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Chemoautotrophic function of bacterial symbionts in small Pogonophora

Published online by Cambridge University Press:  11 May 2009

A. J. Southward
Affiliation:
The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PL1 2PB
Eve C. Southward
Affiliation:
The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PL1 2PB
P. R. Dando
Affiliation:
The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PL1 2PB
R. L. Barrett
Affiliation:
The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PL1 2PB
R. Ling
Affiliation:
The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PL1 2PB

Introduction

The small species of Pogonophora that are widely distributed in sediments along the Continental Slope and in the Norwegian fjords (Webb, 1965; Southward & Southward, 1967; Southward, 1971,1979) carry Gram-negative bacteria in the posterior part of the body (Southward, 1982). In this they resemble the giant pogonophores (Vestimentifera) that live around hydrothermal vents in the Pacific ocean floor (Cavanaugh et al. 1981; Cavanaugh, 1983). The bacteria in both groups are autotrophic (Felbeck, 1981; Southward et al. 1981), capable of synthesizing organic matter from carbon dioxide. The bacteria in Riftia and other vent pogonophores appear to obtain energy by oxidation of reduced sulphur compounds (Felbeck, 1981; Felbeck, Childress & Somero, 1981). Hydrothermal vent waters may contain as much as 6 nut dissolved sulphide (Edmond et al. 1982; Edmond & Von Damm, 1983), which is diluted to about 200-300 μM near the giant pogonophores, whose blood can transport sulphide without affecting the affinity of its haemoglobin for oxygen (Arp & Childress, 1983; Powell & Somero, 1983; Childress, Arp & Fisher, 1984).

