Abstract
Solemya borealis Totten was collected from anoxic sediments in Buzzards Bay, Massachusetts in April and July 1989 and examined for the presence of symbiotic, chemoautotrophic bacteria. In addition, sediment cores collected at the same site were analyzed throughout the year, to provide a detailed description of the S. borealis habitat. Here we present structural, enzymatic, biochemical, and stable isotope data which suggests that S. borealis, like the related species Solemya velum Say and Solemya reidi Bernard, contains high concentrations of symbiotic chemoautotrophic bacteria in gill bacteriocytes which play a significant role in nutrition. Transmission electron microscopy revealed the presence of rod-shaped cells, which resemble Gram-negative bacteria, within gill epithelial cells. Ribulose-1,5-bisphosphate carboxylase activity in cell-free extracts of S. borealis gill tissue was comparable with that found in other invertebrate-chemoautotroph symbioses. Very negative δ34S ratios (-32.6 to-15.7‰) suggest the utilization of porewater sulfides as both an energy and a sulfur source for the symbionts. Carbon and nitrogen stable isotope ratios were extremely negative (δ13C=-32 to-34.6‰, δ15N=-9.7 to-8.6‰), similar to those of other bivalve-chemoautotroph symbioses. High concentrations of cis-vaccenic acid, a fatty acid previously found in other invertebrate-chemoautotroph symbioses, were found in all the major lipid classes of the gills of S. borealis. The stable isotope ratios and lipid composition of S. borealis suggest that most of this bivalve's nutritional requirements are supplied by bacterial endosymbionts. High levels of taurine in the free amino acid pool of S. borealis suggest the existence of unusual amino acid metabolic pathways which may be the result of endosymbiont activity. The S. borealis specimens were found in relatively shallow water sediments dominated by silts and clays. The sediments contain high concentrations of organic carbon and nitrogen, exhibit limited oxygen penetration, and have high rates of ammonium and sulfide input from the anaerobic microbial community. Sediment C and N stable isotope ratios reflect the input of algal-derived nutrients to the sediments (δ13C=-20.7 to-20.9‰, δ15N=+7.7 to +20.8‰). Sediment δ34S ratios ranged from-18.7 to-25.1‰ demonstrating the presence of sulfur produced by bacterial dissimilatory sulfate reduction processes.
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Literature cited
Anderson, A. E., Childress, J. J., Favuzzi, J. A. (1987). Net uptake of CO2 driven by sulphide and thiosulphate oxidation in the bacterial symbiont-containing clam Solemya reidi. J. exp. Biol. 133:1–31
Beudeker, R. F., Cannon, G. C., Keunen, J. C., Shively, J. M. (1980). Relations between D-ribulose 1,5-bisphosphate carboxylase, carboxysomes and CO2 fixing capacity in the obligate, chemolithoautotroph Thiobacillus neapolitanus grown under different limitations in the chemostat. Archs Microbiol. 124: 185–189
Bishop, S. H., Ellis, L. L., Burcham, J. M: (1983). Amino acid metabolism in molluscs. In: Hochachka, P. W. (ed.). The Mollusca, Vol. 1. Metabolic biochemistry and molecular biomechanics. Academic Press, New York, p. 244–327
Cavanaugh, C. M. (1983). Symbiosis of chemoautotrophic bacteria and marine invertebrates from sulphide-rich habitats. Nature, Lond. 302:58–61
Cavanaugh, C. M. (1985). Symbiosis of chemoautotrophic bacteria and marine invertebrates from deep-sea hydrothermal vents and reducing sediments. In: Jones, M. L. (ed.) Hydrothermal vents of the eastern Pacific: an overview. Bull. biol. Soc. Wash. 6: 373–388
Cavanaugh, C. M., Abbott, M. S., Veenhuis, M. (1988). Immunochemical localization of ribulose-1,5-bisphosphate carboxylase in the symbiont-containing gills of Solemya velum (Bivalvia: Mollusca). Proc. natn. Acad. Sci. U.S.A. 85:7786–7789
Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. W., Waterbury, J. B. (1981). Procaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science, New York 213:340–342
Chen, C., Rabourdin, B., Hammen, C. S. (1987). The effect of hydrogen sulfide on the metabolism of Solemya velum and enzymes of sulfide oxidation in gill tissue. Comp. Biochem. Physiol. 88B:949–952
Cline, J. D. (1969). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14:454–458
Conway, N., McDowell Capuzzo, J. (1990). The use of biochemical indicators in the study of trophic interactions in animal-bacteria symbioses: Solemya velum, a case study. In: Trophic relationships in the marine environment. Proc. 24th Eur. mar. Biol. Symp.: 553–564 [Barnes, M., Gibson, R. N. (eds.) Aberdeen University Press, Aberdeen]
