Skip to main content
SpringerLink
Log in

Seasonal variation in rates of heterotrophic nitrogen fixation (acetylene reduction) in Zostera noltii meadows and uncolonised sediments of the Bassin d'Arcachon, south-west France

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Nitrogen fixation (acetylene reduction) rates were measured over an annual cycle in meadows of the seagrass Z. noltii and uncolonised sediments of the Bassin d'Arcachon, south-west France, using both slurry and whole core techniques. Measured rates using the slurry technique in Z. noltii colonised sediments were consistently higher than those determined in isolated cores. This was probably due to the release of labile organic carbon sources during preparation of the slurries. Thus, in colonised sediments the whole core technique may provide a more accurate estimate of in situ activity. Acetylene reduction rates measured by the whole core technique in colonised sediments were 1.8 to 4-fold greater, dependent upon the season, in the light compared with those measured in the dark, indicating that organic carbon released by the plant roots during photosynthesis was an important factor regulating nitrogen fixation. In contrast acetylene reduction rates in uncolonised sediments were independent of light.

Addition of sodium molybdate, a specific inhibitor of sulphate reduction inhibited acetylene reduction activity in Z. noltii colonised sediments by > 80% as measured by both slurry and whole core techniques irrespective of the light regime, throughout the year inferring that sulphate reducing bacteria (SRB) were the dominant component of the nitrogen fixing microflora. A mutualistic relationship between Z. noltii and nitrogen fixing SRB in the rhizosphere, based on the exchange of organic carbon and fixed nitrogen is proposed. In uncolonised sediments sodium molybdate initially severely inhibited acetylene reduction rates, but the level of this inhibition declined over the course of the year. These data indicate that the nitrogen fixing SRB associated with the Zostera roots and rhizomes were progressively replaced by an aerobic population of nitrogen fixers associated with the decomposition of this recalcitrant high C:N ratio organic matter.

Acetylene and sulphate reduction rates in the seagrass beds showed distinct summer maxima which correlated with a reduced availability of NH +4 in the sediment and the growth cycle of Z. noltii in the Bassin. Overall, these data indicate that acetylene reduction (nitrogen fixation) activity in the rhizosphere of Z. noltii was regulated both by release of organic carbon from the plant roots and maintenance of low ammonium concentrations in the root zone due to efficient ammonium assimilation.

Nitrogen fixation rates determined from acetylene reduction rates measured by the whole core technique ranged from 0.1 to 7.3 mg N m−2 d−1 in the Z. noltii beds and between 0.02 and 3.7 mg N m−2 d−1 in uncolonised sediments, dependent upon the season. Nitrogen fixation in the rhizosphere of Z. noltii was calculated to contribute between 0.4 and 1.1 g N m−2 y−1 or between 6.3 and 12% of the annual fixed nitrogen requirement of the plants. Heterotrophic nitrogen fixation therefore represents a substantial local input of fixed nitrogen to the sediments of this shallow coastal lagoon and contributes to the overall productivity of Z. noltii in this ecosystem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams, M. W. W. & L. E. Mortensen, 1984. The physical and catalytical properties of hydrogenase II of Clostridium pasteurianum. J. Biol. Chem. 259: 7045–7055.

    Google Scholar 

  • Auby, I., 1991. Contribution à l'étude des herbiers de Zostera noltii dans le Bassin d'Arcachon: dynamique, production et dégradation, macrofaune associée. Ph.D. thesis, Université de Bordeaux I.

  • Auby, I., F. Manaud, D. Maurer & G. Trut, 1994. Etude de la prolifération des algues vertes dans le Bassin d'Arcachon. Rapport IFREMER-CEMAGREF-SSA-SABARC. 163 pp, IFREMER, Arcachon, France.

    Google Scholar 

  • Blackburn, T. H., D. B. Nedwell & W. J. Wiebe, 1994. Active mineral cycling in a Jamaican seagrass sediment. Mar. Ecol. Prog. Ser. 110: 233–239.