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1986

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References

REFERENCES

Akazawa, T., Takabe, T. & Kobayashi, H., 1984. Molecular evolution of ribulose-1,5-bisphosphate carboxylase/oxygenase. Trends in Biochemical Sciences, 9, 380383.CrossRefGoogle Scholar
Arp, A. J. & Childress, J. J., 1983. Sulfide binding by the blood of the hydrothermal vent tubeworm Riftia pachyptila. Science, New York, 219, 295297.CrossRefGoogle Scholar
Berg, C. J. & Alatolo, P., 1984. Potential of chemosynthesis in molluscan mariculture. Aquaculture, 39, 165179.CrossRefGoogle Scholar
Brattegard, T., 1967. Pogonophora and associated fauna in the deep basin of Sognefjorden. Sarsia, 29, 299306.CrossRefGoogle Scholar
Cavanaugh, C. M., 1983. Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature, London, 302,5861.CrossRefGoogle Scholar
Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. W. & Waterbury, J. B., 1981. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science, New York, 213, 340342.CrossRefGoogle ScholarPubMed
Childress, J. J., Arp, A. J. & Fisher, C. R., 1984. Metabolic and blood characteristics of the hydrothermal vent tube-worm Riftia pachyptila. Marine Biology, 83, 109124.CrossRefGoogle Scholar
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. Marine Ecology-Progress Series, 23, 8598.CrossRefGoogle Scholar
Dando, P. R., Southward, A. J. & Southward, E. C., 1986 a. Chemoautotrophic symbionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its habitat. Proceedings of the Royal Society (B), in press.Google Scholar
Dando, P. R., Southward, A. J., Southward, E. C. & Barrett, R. L., 1986 b. Possible energy sources for chemoautotrophic prokaryotes symbiotic with invertebrates from a Norwegian fjord. Ophelia, in press.CrossRefGoogle Scholar
Dybern, B. I., 1967. Topography of Kviturdvikpollen and Vägsbopollen on the west coast of Norway. Sarsia, 30, 127.CrossRefGoogle Scholar
Edmond, J. M., Von Damm, K. L., Mcduff, R. E. & Measures, C. I., 1982. Chemistry of hot springs on the East Pacific Rise and their effluent dispersal. Nature, London, 297, 187191.CrossRefGoogle Scholar
Edmond, J. M. & Von Damm, K., 1983. Hot springs on the ocean floor. Scientific American, 248, 7085.CrossRefGoogle Scholar
Felbeck, H., 1981. Chemoautotrophic potential of the hydrothermal vent tube worm Riftia pachyptila Jones (Vestimentifera). Science, New York, 213, 336338.CrossRefGoogle ScholarPubMed
Felbeck, H., 1983. Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: an animal-bacteria symbiosis. Journal of Comparative Physiology, 152, 311.CrossRefGoogle Scholar
Felbeck, H., Childress, J. J. & Somero, G. N., 1981. Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature, London, 293, 291293.CrossRefGoogle Scholar
Fisher, C. R. & Hand, S. C., 1984. Chemoautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 167, 445459.CrossRefGoogle ScholarPubMed
Flügel, H. J. & Langhof, I., 1983. A new hermaphroditic pogonophore from the Skagerrak. Sarsia, 68, 131138.CrossRefGoogle Scholar
Hand, S. C. & Somero, G. N., 1983. Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 165, 167181.CrossRefGoogle Scholar
Howarth, R. W. & Jorgensen, B. B. 1984. Formation of35S-labelled elemental sulfur and pyrite in coastal marine sediments (Limfjorden and Kysing Fjord, Denmark) during short-term 35SO4−2 reduction measurements. Geochimica et cosmochimica acta, 48, 18071818.CrossRefGoogle Scholar
Jørgensen, B. B., 1977. The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnology and Oceanography, 22, 814832.CrossRefGoogle Scholar
Jørgensen, B. B., 1980. Mineralization and the bacterial cycling of carbon, nitrogen and sulphur in marine sediments. In Contemporary Microbial Ecology (ed. Ellwood, D. C.et al..) pp. 239251. London: Academic Press.Google Scholar
Jorgensen, B. B., 1982. Mineralization of organic matter in the sea bed - the role of sulphate reduction. Nature, London, 296, 643645.CrossRefGoogle Scholar
Kelly, D. P., 1982. Biochemistry of the chemolithotrophic oxidation of inorganic sulphur. Philosophical Transactions of the Royal Society (B), 298, 499529.Google ScholarPubMed
Kelly, D. P. & Kuenen, J. G., 1984. Ecology of the colourless sulphur bacteria. In Aspects of Microbial Nutrition and Ecology (ed. Codd, G. A.), pp. 211240. New York: Academic Press.Google Scholar
Lie, U., Magnesen, T., Thunberg, B. & Aksnes, D. L., 1983. Preliminary studies on the vertical distribution of size-fractions in the zooplankton community of Lindaspollene, western Norway. Sarsia, 68, 6580.CrossRefGoogle Scholar
Little, C. & Gupta, B. L., 1969. Studies on Pogonophora. II. Uptake of nutrients. Journal of Experimental Biology, 51, 759773.CrossRefGoogle Scholar
Lorimer, G. H., Badger, M. R. & Andrews, T. J., 1977. D-ribulose-l,5-bisphosphatecarboxylaseoxygenase. Analytical Biochemistry, 70, 6675.CrossRefGoogle Scholar
Matthews, J. L. B. & Sands, N. J., 1973. Ecological studies on the deep water pelagic community of Korsfjorden, western Norway. The topography of the area and its hydrography in 1968–1972, with a summary of the sampling programme. Sarsia, 52, 2952.CrossRefGoogle Scholar
Powell, M. A. & Somero, G. N., 1983. Blood components prevent sulfide poisoning of respiration of the hydrothermal vent tube worm Riftia pachyptila. Science, New York, 219, 297299.CrossRefGoogle ScholarPubMed
Ribbons, D. W., Harrison, J. E. & Wadzinski, A. M., 1970. Metabolism of single carbon compounds. Annual Review of Microbiology, 24, 135158.CrossRefGoogle ScholarPubMed
Southward, A. J. & Southward, E. C., 1963. Notes on the biology of some Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 43, 5764.CrossRefGoogle Scholar
Southward, A. J. & Southward, E. C., 1980. The significance of dissolved organic compounds in the nutrition of Siboglinum ekmani and other small species of Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 60, 10051034.CrossRefGoogle Scholar
Southward, A. J. & Southward, E. C., 1981. Dissolved organic matter and the nutrition of the Pogonophora: a reassessment based on recent studies of their morphology and biology. Kieler Meeresforschungenen, sonderheft, 5, 445453.Google Scholar
Southward, A. J., Southward, E. C., Brattegard, T. & Bakke, T., 1979. Further experiments on the value of dissolved organic matter as food for Siboglinum fiordicum (Pogonophora). Journal of the Marine Biological Association of the United Kingdom, 59, 133148.CrossRefGoogle Scholar
Southward, A. J., Southward, E. C., Dando, P. R., Rau, G. H., Felbeck, H. & Flugel, H., 1981. Bacterial symbionts and low13C/12C ratios in tissues of Pogonophora indicate unusual nutrition and metabolism. Nature, London, 293, 616620.CrossRefGoogle Scholar
Southward, E. C., 1971. Recent researches on the Pogonophora. Oceanography and Marine Biology, an Annual Review, 9, 193220.Google Scholar
Southward, E. C., 1972. On some Pogonophora from the Caribbean and the Gulf of Mexico. Bulletin of Marine Science, 22, 739776.Google Scholar
Southward, E. C., 1979. Horizontal and vertical distribution of Pogonophora in the Atlantic Ocean. Sarsia, 64, 5155.CrossRefGoogle Scholar
Southward, E. C., 1982. Bacterial symbionts in Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 62, 889906.CrossRefGoogle Scholar
Southward, E. C. & Southward, A. J., 1966. A preliminary account of the general and enzyme histochemistry of Siboglinum atlanticum and other Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 46, 579616.Google Scholar
Southward, E. C. & Southward, A. J., 1967. The distribution of Pogonophora in the Atlantic Ocean. Symposia of the Zoological Society of London, no. 19, 145158.Google Scholar
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. Marine Ecology-Progress Series, 28, 233240.CrossRefGoogle Scholar
Truper, H. G., 1982. Microbial processes in the sulfur cycle through time. In Mineral Deposits and the Evolution of the Biosphere (ed. Holland, H. H. and Schildowski, M.), pp. 530. Berlin: Springer Verlag.CrossRefGoogle Scholar
Wassmann, P. & Aadnesen, A., 1984. Hydrography, nutrients, suspended organic matter, and primary production in a shallow fjord system on the west coast of Norway. Sarsia, 69, 139153.CrossRefGoogle Scholar
Webb, M., 1964. Additional notes on Sclerolinum brattstromi (Pogonophora) and the establishment of a new family, Sclerolinidae. Sarsia, 16, 4758.CrossRefGoogle Scholar
Webb, M., 1965. Notes on the distribution of Pogonophora in Norwegian fjords. Sarsia, 18, 1115.CrossRefGoogle Scholar
Wiborg, K. F., 1944. The production of zooplankton in a land-locked fjord. Fiskeridirektoratets skrifter (ser. Havundersogelser), 7 (7), 83 pp.Google Scholar
Wiborg, K. F., 1971. Investigations on euphausids in some fjords on the west coast of Norway in 1966–1969. Fiskeridirektoratets skrifter (ser. Havundersagelser), 16, 1035.Google Scholar