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Nitrogen cycling in microbial mats: rates and patterns of denitrification and nitrogen fixation

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Abstract

Spatial and temporal variations in nitrogen fixation and denitrification rates were examined between July 1991 and September 1992 in the intertidal regions of Tomales Bay (California, USA). Microbial mat communities inhabited exposed mudflat and vegetated marsh surface sediments. Mudflat and marsh sediments exhibited comparable rates of nitrogen fixation. Denitrification rates were higher in marsh sediments. Nitrogen fixation rates were lowest during January at both sites, whereas highest rates occurred during summer and fall. Denitrification rates were highest during fall and winter months in marsh sediments, while rates in mudflat sediments were highest during summer and fall. In mudflat sediments, nitrogen fixation and denitrification rates, integrated over 24 h, ranged from 6 to 79 mg N m-1 d-1 and 1 to 10 mg N m-2 d-1, respectively. Rates of denitrification represented between 6 and 20% of nitrogen fixation rates during the day, but exceeded or were equivalent to nitrogen fixation rates at night. The highest integrated rates of both nitrogen fixation and denitrification occurred during July, whereas, the highest percent loss occurred during spring when denitrification rates amounted to 20% of nitrogen fixation rates during the day. Over an annual cycle, inputs of fixed N to mudflat communities occurred exclusively during daylight. These results underscore the importance of determining integrated diel rates of both nitrogen fixation and denitrification when constructing N budgets. Using this approach, it was shown that microbial denitrification can represent a significant loss of combined nitrogen from mats on daily as well as monthly time scales.

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References

  • Aizenshtat Z, Lipiner G, Cohen Y (1984) Biogeochemistry of carbon and sulfur cycle in the microbial mats of the Solar Lake (Sinai). In: Cohen Y, Castenholtz RW, Halverson HO (eds) Microbial mats: stromatolites. Am Soc Microbiol, Washington, DC, pp 149–170

    Google Scholar 

  • Andersen TK, Jensen MH, Sørensen J (1984) Diurnal variation of nitrogen cycling in coastal, marine sediments. I Denitrification Mar Biol 83:171–176

    Google Scholar 

  • Bautista MF, Paerl HW (1985) Diel N2 fixation in an intertidal marine microbial mat community. Mar Chem 16:369–377

    Google Scholar 

  • Bebout BM (1992) Interactions of nitrogen and carbon cycling in microbial mats and stromatolites. PhD Dissertation. Univ of North Carolina at Chapel Hill, North Carolina

    Google Scholar 

  • Bebout BM, Fitzpatrick MW, Paerl HW (1993) Identification of the sources of energy for nitrogen fixation and physiological characterization of the nitrogen-fixing members of a marine microbial mat community. Appl envirl Microbiol 59:1495–1503

    Google Scholar 

  • Bebout BM, Paerl HW, Crocker KM, Prufert LE (1987) Diel interactions of oxygenic photosynthesis and N2 fixation (acetylene reduction) in a marine microbial mat community. Appl envirl Microbiol 53:2353–2362

    Google Scholar 

  • Caffrey JM, Kemp WM (1990) Nitrogen cycling in sediments with estuarine populations of Potamogeton perfoliatus and Zostera marina. Mar Ecol Prog Ser 66:147–160

    Google Scholar 

  • Canfield DE, Des Marias DJ (1991) Aerobic sulfate reduction in microbial mats. Science, NY 251:1471–1473

    Google Scholar 

  • Canfield DE, Des Marias DJ (1993) Biogeochemical cycles of carbon, sulfur and free oxygen in a microbial mat. Geochim cosmochim Acta 57:3971–3984

    Google Scholar 

  • Capone DG (1983) Benthic nitrogen fixation. In: Carpenter EJ, Capone DG (eds) Nitrogen in the marine environment. Academic Press, New York, pp 105–137

    Google Scholar 

  • Cohen Y, Castenholtz RW, Halverson HO (1984) Microbial mats: stromatolites. Am Soc Microbiol, Washington, DC