    Google Scholar 

  • Boyle, C. D. & D. G. Patriquin, 1981. Carbon metabolism of Spartina alterniflora Loisel in relation to that of associated nitrogen-fixing bacteria. New Phytol. 89: 275–288.

    Google Scholar 

  • Caffrey, J. M. & W. M. Kemp, 1992. Influence of the submersed plant, Potamogeton perfoliatus, on nitrogen cycling in estuarine sediments. Limnol. Oceanogr. 37: 1483–1495.

    Google Scholar 

  • Canfield, D. E., 1989. Sulfate reduction and oxic respiration in marine sediments: implications for organic carbon preservation in euxinic environments. Deep Sea Res. 36: 121–138.

    Google Scholar 

  • Capone, D. G., 1988. Benthic nitrogen fixation. In T. H. Blackburn & J. Sørensen (eds), Nitrogen cycling in coastal marine environments. John Wiley & Sons Ltd, Chichester. 85–123.

    Google Scholar 

  • Capone, D. G. & J. M. Budin, 1982. Nitrogen fixation associated with rinsed roots and rhizomes of the eelgrass Zostera marina. Pl. Physiol. 70: 1601–1604.

    Google Scholar 

  • Capone, D. G., P. A. Penhale, R. S. Oremland & B. F. Taylor, 1979. Relationship between productivity and N2 (C2H2) fixation in the rhizosphere of Thalassia testudinium. Limnol. Oceanogr. 24: 117–125.

    Google Scholar 

  • Capone, D. G. & B. F. Taylor, 1980. N2 fixation in the rhizosphere of Thalassia testudinium. Can. J. Microbiol. 26: 998–1005.

    Google Scholar 

  • Clarke, K. R. & N. J. P. Owens, 1983. A simple and versatile microcomputer program for the determination of ‘most probable number’. J. Microbiol. Meth. 1: 133–137.

    Google Scholar 

  • Dennison, W. C, R. C. Aller & R. S. Alberte, 1987. Sediment ammonium availability and eelgrass (Zostera marina) growth. Mar. Biol. 94: 469–477.

    Google Scholar 

  • Dixon, R. A., 1984. The genetic complexity of nitrogen fixation. J. gen. Microbiol. 130: 2745–2755.

    Google Scholar 

  • Eppley, R. W., E. H. Renger & W. G. Harrison, 1979. Nitrate and phytoplankton production in southern California waters. Limnol. Oceanogr. 24: 483–494.

    Google Scholar 

  • Herbert, R. A., 1975. Heterotrophic nitrogen fixation in shallow estuarine sediments. J. exp. mar. Biol. Ecol. 18: 215–225.

    Google Scholar 

  • Hines, M. E. & W. B. Lyons, 1982. Biogeochemistry of nearshore Bermudan sediments. I. Sulfate reduction rates and nutrient regeneration. Mar. Ecol. Prog. Ser. 8: 87–94.

    Google Scholar 

  • Hines, M. E., S. L. Knollmeyer & J. B. Tugel, 1989. Sulfate reduction and other sedimentary biogeochemistry in a northern New England salt marsh. Limnol. Oceanogr. 34: 578–590.

    Google Scholar 

  • Hines, M. E., G. T. Banta, A. E. Giblin & J. E. Hobbie, 1994. Acetate concentrations and oxidation in salt-marsh sediments. Limnol. Oceanogr. 39: 140–148.

    Google Scholar 

  • Houchins, J. P., 1984. The physiology and biochemistry of hydrogen metabolism in cyanobacteria. Biochim. Biophys. Acta. 768: 227–255.

    Google Scholar 

  • Howes, B. L., J. W. H. Dacey & S. G. Wakeham, 1985. Effects of sampling technique on measurements of porewater constituents in salt marsh sediments. Limnol. Oceanogr. 30: 221–227.

    Google Scholar 

  • Iizumi, H., A. Hattori & C. P. McRoy, 1982. Ammonium regeneration and assimilation in eelgrass (Zostera marina) beds. Mar. Biol. 66: 59–65.

