Skip to main content
Log in

Nitrogenase Activity and nifH Expression in a Marine Intertidal Microbial Mat

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

N2 fixation, diazotrophic community composition, and organisms actively expressing genes for N2 fixation were examined over at 3−year period (1997–1999) for intertidal microbial mats on a sand flat located in the Rachel Carson National Estuarine Research Reserve (RCNERR) (Beaufort, NC, USA). Specifically, diel variations of N2 fixation in the mats from the RCNERR were examined. Three distinct diel patterns of nitrogenase activity (NA) were observed. NA responses to short-term inhibitions of photosynthesis corresponded to one of the three patterns. High rates of NA were observed during peak O2 production periods for diel experiments during summer months. Different types of NA diel variations correspond to different stages of mat development. Chloramphenicol treatments indicated that the mechanism of protein synthesis supporting NA changed throughout the day. Analysis of mat DNA and RNA gave further evidence suggesting that in addition to cyanobacteria, other functional groups were responsible for the NA observed in the RCNERR mats. The role of microbial diversity in the N2 fixation dynamics of these mats is discussed.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. MF Bautista HW Paerl (1985) ArticleTitleDiel N2 fixation in an intertidal marine cyanobacterial mat community Mar Chem 16 369–377 Occurrence Handle10.1016/0304-4203(85)90057-X Occurrence Handle1:CAS:528:DyaL2MXlsVKksLY%3D

    Article  CAS  Google Scholar 

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

  3. BM Bebout MW Fitzpatrick HW Paerl (1993) ArticleTitleIdentification of the sources of energy for nitrogen fixation and physiological characterization of nitrogen-fixing members of a marine microbial mat community Appl Environ Microbiol 59 1495–1503 Occurrence Handle1:CAS:528:DyaK3sXkt1Cns74%3D

    CAS  Google Scholar 

  4. BM Bebout HW Paerl JE Bauer DE Canfield DJ Des Marais (1994) Nitrogen cycling in microbial mat communities: the quantitative importance of N-fixation and other sources of N for primary production LJ Stal P Caumette (Eds) Microbial Mats: Structure, Development, and Environmental Significance Springer-Verlag Berlin 265–278

    Google Scholar 

  5. BM Bebout HW Paerl KM Crocker LE Prufert (1987) ArticleTitleDiel interactions of oxygenic photosynthesis and nitrogen fixation (acetylene reduction) in a marine microbial mat community Appl Environ Microbiol 53 2353–2362 Occurrence Handle1:CAS:528:DyaL1cXjsFOj

    CAS  Google Scholar 

  6. B Bergman JR Gallon AN Rai LJ Stal (1997) ArticleTitleN2 fixation by non-heterocystous cyanobacteria FEMS Microbiol Rev 19 139–185 Occurrence Handle10.1016/S0168-6445(96)00028-9 Occurrence Handle1:CAS:528:DyaK2sXptlSksA%3D%3D

    Article  CAS  Google Scholar 

  7. Y Cohen RW Castenholz HO Halverson (1984) Microbial Mats: Stromatolites Alan Liss New York

    Google Scholar 

  8. G Gerdes WE Krumbein (1994) Pertidal potential stromatolites: a synopsis J Bertrand-Sarfatti C Monty (Eds) Phanerozoic Stromatolites II Kluwer Academic Publishers Dordrecht 101–129

    Google Scholar 

  9. Felsenstein, J (1995) Phylip [Phylogeny Inference Package (3.57)]. University of Washington

  10. K Jones (1982) ArticleTitleNitrogen fixation in the temperate estuarine intertidal sediments of the River Lune Limnol Oceanogr 27 455–460 Occurrence Handle1:CAS:528:DyaL38Xks1SmsLY%3D

    CAS  Google Scholar 

  11. K Jones (1992) ArticleTitleDiurnal nitrogen fixation in tropical marine cyanobacteria: a comparison between adjacent communities of non-heterocystous Lyngbya sp. and heterocystous Calothrix sp. B Phycol J 27 107–118