    Google Scholar 

  • Cohen Y, Rosenberg H (1989) Microbial mats: physiological ecology of benthic communities. Am Soc Microbiol, Washington, DC

    Google Scholar 

  • Christensea PB, Nielsen LP, Revsbech NP, Sørensen J (1989) Microzonation of denitrification activity in stream sediments as studied with a combined oxygen and nitrous oxide microsensor. Appl envirl Microbiol 55:1234–1241

    Google Scholar 

  • Christensen PB, Nielsen LP, Sørensen J, Revsbech NP (1990) Denitrification in nitrate-rich streams: diel and seasonal variation related to benthic oxygen metabolism. Limnol Oceanogr 35:640–651

    Google Scholar 

  • Dalsgaard T, Revsbech NP (1992) Regulating factors of denitrification in trickling filter biofilms as measured with the oxygen/nitrous oxide microsensor. Fedn eur microbiol Soc. (FEMS) Microbiol Ecol 101:151–164

    Google Scholar 

  • Dank SM, Evans EH, Whittaker PA (1983) Photosynthetic systems: structure, function, and assembly. John Wiley & Sons, Chichester

    Google Scholar 

  • Des Marias DJ, Canfield DE, Bauer JE (1992) Carbon and oxygen budget of subtidal and intertidal microbial mats. Abstract, ASLO Winter Meeting, Santa Fe, New Mexico, USA

  • Dodds WK (1989) Microscale vertical profiles of N2 fixation, photosynthesis, O2, chiorophyll a and light in a cyanobacterial assemblage. Appl envirl Microbiol 55:882–886

    Google Scholar 

  • Hardy RWF, Holsten M, Jackson RD, Burns EK (1968) The acetylene-ethylene assay for N fixation: laboratory and field evaluation. Pl Physiol 43:1165–1207

    Google Scholar 

  • Henriksen K, Kemp WM (1988) Nitrification in estuarine and coastal marine sediments. In: Blackburn TH, Sørensen J (eds) Nitrogen cycling in coastal marine environments. SCOPE 33. John Wiley & Sons, New York, pp 207–249

    Google Scholar 

  • Javor B, Castenholtz RW (1984) Productivity studies of microbial mats, Laguna Guerrero Negro, Mexico. In: Cohen Y, Castenholtz RW, Halverson HO (eds) Microbial mats: stromatolites. Am Soc Microbiol, Washington, DC, pp 149–170

    Google Scholar 

  • Jenkins MC, Kemp WM (1984) The coupling of nitrification and denitrification in two estuarine sediments. Limnol Oceanogr 29:609–619

    Google Scholar 

  • Jorgensen BB, Revsbech NP, Blackburn TH, Cohen Y (1979) Diurnal cycles of oxygen and sulfide microgradients and microbial photosynthesis in a cyanobacterial microbial mat. Appl envirl Microbiol 38:46–58

    Google Scholar 

  • Joye SB (1993) Spatial and temporal patterns of denitrification and nitrogen fixation in the sediments of a Mediterranean-type estuary: Tomales Bay, California. PhD Dissertation. Univ of North Carolina at Chapel Hill, North Carolina

    Google Scholar 

  • Joye SB, Paerl HW (1993a) Nitrogen fixation and denitrification in the intertidal and subtidal environments of Tomales Bay, California. In: Oremland RS (ed) The biogeochemistry of global change: radiative trace gases. Blackwell Scientific, New York, pp 633–653

    Google Scholar 

  • Joye SB, Paerl HW (1993b) Contemporancous N fixation and denitrification in marine microbial mats: rapid response to runoff events. Mar Ecol Prog Ser 94:267–274

    Google Scholar 

  • Kaplan W, Valiela I, Teal JM (1979) Denitrification in a salt marsh ecosystem. Limnol Oceanogr 24:726–734