    Google Scholar 

  • Jones, K., 1982. Nitrogen fixation in the temperate estuarine intertidal salt marsh sediments of the river Lune. Limnol. Oceanogr. 22: 814–832.

    Google Scholar 

  • Jørgensen, B. B., 1977. The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnol. Oceanogr. 22: 814–832.

    Google Scholar 

  • Jørgensen, B. B., 1982. Mineralization of organic matter in the sea bed: the role of sulphate reduction. Nature 296: 643–645.

    Google Scholar 

  • Kenworthy, W. J., C. Currin, G. Smith & G. Thayer, 1987. The abundance biomass and acetylene reduction activity of bacteria associated with decomposing rhizomes of two seagrasses, Zostera marina and Thalassia testudinium. Aquat. Bot. 27: 97–119.

    Google Scholar 

  • Kristensen, E., G. M. King, M. Holmer, G. T. Banta, M. H. Jensen, K. Hansen & N. Bussarawit, 1994. Sulfate reduction, acetate turnover and carbon metabolism in sediments of the An Nam Bor mangrove, Phuket, Thailand. Mar. Ecol. Prog. Ser. 109: 245–255.

    Google Scholar 

  • McRoy, C. P. & C. McMillan, 1977. Production, ecology and physiology of seagrasses. In C. P. McRoy & C. Helfferich (eds). Seagrass ecology. Marcel Dekker, New York. 53–87.

    Google Scholar 

  • McRoy, C. P., J. J. Goering & B. Chaney, 1973. Nitrogen fixation associated with seagrasses. Limnol. Oceanogr. 18: 998–1002.

    Google Scholar 

  • Moriarty, D. J. W. & P. I. Boon, 1989. Interactions of seagrasses with sediment and water. In A. W. D. Larkum, A. J. McComb & S. A. Shepherd (eds), Biology of seagrasses. Elsevier, Amsterdam: 500–535.

    Google Scholar 

  • Moriarty, D. J. W. & M. J. O'Donohue, 1993. Nitrogen fixation in seagrass communities during summer in the Gulf of Carpentaria, Australia. Aust. J. mar. Freshwat. Res. 44: 117–125.

    Google Scholar 

  • Moriarty, D. J. W., P. I. Boon, J. A. Hansen, W. G. Hunt, I. R. Poiner, P. C. Pollard, G. W. Skyring & D. C. White, 1985. Microbial biomass and productivity in seagrass beds. Geomicrobiol. J. 4: 21–51.

    Google Scholar 

  • Moriarty, D. J. W., D. G. Roberts & P. C. Polard, 1990. Primary and bacterial productivity of tropical seagrass communities in the Gulf of Carpentaria, Australia. Mar. ecol. Prog. Ser. 61: 145–157.

    Google Scholar 

  • Nazina, T. N., E. P. Rozanova & T. A. Kalininskaya, 1979. Fixation of molecular nitrogen by sulfate-reducing bacteria from oil strata. Mikrobiologiya 48: 133–136.

    Google Scholar 

  • Nedwell, D. & S. Aziz, 1980. Heterotrophic nitrogen fixation in an intertidal salt marsh sediment. Estuar. coast. mar. Sci. 10: 699–702.

    Google Scholar 

  • Nedwell, D. B., T. H. Blackburn & W. J. Wiebe, 1994. Dynamic nature of the turnover of organic carbon, nitrogen and sulphur in the sediments of a Jamacaican mangrove forest. Mar. Ecol. Prog. Ser. 110: 223–231.

    Google Scholar 

  • Nixon, S. W. & M. E. Q. Pilson, 1983. Nitrogen in estuarine and coastal marine ecosystems. In J. E. Carpenter & D. G. Capone (eds), Nitrogen in the marine environment. Academic Press, New York. 565–647.

    Google Scholar 

  • O'Donohue, M. J., D. J. W. Moriarty & I. C. MacRae, 1991a. Nitrogen fixation in sediments and the rhizosphere of the seagrass Zostera capricornia. Microb. Ecol. 22: 53–64.

