Abstract
Dinitrogen fixation associated with bacteria in the gastrointestinal tract of sea urchins appears to be a widespread phenomenon: sea urchins from the tropics (Diadema antillarum, Echinometra lacunter, Tripneustes ventricosus), the temperature zone (Strongylocentrotus droebachiensis) and the arctic (S. droebachiensis) exhibited nitrogenase activity (C2H2 reduction). Pronounced seasonal variation was found in nitrogenase activity of temperate sea urchins feeding on kelp (Laminaria spp.) and eelgrass (Zostera marina). The mean monthly nitrogenase activity was inversely correlated with the nitrogen content of the sea urchin's food, which varied up to fivefold over the course of a year. The highest rate of nitrogenase activity recorded for a temperate sea urchin during the 14 month sampling period was 11.6μg N fixed g wet wt-1 d-1, with a yearly mean activity of 1.36 μg N fixed g wet wt-1 d-1. Studies with 15N confirmed the C2H2 reduction results and showed incorporation of microbially-fixed nitrogen into S. droebachiensis demonstrating that N2 fixation can be a source of N for the sea urchin. Laboratory experiments indicated that part of the sea urchin's (S. droebachiensis) normal gastrointestinal microflora is responsible for the observed nitrogenase activity.
Similar content being viewed by others
Literature Cited
Beeson, R. J. and P. T. Johnson: Natural bacterial flora of the bean clam, Donax gouldi. J. Invert. Pathol. 9, 104–110 (1967)
Benemann, J. R.: Nitrogen fixation in termites. Science, N. Y. 181, 164–165 (1973)
Bergersen, F. J. and E. H. Hipsley: The presence of N2-fixing bacteria in the intestines of man and animals. J. Gen. Microbiol. 60, 61–65 (1970)
Boyd, C. E. and C. P. Goodyear: Nutritive quality of food in ecological systems. Arch. Hydrobiol. 69, 256–270 (1971)
Bremner, J. M. and A. P. Edwards: Determination and isotoperatio analysis of different forms of nitrogen in soils. I. Apparatus and procedures for distillation of ammonium. Soil Sci. Soc. Am. Proc. 29, 504–507 (1965)
Breznak, J. A.: Symbiotic relationships between termites and their intestinal microbiota. In: Symbiosis (Society for Experimental Biology Symposium Ser., no. 29), pp 559–580. Ed. by D. H. Jenning and D. L. Lee. Cambridge University Press 1975
Breznak, J. A., W. J. Brill, J. W. Mertins and H. C. Cooper: Nitrogen fixation in termites. Nature, Lond. 244, 577–580 (1973)
Burkholder, P. R., L. M. Burkholder and L. R. Almodovar: Nutritive constituents of some Caribbean marine algae. Bot. Mar. 14, 132–135 (1971)
Carpenter, E. J. and J. L. Culliney: Nitrogen fixation in marine shipworms. Science, N. Y. 187, 551–552 (1975)
Chapman, A. R. O. and J. S. Craigie: Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar. Biol. 40, 197–205 (1977)
Chapman, A. R. O. and J. E. Lindley: Seasonal growth of Laminaria solidungula in the Canadian High Arctic in relation to irradiance and dissolved nutrient concentrations. Mar. Biol. 57, 1–5 (1980)
Cochran, W. G.: Estimation of bacterial densities by means of the “Most Probable Number”. Biometrics 6, 105–116 (1950)
Colwell, R. R. and J. Liston: Microbiology of shellfish. Bacteriological study of the natural flora of Pacific oysters (Crassostrea gigas). Appl. Microbiol. 8, 104–109 (1960)
Colwell, R. R. and J. Liston: The natural bacterial flora of certain marine invertebrates. J. Insect Pathol. 4, 23–33 (1962)
Dilworth, M. J.: Dinitrogen fixation. Ann. Rev. Plant. Physiol. 25, 81–114 (1974)
Ebert, T. A.: Growth rates of the sea urchin Strongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49, 1075–1091 (1968)
Elleway, R. F., J. R. Sabine and D. J. D. Nicholas: Acetylene reduction by rumen microflora. Arch. Mikrobiol. 76, 277–291 (1971)
Emlen, J. M.: Ecology: An evolutionary approach, 493 pp. Reading: Addison-Wesley Pub. Co. 1973
Farmanfarmaian, A. and J. H. Phillips: Digestion, storage and translocation of nutrients in the purple sea urchin (Strongylocentrotus purpuratus). Biol. Bull. 123, 105–120 (1962)
Fiedler, R. and G. Proksch: The determination of 15N by emission and mass spectrometry in biochemical analysis: a review. Anal. Chim. Acta 78, 1–62 (1975)
Fong, W. and K. H. Mann: Role of gut flora in the transfer of amino acids through a marine food chain. Can. J. Fish. Aquat. Sci. 37, 88–96 (1980)
Fuji, A.: Ecological studies on the growth and food consumption of Japanese common littoral sea urchin, Strongylocentrotus intermedius (A. Agassiz). Mem. Fac. Fish. Hokkaido Univ. 15, 83–160 (1967)
Granhall, U. and P. Ciszuk: Nitrogen fixation in rumen contents indicated by the acetylene reduction test. J. Gen. Microbiol. 65, 91–93 (1971)
