Microbial Ecology

, Volume 69, Issue 4, pp 778–787 | Cite as

Across-Habitat Comparison of Diazotroph Activity in the Subarctic

  • Kathrin Rousk
  • Pernille L. Sorensen
  • Signe Lett
  • Anders Michelsen
Plant Microbe Interactions

Abstract

Nitrogen (N) fixation by N2-fixing bacteria (diazotrophs) is the primary N input to pristine ecosystems like boreal forests and subarctic and arctic tundra. However, the contribution by the various diazotrophs to habitat N2 fixation remains unclear. We present results from in situ assessments of N2 fixation of five diazotroph associations (with a legume, lichen, feather moss, Sphagnum moss and free-living) incorporating the ground cover of the associations in five typical habitats in the subarctic (wet and dry heath, polygon-heath, birch forest, mire). Further, we assessed the importance of soil and air temperature, as well as moisture conditions for N2 fixation. Across the growing season, the legume had the highest total as well as the highest fraction of N2 fixation rates at habitat level in the heaths (>85 % of habitat N2 fixation), whereas the free-living diazotrophs had the highest N2 fixation rates in the polygon heath (56 %), the lichen in the birch forest (87 %) and Sphagnum in the mire (100 %). The feather moss did not contribute more than 15 % to habitat N2 fixation in any of the habitats despite its high ground cover. Moisture content seemed to be a major driver of N2 fixation in the lichen, feather moss and free-living diazotrophs. Our results show that the range of N2 fixers found in pristine habitats contribute differently to habitat N2 fixation and that ground cover of the associates does not necessarily mirror contribution.

Keywords

Boreal forest Cyanobacteria Heterotrophs Methanotrophs N deposition Nitrogen fixation Subarctic tundra Symbiosis 