Conway, N., McDowell Capuzzo, J. (1991). Incorporation and utilization of bacterial lipids by the Solemya velum symbiosis. Mar. Biol. 108:277–291
Conway, N., McDowell Capuzzo, J. (1992). Excess taurine in the Solemya velum symbiosis, possible sources and functions. Comp. Biochem. Physiol. B (in press)
Conway, N., McDowell Capuzzo, J., Fry, B. (1989). The role of endosymbiotic bacteria in the nutrition of Solemya velum: evidence from a stable isotope analysis of endosymbionts and host. Limnol. Oceanogr. 34:149–155
Dall, W. H. (1908). A revision of the Solenomyacidae. Nautilus 22(1):1–2
Dando, P. R., Southward, A. J. (1986). Chemoautotrophy in bivalve molluscs of the genus Thyasira. J. mar. biol. Ass. U.K. 66: 915–929
Dando, P. R., Southward, A. J., Southward, E. C., Terwilliger, N. B. Terwilliger, R. C. (1985). Sulphur-oxidizing bacteria and haemoglobin in gills of the bivalve mollusc Myrtea spinifera. Mar. Ecol. Prog. Ser. 23:85–98
Degens, E. T. (1969). Biogeochemistry of stable carbon isotopes. In: Eglinton, E., Murphy, M. J. T. (eds.) Organic geochemistry. Springer-Verlag, Berlin, p. 304–329
Distel, D. L., Lane, D. J., Olsen, G. J., Ciovannoni, S. J., Pace, B., Pace, N. R., Stahl, D. A., Felbeck, H. (1988). Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J. Bact. 170:2506–2510
Felbeck, H. (1983). Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: an animal-bacterial symbiosis. J. Comp. Physiol. (Sect. B) 152:3–11
Fiala-Médioni, A., Alayse, A. M., Cahet, G. (1986). Evidence of in situ uptake and incorporation of bicarbonate and amino acids by a hydrothermal vent mussel. J. exp. mar. Biol. Ecol. 96: 191–198
Fisher, C. R. (1990). Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev. aquat. Sciences 2:399–443
Fisher, C. R. Childress, J. J. (1986). Translocation of fixed carbon from symbiotic bacteria to host tissues in the gutless bivalve Solemya reidi. Mar. Biol. 93:59–68
Fry, B., Cox, J., Gest, H., Hayes, J. M. (1986). Discrimination between 34S and 32S during bacterial metabolism of inorganic sulfur compounds. J. Bact. 165:328–330
Fry, B., Sherr, E. B. (1984). δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib. mar. Sci. Univ. Tex. 27:13–47
Fulco, A. J. (1983). Fatty acid metabolism in bacteria. Prog. Lipid Res. 22:133–160
Gearing, J. N., Gearing, P. J., Rudnick, D. T., Requejo, A. G., Hutchins, M. J. (1984). Isotope variability of organic carbon in a phytoplankton-based temperature estuary. Geochim. cosmochim. Acta 48:1089–1098
Giere, O., Conway, N., Gastrock, G., Schmidt, C. (1991) Regulation of the gutless annelid ecology by endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 68:287–299
Giero, O., Felbeck, H., Dawson, R., Liebezeit, G. (1984). The gutless marine oligochaete Phallodrilus leukodermatus Giere, a tubificid of structural, ecological and physiological significance. Hydrobiologica 115:83–89
Goad, L. J. (1976). The steroids of marine algae and invertebrate animals. In: Malins, D. C., Sargent, J. R. (eds.) Biochemical and biophysical perspectives in marine biology, Vol. 3. Academic Press, New York, p. 213–318
Goldfine, H. (1972). Comparative aspects of bacterial lipids. Adv. microb. Physiol. 8:1–58
Goldhaber, M. B., Kaplan, I. R. (1975). Controls and consequences of sulfate reduction rates in recent marine sediments. Soil Sci. 119:42–55
Gustafson, R. G., Reid, R. G. B. (1988). Association of bacteria with larvae of the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae). Mar. Biol. 97:389–401
Hartmann, U. M., Nielson, H. (1969). δ34S Werte in rezenten Meeressedimenten und ihre Deutung am Beispiel einiger Sedimentprofile aus der westlichen Ostsee. Geol. Rdsch. 58:621–655
Howes, B. L., Dacey, J. W. H., King, G. M. (1984). Carbon flow through oxygen and sulfate reduction pathways in salt marsh sediments. Limnol. Oceanog. 29:1037–1051
Joseph, J. D. (1982). Lipid composition of marine and estuarine invertebrates. Part II: Mollusca, Prog. Lipid. Res. 21:109–153
Jørgensen, B. B. (1977). The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnol. Oceanogr. 22:814–832
Kelley, D. P., Kuenen, J. G. (1984). Ecology of the colourless sulphur bacteria. In: Codd, G. A. (ed.) Aspects of the microbial nutrition and ecology. Academic Press, New York, p. 211–240
Kuznetsov, A. P., Ohta, S., Endow, K. (1990). Morphofunctional consequences of bacterial symbiotrophy in solemya (Petrasma) pusilla (Protobranchia, Bivalvia) from the Sagami Bay (Central Japan). Izv. Akad. Nauk SSSR 6:895–903