Guerinot, M. L. and D. G. Patriquin: N2-fixing vibrios isolated from the gastrointestinal tract of sea urchins. Can. J. Microbiol. 27, 311–317 (1981)
Guerinot, M. L., W. Fong and D. G. Patriquin: Nitrogen fixation (acetylene reduction) associated with sea urchins (Strongylocentrotus droebachiensis) feeding on seaweeds and eelgrass. J. Fish. Res. Bd Can. 34, 416–420 (1977)
Hardy, R. W. F., R. D. Holsten, E. K. Jackson and R. C. Burns: The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol. 43, 1185–1207 (1968)
Harrison, P. G. and K. H. Mann: Chemical changes during the seasonal cycle of growth and decay in eelgrass (Zostera marina) on the Atlantic coast of Canada. J. Fish. Res. Bd Can. 32, 615–621 (1975)
Hobson, P. N., R. Summers, J. R. Postgate and D. A. Ware: Nitrogen fixation in the rumen of a living sheep. J. Gen. Microbiol. 77, 225–226 (1973)
Hood, M. A. and S. P. Meyers: Microbial aspects of penaeid shrimp digestion. In: Proc. 26th Ann. Meeting Gulf and Caribbean Fish., New Orleans, pp 81–92. 1974
Jones, G. A. and A. Taylor: Gas metabolism in ovine rumen cultures on a nitrogen-deficient medium. Can. J. Microbiol. 21, 1803–1806 (1975)
Jones, K. and J. G. Thomas: Nitrogen fixation by the rumen contents of sheep. J. Gen. Microbiol. 85, 97–101 (1974)
Lasker, R. and A. C. Giese: Nutrition of the sea urchin, Strongylocentrotus purpuratus. Biol. Bull. 106, 328–340 (1954)
Lawrence, J. M.: On the relationships between marine plants and sea urchins. Oceanogr. mar. Biol. Ann. Rev. 13, 213–286 (1975)
Lilly, G. R.: The influence of diet on the growth and bioenergetics of the tropical sea urchin, Tripneustes ventricosus. 216 pp. Ph.D. thesis, University of British Columbia 1975
LiPun, H. H. and L. D. Satter: Nitrogen fixation in ruminants. J. Anim. Sci. 41, 1161–1163 (1975)
Liston, J. and R. R. Colwell: Host and habitat relationships of marine commensal bacteria. In: Symposium on marine microbiology, pp 611–624. Ed. by C. H. Oppenheimer. Springfield: Charles C. Thomas 1963
Mann, K. H.: Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada. I. Zonation and biomass of seaweeds. Mar. Biol. 12, 1–10 (1972)
Miller, P. J. and K. H. Mann: Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada. III. Energy transformations by sea urchins. Mar. Biol. 18, 99–114 (1973)
Oomen, H. A. P. C.: Interrelationship of the human intestinal flora and protein utilization. Proc. Nutr. Soc. 29, 197–206 (1970)
Patriquin, D. G.: The origin of nitrogen and phosphorus for growth of the marine angiosperm Thalassia testudinum. Mar. Biol. 15, 35–46 (1972)
Patriquin, D. G. and C. Keddy: Nitrogenase activity (acetylene reduction) in a Nova Scotia salt marsh: its association with angiosperms and the influence of some edaphic factors. Aquat. Bot. 4, 227–244 (1978)
Prim, P. and J. M. Lawrence: Utilization of marine plants and their constituents by bacteria isolated from the gut of Echinoids (Echinodermata). Mar. Biol. 33, 167–173 (1975)
Rennie, R. J., D. A. Rennie and M. Fried: Concepts of 15N usage in dinitrogen fixation studies. In: Isotopes in biological dinitrogen fixation, pp 107–113. Vienna: International Atomic Energy Agency 1978
Russell-Hunter, W. D.: Aquatic productivity. 306 pp. London: Collier-Macmillan 1970
Sochard, M. R., D. F. Wilson, B. Austin and R. R. Colwell: Bacteria associated with the surface and gut of marine copepods. Appl. environ. Microbiol. 37, 750–759 (1979)
Solórzano, L.: Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr. 14, 799–801 (1969)
Stewart, W. D. P.: Nitrogen turnover in marine and brackish habitats. II. Use of 15N in measuring nitrogen fixation in the field. Ann. Bot. N.S. 31, 385–407 (1967)
Strickland, J. D. H. and T. R. Parsons: A practical handbook of seawater analysis. 310 pp. Ottawa: Fish. Res. Bd Can. Bull. 167, 1972
Tokin, I. B. and G. F. Filimonova: Electron microscope study of the digestive system of Strongylocentrotus droebachiensis (Echinodermata: Echinoidea). Mar. Biol. 44, 143–155 (1977)
Unkles, S. E.: Bacterial flora of the sea urchin Echinus esculentus. Appl. environ. Microbiol. 34, 347–350 (1977)
Vadas, R. L.: Preferential feeding: an optimization strategy in sea urchins. Ecol. Monogr. 47, 337–371 (1977)
Wilkinson, C. R.: Microbial associations in sponges. II. Numerical analysis of sponge and water bacterial populations. Mar. Biol. 49, 169–176 (1978)
Author information
Authors and Affiliations
Additional information
Communicated by R. O. Fournier, Halifax
Rights and permissions
About this article
Cite this article
Guerinot, M.L., Patriquin, D.G. The association of N2-fixing bacteria with sea urchins. Mar. Biol. 62, 197–207 (1981). https://doi.org/10.1007/BF00388183
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00388183