    Google Scholar 

  12. P Macheroux S Hill S Austin T Eydmann T Jones (1998) ArticleTitleElectron donation to the flavoprotein NifL, a redox-sensing transcriptional regulator Biochem J 332 413–419 Occurrence Handle1:CAS:528:DyaK1cXkt1SqsLk%3D Occurrence Handle9601070

    CAS  PubMed  Google Scholar 

  13. JB Olson TF Steppe RW Litaker HW Paerl (1998) ArticleTitleN2 fixing microbial consortia associated with the ice cover of Lake Bonney, Antarctica Microb Ecol 36 231–238 Occurrence Handle10.1007/s002489900110 Occurrence Handle1:CAS:528:DyaK1MXks1CktA%3D%3D Occurrence Handle9852503

    Article  CAS  PubMed  Google Scholar 

  14. JB Olson RW Litaker HW Paerl (1999) ArticleTitleUbiquity of heterotrophic diazotrophs in marine microbial mats Aquat Microb Ecol 19 29–36

    Google Scholar 

  15. HW Paerl M Fitzpatrick BM Bebout (1996) ArticleTitleSeasonal nitrogen fixation dynamics in a marine microbial mat: potential roles of cyanobacteria and microheterotrophs Limnol Oceanogr 41 419–427 Occurrence Handle1:CAS:528:DyaK28XkvFKht74%3D

    CAS  Google Scholar 

  16. HW Paerl JL Pinckney TF Steppe (2000) ArticleTitleCyanobacterial-bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments Environ Microbiol 2 11–25 Occurrence Handle10.1046/j.1462-2920.2000.00071.x Occurrence Handle1:STN:280:DC%2BD3M3jtlylsg%3D%3D Occurrence Handle11243256

    Article  CAS  PubMed  Google Scholar 

  17. HW Paerl LE Prufert WW Ambrose (1991) ArticleTitleContemporaneous nitrogen fixation and oxygenic photosynthesis in the non-heterocystous mat-forming cyanobacterium Lyngbya aestuarii Appl Environ Microbiol 57 3086–3092 Occurrence Handle1:CAS:528:DyaK3MXmslGnu7g%3D

    CAS  Google Scholar 

  18. JL Pinckney HW Paerl M Fitzpatrick (1995) ArticleTitleImpacts of seasonality and nutrients on microbial mat community structure and function Mar Ecol Prog Ser 123 207–216

    Google Scholar 

  19. JR Postgate (1982) The Fundamentals of Nitrogen Fixation Cambridge University Press Cambridge, UK

    Google Scholar 

  20. JR Postgate HM Kent RL Robson (1988) Nitrogen fixation by Desulfovibrio JA Cole SJ Ferguson (Eds) The Nitrogen and Sulphur Cycles Cambridge University Press Cambridge, UK 457–471

    Google Scholar 

  21. N Revsbech BB Jørgensen TH Blackburn (1983) ArticleTitleMicroelectrode studies of the photosynthesis and O2, H2S, and pH profiles of a microbial mat Limnol Oceanogr 28 1062–1074

    Google Scholar 

  22. GW Skyring RM Lynch GD Smith (1988) ArticleTitleAcetylene reduction and hydrogen metabolism by a cyanobacterial-sulfate-reducing bacterial mat ecosystem GeoMicrobiol 6 25–32 Occurrence Handle1:CAS:528:DyaL1cXls1Ojsrc%3D

    CAS  Google Scholar 

  23. L Stal P Caumette (1994) Microbial Mats: Structure, Development, and Environmental Significance Springer-Verlag Berlin

    Google Scholar 

  24. LJ Stal S Grossberger WE Krumbein (1984) ArticleTitleNitrogen fixation associated with the cyanobacterial mat of a marine laminated microbial ecosystem Mar Biol 82 217–224 Occurrence Handle10.1007/BF00392402 Occurrence Handle1:CAS:528:DyaL2MXitVSqs78%3D