Lehninger, A. L. (1975). Biochemistry, 2nd edn. Worth Publishers Inc., New York
McCaffrey, M. A., Farrington, J. W., Repeta, D. J. (1989). Geochemical implications of the lipid composition of Thioploca sp. from the Peru upwelling region-15°S. Org. Geochem. 14:61–68
Miziorko, H. M., Lorimer, G. H. (1983). Ribulose-1,5-bisphosphate carboxylase-oxygenase. A. Rev. Biochem. 52:507–535
Moreno, J., Pollero, A. E., Moreno, V. J., Brenner, R. R. (1980). Lipids and fatty acids of the mussel (Mytilus platensis d'Orbigny) from South Atlantic Waters. J. exp. mar. Biol. Ecol. 48: 263–276
Morse, E. S. (1913). Observation of living Solenomya velum and borealis. Biol. Bull. mar. biol. Lab., Woods Hole 25:261–281
Morse, E. S. (1919). Observations on living lamellibranchs of New England. Proc. Boston. Soc. nat. Hist. 35(5):139–196
Piretti, M. V., Tioli, F., Pagliuca, G. (1987). Investigation of the seasonal variations of sterol and fatty acid constituents in the bivalve molluscs Venus gallina and Scapharca inaequivalvis (Bruguiére). Comp. Biochem. Physiol. 88B:1201–1208
Pollero, R. J., Re, M. E., Brenner, R. R. (1979). Seasonal changes of the lipids of the mollusc Chlamys technelcha. Comp. Biochem. Physiol. 64A:257–263
Reid, R. G. B. (1980). Aspects of the biology of a gutless species of Solemya (Bivalvia: Protobranchia). Can. J. Zool. 58:386–393
Reid, R. G. B., Brand, D. G. (1987). Observations on Australian Solemyidae. J. malac. Soc. Aust. 8:41–50
Rounick, J. S., Winterbourn, M. J. (1986). Stable carbon isotopes and carbon flow in ecosystems. BioSci. 236:171–177
Ruby, E. G., Jannasch, H. W., Deuser, W. G. (1987). Fractionation of stable carbon isotopes during chemoautotrophic growth of sulfur-oxidizing bacteria. Appl. envirl Microbiol. 53:1940–1943
Sanders, H. L. (1958). Benthic studies in Buzzards Bay. I. Animal-sediment relationships. Limnol. Oceanogr. 3:245–258
Sanders, H. L. (1960). Benthic studies in Buzzards Bay. III. The structure of the soft-bottom community. Limnol. Oceanogr. 5: 138–153
Scheiner, D. (1976). Determination of ammonia and Kjeldahl nitrogen by indophenol method. Wat. Res. 10:31–36
Southward, A. J., Southward, E. C., Dando, P. R., Barrett, R. L., Ling, R. (1986). Chemoautotrophic function of bacterial symbionts in small pogonophora. J. mar. biol. Ass. U.K. 66:415–437
Southward, E. C. (1986). Gill symbionts in thyasirids and other bivalve molluscs. J. mar. biol. Ass. U.K. 66:889–914
Soyer, J., Soyer-Gobillard, M.-O., Thiriot-Quiévreux, C., Bouvy, M., Cahet, G. (1987). Chemoautotrophic bacterial endosymbionts in Spisula subtruncata (Bivalvia, Mactridae). Ultrastructure, metabolic significance and evolutionary implications. Symbioses 3:301–314
Spiro, B., Greenwood, P. B., Southward, A. J., Dando, P. R. (1986). 13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutritional importance of chemoautotrophic endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 28:233–240
Stahl, D. A., Lane, D. J., Olsen, G. J., Pace, N. R. (1984). Analysis of hydrothermal vent associated symbionts by ribosomal RNA sequences. Science, New York 224:409–411
Tabatabai, M. A. (1974). Determination of SO4 in water samples. Sulphur Inst. J. 10:11–14
Verma, D. P. S., Long, S. (1983). The molecular biology of Rhizobium-legume symbiosis. Int. Rev. Cytol. (Suppl.) 14:211–245
Williams, C. A., Nelson, D. C., Farah, B. A., Jannasch, H. W., Shively, J. M: (1988). Ribulose bisphosphate carboxylase activity of the procaryotic symbiont of a hydrothermal vent tube worm: kinetics, activity and gene hybridization. Fedn eur. microbiol. Soc. (FEMS) Lett. 50:107–112
Yonge, C. M. (1939). The protobranchiate mollusca: a functional interpretation of their structure and evolution. Phil. Trans. R. Soc. (Ser. B): 230–279
Zhabina, N. N., Volkov, I. I. (1976). A method of determination of various sulfur compounds in sea sediments and rocks. In: Krumbein, W. E. (ed.) Environmental biogeochemistry and geomicrobiology, Vol. 3. Methods, metals and assessment. Ann Arbor Science Publ. Ann Arbor
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Communicated by J. Grassle, New Brunswick
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Conway, N.M., Howes, B.L., McDowell Capuzzo, J.E. et al. Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve-bacteria symbiosis. Marine Biology 112, 601–613 (1992). https://doi.org/10.1007/BF00346178
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DOI: https://doi.org/10.1007/BF00346178