    Google Scholar 

  • O'Donohue, M. J., D. J. W. Moriarty & I. C. MacRae, 1991b. A comparison of methods for determining rates of acetylene reduction (nitrogen fixation) by heterotrophic bacteria in seagrass sediment. J. Microbiol. Meths. 13: 171–183.

    Google Scholar 

  • Oremland, R. S. & D. G. Capone, 1988. Use of ‘specific inhibitors’ in biogeochemistry and microbial ecology. Adv. Microbiol. Ecol. 10: 285–383.

    Google Scholar 

  • Oremland, R. S., J. W. Gotto & B. F. Taylor, 1976. N2 (C2H2) fixation associated with the rhizosphere communities of the seagrass Thalassia testudinium. Abstracts of the annual meeting of the American Society of Microbiology. abstr. 171.

  • Patriquin, D. G., 1972. The origin of nitrogen and phosphorus for the growth of the marine angiosperm Thalassia testudinium. Mar. Biol. 15: 25–46.

    Google Scholar 

  • Patriquin, D. G. & R. Knowles, 1972. Nitrogen fixation in the rhizosphere of marine angiosperms. Mar. Biol. 16: 49–58.

    Google Scholar 

  • Patriquin, D. G. & C. McClung, 1978. Nitrogen accretion, and the nature and possible significance of N2 fixation (acetylene reduction) in a Nova Scotian Spartina alterniflora stand. Mar. Biol. 47: 227–242.

    Google Scholar 

  • Payne, W. J., 1984. Influence of acetylene on microbial and enzymatic assays. J. Microbiol. Methods. 2: 117–133.

    Google Scholar 

  • Pereg, L. L., Y. Lipkin & N. Sar., 1994. Different niches of the Halophila stipulacea seagrass bed harbor distinct populations of nitrogen fixing bacteria. Mar. Biol. 119: 327–333.

    Google Scholar 

  • Pfennig, N., F. Widdel & H. G. Trüper, 1981. The dissimilatory sulfate reducing bacteria. In M. P. Starr, H. Stolp, H. G. Trüper, A. Balows & H. G. Schlegel (eds), The Prokaryotes vol 1. Springer-Verlag, New York. 926–940.

    Google Scholar 

  • Pfennig, N., H. G. Trüper, 1992. The family Chromatiaceae. In A. Balows, H. G. Trüper, M. Dworkin & K. H. Schleifer (eds), The Prokaryotes, vol 4. Springer-Verlag, New York. 3200–3331.

    Google Scholar 

  • Postgate, J. R., 1982. The fundamentals of nitrogen fixation. Cambridge University Press, London.

    Google Scholar 

  • Postgate, J. R. & H. M. Kent, 1984. Derepression of nitrogen fixation in Desulfovibrio gigas and its stability to ammonia or oxygen stress in vivo. J. gen. Microbiol. 130: 2824–1.

    Google Scholar 

  • Postgate, J. R., H. M. Kent, S. Hill & H. Blackburn, 1985. Nitrogen fixation by Desulfovibrio gigas and other species of Desulfbvib-rio. In P. W. Ludden & J. E. Burris (eds). Nitrogen fixation and CO2 metabolism. Elsevier, Amsterdam. 225–234.

    Google Scholar 

  • Postgate, J. R., H. M. Kent & R. L. Robson, 1988. Nitrogen fixation by Desulfovibrio. In J. A. Cole & S. J. Ferguson (eds). The nitrogen and sulphur cycles. Society of General Microbiology Symposium 42. Cambridge University Press, Cambridge. 457–471.

    Google Scholar 

  • Riederer-Henderson, M. A. & P. W. Wilson, 1970. Nitrogen fixation by sulphate reducing bacteria. J. gen. Microbiol. 61: 27–31.

    Google Scholar 

  • Ryther, J. H. & W. M. Dunstan, 1971. Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science 171: 1008–1013.

    Google Scholar 

  • Short, F. T., 1983. The response of interstitial ammonium in eelgrass (Zostera marina) beds to environmental perturbations. J. exp. mar. Biol. Ecol. 68: 195–208.

