electron mi­ croscopy (SEM), by fixation in a solution of 2% glutaralde­ Membrane-bounded, oval or rounded, intracytoplasmic hyde, 0.2 M phosphate buffer, and 0.14 M NaCI at pH 7.3; granular vesicles measuring up to 4,um in longest dimen­ followed by three rinses with a solution of0.2 M phosphate sion are present in the basal regions of the larval test of buffer and 0.28 M NaCI; and post-fixation in 2% OsO. in Solemya reidi, adjacent to the space separating the test and 1.25% NaHC03 . Specimens were dehydrated in alcohol. definitive tissues (Fig. 9). These granular vesicles possess a Further preparation of specimens for microscopy has been homogeneous granular matrix and are common to all test described earlier (Gustafson and Reid 1986). cells. On about the fourth day of development, particles re­ sembling prokaryotic cells were seen within the vesicular matrix (Figs. 10, II). An electron-lucent nuclear region is Results apparent in these particles and each vesicle is surrounded by a single-unit membrane (Fig. 12). By the fifth day of Bacteria in adult Solemya reidi development, definite prokaryotic cells are present within many of the vesicles (Figs. 13-16) while rod-shaped, Bacteriocytes, cells containing bacteria, are located in the Gram-negative, bacteria, measuring up to 1.4,um long by proximal portion of the gill lamellae and alternate regu­ 0.75 ,urn wide, lie free within the space between the test and larly with intercalary cells which lack symbionts (Fig. I). definitive epithelia of the embryo (Figs. 17, 18) in configu­ Rod-shaped unicellular bacteria, ranging in length from rations suggestive of their having been released from the 1.7 to 5,um (as determined from lEM micrographs), line test (Fig. 17). The presence of a distinct non-membrane the distal aspect of each bacteriocyte in close contact with bounded nuclear region, the absence of internal membrane the lateral surface of the gill lamellae and the mantle-cavity bounded organelles, and the presence of a tripartite cell environment. A microvillar layer, derived from adjacent wall typical of Gram-negative bacteria are the criteria used intercalary cells, covers the external surface of the bac­ to classify these particles as bacteria (Costerton 1979). teriocytes. A few mitochondria are present in each bac­ Initially, the vesicular matrix is a homogeneous granu­ teriocyte; however, many more occur in the intercalary lar substance (Figs. 9-11), but as bacteria undergo trans­ cells. The bacteria are intracellular; each bacterium is sur­ formation, numerous membranes and small vesicles de­ rounded by what appears to be a host-derived membrane velop within the matrix (Fig. 14). Large electron-lucent (Figs. 1-3). vacuoles are present in granular vesicles in which bacteria are forming (Figs. 13, 17). During synthesis of the putative bacterial cell walls, a Oocyte inclusions large amount of secondary membrane is formed and sur­ rounds the transforming bacteria (Figs. 14, 15). A non­ Ovarian oocytes, artificially stripped ova and early cleav­ membrane-bounded electron-lucent fibrous region is pres­ age stages were examined with TEM for evidence of sym­ ent in the center of these bacterial particles. bionts. No typical bacterial forms were present (Figs. 4-6). Following metamorphosis, which includes ingestion of However, an extensive survey of inclusions in ovarian eggs portions of the test (Gustafson and Reid 1986, 1988), many of Solemya reidi revealed several structures of doubtful rod-shaped bacteria, measuring up to 1.3,um long and identity. Unidentified inclusions ("u" in Figs. 4 and 5) bear 0.75,um wide were observed in the perivisceral cavity superficial resemblance to prokaryotic cells seen by lEM along with debris from the ingested test cells (Figs. 19-21). v- me .... me .... .~ ~ -.f mc Figs. 1-3. So/emya reidi. I: Adult gill filamen t showing alternate arrangeme nt of bacteri ocytes (be) and intercalary cells (scale bar = 5 ,urn).
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