    Google Scholar 

  • Kaspar HF (1982) Denitrification in marine sediments: measurement of capacity and estimate of in situ rate. Appl envirl Microbiol 43:522–527

    Google Scholar 

  • Kemp WM, Sampou P, Caffrey J, Meyer M, Henriksen K, Boynton WR (1990) Ammonium recycling versus denitrification in Chesapeake Bay sediments. Limnol Oceanogr 35:1545–1563

    Google Scholar 

  • Knowles R (1982) Denitrification. Microbiol Rev 46:43–70

    Google Scholar 

  • Kreig NR, Hoffman PS (1986) Microaerophily and oxygen toxicity. A Rev Microbiol 40:107–130

    Google Scholar 

  • Nielsen LP, Christensen PB, Revsbech NP, Sørensen J (1990a) Denitrification and oxygen respiration in biofilms studied with a microsensor for nitrous oxide and oxygen. Microb Ecol 19:63–72

    Google Scholar 

  • Nielsen LP, Christensen PB, Revsbech NP, Sørensen J (1990b) Denitrification and photosynthesis in stream sediment studied with microsensor and whole-core techniques. Limnol Oceanogr 35:1135–1144

    Google Scholar 

  • Oberdorfer JA, Valentino MA, Smith SV (1990) Groundwater contribution to the nutrient budget of Tomales Bay, California. Biogeochemistry (Dordrecht) 10:199–216

    Google Scholar 

  • Oremiand RS, Capone DG (1987) Use of specific inhibitors in microbial ecology and biogeochemical studies. In: Marshall KC (ed) Advances in microbial ecology, Vol. 10. Plenum Press, New York, pp 285–383

    Google Scholar 

  • Paerl HW (1984a) Interactions with bacteria. In: Carr MR, Whitton RW (eds) The biology of cyanobacteria. Blackwell Scientific, Oxford, pp 441–461

    Google Scholar 

  • Paerl HW (1984b) Transfer of N2 and CO2 fixation products from Anabaena oscillaroides to associated bacteria during inorganic carbon sufficiency and efficiency. J Phycol 20:600–608

    Google Scholar 

  • Paerl HW, Bebout BM, Prufert LE (1989) Diel patterns of oxygenic photosynthesis and nitrogen fixation in microbial mats. In: Cohen Y, Rosenberg H (eds) Microbial mats: physiological ecology of benthic microbial communities. Am Soc Microbiol, Washington, DC, pp 326–341

    Google Scholar 

  • Paerl HW, Prufert LE (1987) Oxygen-poor microzones as potential sites of microbial N2 fixation in nitrogen-depleted aerobic marine waters. Appl envirl Microbiol 53:1078–1087

    Google Scholar 

  • Paerl HW, Prufert LE, Ambrose WW (1991) Contemporaneous N2 fixation and oxygenic photosynthesis in the non-heterocystous mat-forming Lyngbya aestuarii. Appl envirl Microbiol 57:3086–3092

    Google Scholar 

  • Revsbech NP, Christensen PB, Nielsen LP (1989) Microelectrode analysis of photosynthesis and respiratory processes in microbial mats. In: Cohen Y, Rosenberg H (eds) Microbial mats: physiological ecology of benthic microbial communities. Am Soc Microbiol Washington, DC, pp 153–163

    Google Scholar 

  • Revsbech NP, Sørensen J (1990) Combined use of acetylene inhibition and microsensors for quantification of denitrification in sediments and biofilms. In: Revsbech NP, Sørensen J (eds) Denitrification in soils and sediment. FEMS Symposium No 56. Plenum Press, New York, pp 259–276

    Google Scholar 

  • Revsbech NP, Ward DM (1984) Microprofiles of dissolved substances and photosynthesis in microbial mats measured with microelectrodes. In: Cohen Y, Castenholtz RW, Halverson HO (eds) Microbial mats: stromatolites. Am Soc Microbiol, Washington, DC, pp 171–188