    Google Scholar 

  • Smith, R. D., A. M. Pregnall & R. S. Alberte, 1988. Effects of anaerobiosis on root metabolism of Zostera marina (eelgrass): implications for survival in reducing sediments. Mar. Biol. 98: 131–141.

    Google Scholar 

  • Smith, R. I. & M. J. Klug, 1981. Electron donors utilised by sulfate-reducing bacteria in eutrophic lake sediments. Apl. envir. Microbiol. 42: 116–121.

    Google Scholar 

  • Stewart, W. D. P., G. P. Fitzgerald & R. H. Burris, 1967. In situ studies on N2 fixation using the acetylene reduction technique. Proc. not. Acad. Sci. U.S.A. 58: 2071–2078.

    Google Scholar 

  • Taylor, B. F. & R. S. Oremland, 1979. Depletion of adenosine triphosphate in Desulfovibrio by oxyanions of Group IV elements. Curr. Microbiol. 3: 101–103.

    Google Scholar 

  • Voordouw, G., V. Niviere, F. G. Ferris, P. M. Fedorak & D. W. S. Westlake, 1990. Distribution of hydrogenase genes in Desulfovibrio spp. and their use in identification of species from the oilfield environment. Apl. envir. Microbiol. 56: 3748–3754.

    Google Scholar 

  • Welsh, D. T., R. Wellsbury, S. Bourgues, R. de Wit & R. Herbert, 1996. Relationship between porewater organic carbon intent, sulphate reduction and nitrogen fixation (acetylene reduction) in the rhizosphere of Zostera noltii. Hydrobiologia 329 (Dev. Hydrobiol. 117): 169–177.

    Google Scholar 

  • Whiting, G. J., E. L. Gandy & D. C. Yoch, 1986. Tight coupling of root-associated nitrogen fixation and plant photosynthesis in the salt marsh grass Spartina alterniflora and carbon dioxide enhancement of nitrogenase activity. Apl. envir. Microbiol. 52: 108–113.

    Google Scholar 

  • Widdel, F. & F. Bak, 1992. Gram-negative mesophilic sulfate-reducing bacteria. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K. H. Schleifer (eds), The Prokaryotes vol 4. Springer-Verlag, New York. 3352–3378.

    Google Scholar 

  • Wolfenden, J. & K. Jones, 1987. Seasonal variation of in situ nitrogen fixation (C2H2 reduction) in an expanding marsh of Spartina anglica. J. Ecol. 75: 1011–1021.

    Google Scholar 

  • Yoch, D. C. & G. J. Whiting, 1986. Evidence for the NH +4 switch-off regulation of nitrogenase activity by bacteria in salt marsh sediments and roots of the grass Spartina alterniflora. Apl. envir. Microbiol. 51: 143–149.

    Google Scholar 

  • Zuberer, D. A. & W. S. Silver, 1978. Biological dinitrogen fixation (acetylene reduction) associated with Florida mangroves. Apl. envir. Microbiol. 35: 567–575.

    Google Scholar 

  • Zumft, W. G. & F. Castillo, 1978. Regulatory properties of the nitrogenase from Rhodopseudomonas palustris. Arch. Microbiol. 117: 53–60.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Dundee, Miller's Wynd, DD1 4HN, Dundee, Scotland

    David T. Welsh & Rodney A. Herbert

  2. Laboratoire d'Océanographie Biologique, Centre d'Océanographie et de Biologie Marine, Université Bordeaux I, 2 rue Professeur Jolyet, 33120, Arcachon, France

    David T. Welsh & Rutger de Wit

Authors
  1. David T. Welsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sophie Bourguès
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rutger de Wit
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rodney A. Herbert
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Welsh, D.T., Bourguès, S., de Wit, R. et al. Seasonal variation in rates of heterotrophic nitrogen fixation (acetylene reduction) in Zostera noltii meadows and uncolonised sediments of the Bassin d'Arcachon, south-west France. Hydrobiologia 329, 161–174 (1996). https://doi.org/10.1007/BF00034555

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00034555

Key words

Search

Navigation