References

  1. 1.
    Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochem 13:87–115CrossRefGoogle Scholar
  2. 2.
    Elser JJ, Bracken MES, Gruner DS, Harpole WS, Hillebrand H et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–42CrossRefPubMedGoogle Scholar
  3. 3.
    Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochem 58:1–45CrossRefGoogle Scholar
  4. 4.
    Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW et al (2004) Nitrogen cycles: past, present and future. Biogeochem 70:153–226CrossRefGoogle Scholar
  5. 5.
    Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512CrossRefGoogle Scholar
  6. 6.
    Gundale MJ, DeLuca TH, Nordin A (2011) Bryophytes attenuate anthropogenic nitrogen inputs in boreal forests. Glob Change Biol 17:2743–2753CrossRefGoogle Scholar
  7. 7.
    Karlsson GP, Akselsson C, Hellsten S, Karlsson PE, Malm G (2009) Övervakning av luftföroreningar norra Sverige – mätningar och moddellering. Svenska Miljöinstitut IVL rapport B1851. Lund UniversityGoogle Scholar
  8. 8.
    DeLuca TH, Zackrisson O, Nilsson MC, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917–920CrossRefPubMedGoogle Scholar
  9. 9.
    Millbank JW, Kershaw KA (1969) Nitrogen metabolism in lichens. I. Nitrogen fixation in the cephalopodia of Peltigera aphthosa. New Phytol 68:721–729CrossRefGoogle Scholar
  10. 10.
    Alexander V, Schell DM (1973) Seasonal and spatial variation of nitrogen fixation in the Barrow, Alaska, tundra. Arctic Alpine Res 5:77–88CrossRefGoogle Scholar
  11. 11.
    Basilier K, Granhall U (1978) Nitrogen fixation in wet minerotrophic moss communities of a subarctic mire. Oikos 31:236–246CrossRefGoogle Scholar
  12. 12.
    Smith VR (1984) Effects of abiotic factors on acetylene reduction by cyanobacteria epiphytic on moss at a subantarctic island. Appl Environ Microbiol 48:594–600PubMedCentralPubMedGoogle Scholar
  13. 13.
    Van Cleve K, Oliver LK, Schlentner P, Viereck LA, Dyrness CT (1983) Productivity and nutrient cycling in taiga forest ecosystems. Can J For Res 13:747–766CrossRefGoogle Scholar
  14. 14.
    Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106:395–109CrossRefGoogle Scholar
  15. 15.
    Michelsen A, Rinnan R, Jonasson S (2012) Two decades of experimental manipulations of heaths and forest understory in the subarctic. AMBIO 41. Suppl 3:218–230Google Scholar
  16. 16.
    Kurina LM, Vitousek PM (2001) Nitrogen fixation rates of Stereocaulon vulcani on young Hawaiian lava flows. Biogeochem 55:179–194CrossRefGoogle Scholar
  17. 17.
    Zackrisson O, DeLuca TH, Nilsson MC et al (2004) Nitrogen fixation increases with successional age in boreal forests. Ecology 85:3327–3334CrossRefGoogle Scholar
  18. 18.
    Gavazov KS, Soudzilovskaia NA, van Logtestijn RSP, Braster M, Cornelissen JHC (2010) Isotopic analysis of cyanobacterial nitrogen fixation associated with subarctic lichen and bryophyte species. Plant Soil 333:507–517CrossRefGoogle Scholar
  19. 19.
    Steinberg NA, Meeks JC (1991) Photosynthetic CO2 fixation and ribulose bisphosphate carboxylase/oxygenase activity of Nostoc sp. strain UCD (7801) in symbiotic association with Anthoceros punctatus. J Bacteriol 171:6227–6233Google Scholar
  20. 20.
    Zielke M, Solheim B, Spjelkavik S, Olsen RA (2005) Nitrogen fixation in the high arctic: role of vegetation and environmental conditions. Arct Antarct Alp Res 37:372–378CrossRefGoogle Scholar
  21. 21.
    Bay G, Nahar N, Oubre M, Whitehouse MJ, Wardle DA, Zackrisson O, Nilsson MC, Rasmussen U (2013) Boreal feather mosses secrete chemical signals to gain nitrogen. New Phytol 200:54–60CrossRefPubMedGoogle Scholar
  22. 22.
    Belnap J (2002) Nitrogen fixation in biological soil cursts from southeast Utah, USA. Biol Fertil Soils 35:128–135CrossRefGoogle Scholar
  23. 23.
    Simpson FB, Burris RH (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095–97CrossRefPubMedGoogle Scholar
  24. 24.
    Hill S (1992) Physiology of nitrogen fixation in free-living heterotrophs. In: Stacey G, Burris RH, Evans J (eds) Biological Nitrogen Fixation. Chapman and Hall, New York, pp 87–129Google Scholar
  25. 25.
    Coxson DS, Kershaw KA (1983) Rehydration response of nitrogenase activity and carbon fixation in terrestrial Nostoc commune from Stipa-Bouteloua grassland. Can J Bot 61:2658–2668CrossRefGoogle Scholar
  26. 26.
    DeLuca TH, Zackrisson O (2007) Enhanced soil fertility under Juniperus communis in arctic ecosystems. Plant Soil 294:147–155CrossRefGoogle Scholar
  27. 27.
    Schöllhorn R, Burris RH (1967) Acetylene as a competitive inhibitor of N2 fixation. Proc Natl Acad Sci 58:213–216CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Sorensen PL, Michelsen A (2011) Long-term warming and litter addition affects nitrogen fixation in a subarctic heath. Glob Change Biol 17:528–537CrossRefGoogle Scholar