    Google Scholar 

  • Robertson LA, Kuenen JG (1984) Aerobic denitrification: a controversy reviewed. Archs Microbiol 139:351–354

    Google Scholar 

  • SAS Institute 1987 SAS/STAT guide for personal computers. Version 6 Edition. SAS Institute Inc., Cary, North Carolina

    Google Scholar 

  • Skyring GW, Lynch RM, Smith GD (1989) Quantitative relationships between carbon, hydrogen, and sulfur metabolism in cyanobacterial mats. In: Cohen Y, Rosenberg H (eds) Microbial mats: physiological ecology of benthic microbial communities. Am Soc Microbiol, Washington, DC, pp 170–179

    Google Scholar 

  • Smith SV, Hollibaugh JT, Dollar SJ, Vink SM (1991) Tomales Bay metabolism: C−N−P stoichiometry and ecosystem heterotrophy at the land-sea interface. Est cstl Shelf Sci 33:223–257

    Google Scholar 

  • Sørensen J (1978) Denitrification rates in a marine sediment as measured by the acetylene inhibition technique. Appl envirl Microbiol 36:139–143

    Google Scholar 

  • Sørensen J, Rasmussen LK, Koike I (1987) Micromolar sulfide concentrations alleviate acetylene blockage of nitrous oxide reduction by denitrifying Pseudomonas fluorescens. Can J Microbiol 33:1001–1005

    Google Scholar 

  • Stal LJ, Grossberger S, Krumbein WE (1984) Nitrogen fixation associated with the cyanobacterial mat of a marine laminated microbial ecosystem. Mar Biol 82:217–224

    Google Scholar 

  • Stal LJ, Krumbien WE (1982) Nitrogen fixation in a laminated microbial ecosystem. Zentbl Bakt Mikrobiol Hyg (Abt Orig C) 3:564–575

    Google Scholar 

  • Stal LJ, Krumbein WE (1987) Temporal separation of nitrogen fixation and photosynthesis in the filamentous, non-heterocystous cyanobacterium Oscillatoria sp. Archs Microbiol 149:76–80

    Google Scholar 

  • Tam TY, Knowles R (1979) Effects of sulfide and acetylene on nitrous oxide reduction by soil and Pseudomonas florescens. Appl envirl Microbiol 39:105–108

    Google Scholar 

  • Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley & Sons, New York, pp 179–243

    Google Scholar 

  • Tiedje JM, Simkins S, Groffman PM (1989) Perspectives on measurement of denitrification in the field including recommended protocols for acetylene based methods. Pl Soil 115:261–284

    Google Scholar 

  • Valiela I, Teal JM (1979) The nitrogen budget of a salt marsh ecosystem. Nature, Lond 280:652–656

    Google Scholar 

  • Van Raalte CD, Patriquin DG (1979) Use of the acetylene blockage technique for assaying denitrification in a salt marsh. Mar Biol 52:315–320

    Google Scholar 

  • Villbrandt M, Stal LJ, Krumbein WE (1990) Interactions between N fixation and oxygenic photosynthesis in a marine cyanobacterial mat. Fedn eur microbial Soc (FEMS) Microbiol Ecol 74:59–72

    Google Scholar 

  • Ward DM, Beck E, Revsbech NP, Sandbeck KA, Winfrey MR (1984) Decomposition of hotspring microbial mats. In: Cohen Y, Castenholtz RW, Halverson HO (eds) Microbial mats: stromatolites. Am Soc Microbiol, Washington, DC, pp 191–214

    Google Scholar 

  • Zedler JB (1980) Algal mat productivity: comparisons in a salt marsh. Estuaries 3:122–132

    Google Scholar 

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Communicated by J. P. Grassle, New Brunswick

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Joye, S.B., Paerl, H.W. Nitrogen cycling in microbial mats: rates and patterns of denitrification and nitrogen fixation. Marine Biology 119, 285–295 (1994). https://doi.org/10.1007/BF00349568

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