    Article  CAS  Google Scholar 

  25. LJ Stal WE Krumbein (1985) ArticleTitleNitrogenase activity in the non-heterocystous cyanobacterium Oscillatoria sp grown under alternating light–dark cycles Arch Microbiol 143 67–71 Occurrence Handle10.1007/BF00414770 Occurrence Handle1:CAS:528:DyaL2MXmtFSlu78%3D

    Article  CAS  Google Scholar 

  26. LJ Stal WE Krumbein (1987) ArticleTitleTemporal separation of nitrogen fixation and photosynthesis in the filamentous non-heterocystous cyanobacterium Oscillatoria sp. Arch Microbiol 149 76–80 Occurrence Handle10.1007/BF00423140 Occurrence Handle1:CAS:528:DyaL1cXntFyitA%3D%3D

    Article  CAS  Google Scholar 

  27. LJ Stal H Gemerden Particlevan WE Krumbein (1985) ArticleTitleStructure and development of a benthic marine microbial mat FEMS Microb Ecol 31 111–126 Occurrence Handle10.1016/0378-1097(85)90007-2 Occurrence Handle1:CAS:528:DyaL2MXls1Gksr0%3D

    Article  CAS  Google Scholar 

  28. LJ Stal (1995) ArticleTitlePhysiological ecology of cyanobacteria in microbial mats and other communities Tansley Rev 84 New Phytol 131 1–32 Occurrence Handle1:CAS:528:DyaK2MXptFShsLk%3D

    CAS  Google Scholar 

  29. TF Steppe JB Olson HW Paerl RW Litaker J Belnap (1996) ArticleTitleConsortial N2 fixation: a strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats FEMS Microbiol Ecol 21 149–156 Occurrence Handle10.1016/S0168-6496(96)00047-5 Occurrence Handle1:CAS:528:DyaK28XmsVynsr0%3D

    Article  CAS  Google Scholar 

  30. TF Steppe HW Paerl (2002) ArticleTitlePotential N2 fixation by sulfate-reducing bacteria in a marine intertidal microbial mat Aquat Microb Ecol 28 1–2

    Google Scholar 

  31. TF Steppe JL Pinckney J Dyble HW Paerl (2001) ArticleTitleDiazotrophy in modern marine Bahamian Stromatolies Microb Ecol 41 36–44 Occurrence Handle1:CAS:528:DC%2BD3MXjvFygtbw%3D Occurrence Handle11252162

    CAS  PubMed  Google Scholar 

  32. H Gemerden Particlevan (1993) ArticleTitleMicrobial mats: a joint venture Mar Geol 113 3–25 Occurrence Handle10.1016/0025-3227(93)90146-M

    Article  Google Scholar 

  33. M Villbrandt LJ Stal WE Krumbein (1990) ArticleTitleInteractions between nitrogen fixation and oxygenic photosynthesis in a marine cyanobacterial mat FEMS Microbiol Ecol 74 59–72 Occurrence Handle10.1016/0378-1097(90)90516-S Occurrence Handle1:CAS:528:DyaK3cXmt1Oktbw%3D

    Article  CAS  Google Scholar 

  34. JP Zehr LA McReynolds (1989) ArticleTitleUse of degenerate oligonucleotides for amplification of the nifH gene from Trichodesmium thiebautii Appl Environ Microbiol 55 2522–2526 Occurrence Handle1:CAS:528:DyaL1MXlvVymsrk%3D Occurrence Handle2513774

    CAS  PubMed  Google Scholar 

  35. JP Zehr J Mellon S Braun W Litaker T Steppe HW Paerl (1995) ArticleTitleDiversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat Appl Environ Microbiol 61 2527–2532 Occurrence Handle1:CAS:528:DyaK2MXms1Gkur8%3D

    CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge Tom Nanni and John Fear for technical assistance. This work was supported by NSF LEXEN 980895 and NSF Microbial Observatories 0132528.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T.F. Steppe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Steppe, T., Paerl, H. Nitrogenase Activity and nifH Expression in a Marine Intertidal Microbial Mat. Microb Ecol 49, 315–324 (2005). https://doi.org/10.1007/s00248-004-0245-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-004-0245-x

Keywords

Navigation