  29. 29.
    Sorensen PL, Jonasson S, Michelsen A (2006) Nitrogen fixation, denitrification, and ecosystem nitrogen pools in relation to vegetation development in the subarctic. Arct Antarct Alp Res 38:263–272CrossRefGoogle Scholar
  30. 30.
    Lange OL, Belnap J, Reichenberger H (1998) Photosynthesis of the cyanobacterial soil-crust lichen Collema tenax from arid lands in southern Utah, USA: responses of CO2 exchange. Funct Ecol 12:195–202CrossRefGoogle Scholar
  31. 31.
    Hair JF Jr, Anderson RE, Tatham RL, Back WC (1995) Multivariate data analysis. Macmillan, New YorkGoogle Scholar
  32. 32.
    Karagatzides JD, Lewis MC, Schulman HM (1985) Nitrogen fixation in the high arctic tundra at Scarpa Lake, northwest territories. Can J Bot 63:974–979Google Scholar
  33. 33.
    Gundale MJ, Gustafsson H, Nilsson MC (2009) The sensitivity of nitrogen fixation by a feather moss–cyanobacteria association to litter and moisture variability in young and old boreal forest. Can J For Res 39:2542–2549CrossRefGoogle Scholar
  34. 34.
    Jackson BG, Martin P, Nilsson MC, Wardle DA (2011) Response of feather moss associated N2 fixation and litter decomposition to variations in simulated rainfall intensity and frequency. Oikos 120:570–581CrossRefGoogle Scholar
  35. 35.
    Larmola T, Tuittila ES, Tiirola M, Nykänen H, Martikainen PJ, Yrjälä K et al (2010) The role of Sphagnum mosses in the methane cycling of a boreal mire. Ecology 91:2356–2365CrossRefPubMedGoogle Scholar
  36. 36.
    Larmola T, Leppänen SM, Tuittila ES, Aarva M, Merilä P, Fritze H et al (2014) Methanotrophy induces nitrogen fixation during peatland development. PNAS 2:734–739CrossRefGoogle Scholar
  37. 37.
    Basiliko N, Knowles R, Moore TR (2004) Roles of moss species and habitat in methane consumption potential in a northern peatland. Wetlands 24:178–185CrossRefGoogle Scholar
  38. 38.
    Yeager CM, Kuske CR, Carnery TD, Johnson SL, Ticknor LO, Belnap J (2012) Response of biological soil crust diazotrophs to season, altered summer precipitation, and year-round increased temperature in an arid grassland of the Colorado Plateau, USA. Front Microbiol. doi:10.3389/fmicb.2012.00358 PubMedCentralPubMedGoogle Scholar
  39. 39.
    Rousk K, Jones DL, DeLuca TH (2014) The resilience of nitrogen fixation in feather moss (Pleurozium schreberi)-cyanobacteria associations after a drying and rewetting cycle. Plant Soil 377:159–167CrossRefGoogle Scholar
  40. 40.
    Oliver MJ, Bewley JD (1984) Plant desiccation and protein synthesis. IV. RNA synthesis, stability, and recruitment of RNA into protein synthesis during desiccation and rehydration of the desiccation-tolerant moss, Tortula ruralis. Plant Physiol 74:21–25CrossRefPubMedCentralPubMedGoogle Scholar
  41. 41.
    Stewart KJ, Coxson D, Grogan P (2011) Nitrogen inputs by associative cyanobacteria across a low arctic tundra landscape. Arct Antarct Alp Res 43:267–278CrossRefGoogle Scholar
  42. 42.
    Gundale MJ, Nilsson M, Bansal S, Jäderlund A (2012) The interactive effects of temperature and light on biological nitrogen fixation in boreal forests. New Phytol 194:454–463CrossRefGoogle Scholar
  43. 43.
    Gundale MJ, Wardle DA, Nilsson MC (2012) The effect of altered macro-climate on N-fixation by boreal feather mosses. Biol Letters 8:805–808CrossRefGoogle Scholar
  44. 44.
    Zielke M, Ekker AS, Olsen RA, Spjelkavik S, Solheim B (2002) The influence of abiotic factors on biological nitrogen fixation in different types of vegetation in the high arctic, Svalbard. Arct Antarct Alp Res 34:293–299CrossRefGoogle Scholar
  45. 45.
    Lett S, Michelsen A (2014) Seasonal variation in nitrogen fixation and effects of climate change in a subarctic heath. Plant Soil 379:193–204CrossRefGoogle Scholar
  46. 46.
    Pugnaire FI, Luque MT (2001) Changes in plant interactions along a gradient of environmental stress. Oikos 93:42–49CrossRefGoogle Scholar
  47. 47.
    Olsen SL, Sandvik SM, Totland Ø (2013) Influence of two N-fixing legumes on plant community properties and soil nutrient levels in Alpine ecosystem. Arct Antarct Alp Res 45:363–371CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Kathrin Rousk
    • 1
    • 2
  • Pernille L. Sorensen
    • 1
  • Signe Lett
    • 3
  • Anders Michelsen
    • 1
    • 2
  1. 1.Department of Biology, Terrestrial Ecology SectionUniversity of CopenhagenCopenhagenDenmark
  2. 2.Center for Permafrost (CENPERM)University of CopenhagenCopenhagenDenmark
  3. 3.Climate Impacts Research Centre, Department of Ecology and Environmental ScienceUmeå UniversityAbiskoSweden

Personalised recommendations