Skip to main content

Advertisement

Log in

Soil microorganisms respond to five years of climate change manipulations and elevated atmospheric CO2 in a temperate heath ecosystem

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Soil microbial responses to global change can affect organic matter turnover and nutrient cycling thereby altering the overall ecosystem functioning. In a large-scale experiment, we investigated the impact of 5 years of climate change and elevated atmospheric CO2 on soil microorganisms and nutrient availability in a temperate heathland.

Methods

The future climate was simulated by increased soil temperature (+0.3 °C), extended pre-summer drought (excluding 5–8 % of the annual precipitation) and elevated CO2 (+130 ppm) in a factorial design. Soil organic matter and nutrient pools were analysed and linked to microbial measures by quantitative PCR of bacteria and fungi, chloroform fumigation extraction, and substrate-induced respiration to assess their impact of climate change on nutrient availability.

Results

Warming resulted in higher measures of fungi and bacteria, of microbial biomass and of microbial growth potential, however, this did not reduce the availability of nitrogen or phosphorus in the soil. Elevated CO2 did not directly affect the microbial measures or nutrient pools, whereas drought shifted the microbial community towards a higher fungal dominance.

Conclusions

Although we were not able to show strong interactive effects of the global change factors, warming and drought changed both nutrient availability and microbial community composition in the heathland soil, which could alter the ecosystem carbon and nutrient flow in the long-term.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372

    Article  PubMed  Google Scholar 

  • Albert KR, Mikkelsen TN, Michelsen A, Ro-Poulsen H, Van Der Linden L (2011a) Interactive effects of drought, elevated CO2 and warming on photosynthetic capacity and photosystem performance in temperate heath plants. J Plant Physiol 168:1550–1561

    Article  CAS  PubMed  Google Scholar 

  • Albert KR, Ro-Poulsen H, Mikkelsen TN, Michelsen A, Van Der Linden L, Beier C (2011b) Interactive effects of elevated CO2, warming, and drought on photosynthesis of deschampsia flexuosa in a temperate heath ecosystem. J Exp Bot 62:4253–4266

    Article  CAS  PubMed  Google Scholar 

  • Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Chang Biol 14:2898–2909

    Article  Google Scholar 

  • Andresen LC, Michelsen A, Jonasson S, Beier C, Ambus P (2009) Glycine uptake in heath plants and soil microbes responds to elevated temperature, CO2 and drought. Acta Oecol-Int J Ecol 35:786–796

    Article  Google Scholar 

  • Andresen LC, Michelsen A, Ambus P, Beier C (2010a) Belowground heathland responses after 2 years of combined warming, elevated CO2 and summer drought. Biogeochemistry 101:27–42

    Article  Google Scholar 

  • Andresen LC, Michelsen A, Jonasson S, Schmidt IK, Mikkelsen TN, Ambus P, Beier C (2010b) Plant nutrient mobilization in temperate heathland responds to elevated CO2, temperature and drought. Plant Soil 328:381–396

    Article  CAS  Google Scholar 

  • Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235

    Article  PubMed  Google Scholar 

  • Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641

    Article  PubMed  Google Scholar 

  • Bardgett RD, Manning P, Morrien E, De Vries FT (2013) Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle. J Ecol 101:334–343

    Article  Google Scholar 

  • Blagodatskaya E, Blagodatsky S, Dorodnikov M, Kuzyakov Y (2010) Elevated atmospheric CO2 increases microbial growth rates in soil: results of three CO2 enrichment experiments. Glob Chang Biol 16:836–848

    Article  Google Scholar 

  • Blankinship J, Niklaus P, Hungate B (2011) A meta-analysis of responses of soil biota to global change. Oecologia 165:553–565

    Article  PubMed  Google Scholar 

  • Borken W, Savage K, Davidson EA, Trumbore SE (2006) Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Glob Chang Biol 12:177–193

    Article  Google Scholar 

  • Butterly CR, McNeill AM, Baldock JA, Marschner P (2011) Rapid changes in carbon and phosphorus after rewetting of dry soil. Biol Fertil Soils 47:41–50

    Article  CAS  Google Scholar 

  • Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci U S A 104:4990–4995

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Christensen J, Christensen O (2007) A summary of the prudence model projections of changes in european climate by the end of this century. Clim Chang 81:7–30

    Article  Google Scholar 

  • Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533

    Article  CAS  PubMed  Google Scholar 

  • Darby BJ, Neher DA, Housman DC, Belnap J (2011) Few apparent short-term effects of elevated soil temperature and increased frequency of summer precipitation on the abundance and taxonomic diversity of desert soil micro- and meso-fauna. Soil Biol Biochem 43:1474–1481

    Article  CAS  Google Scholar 

  • De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  PubMed  Google Scholar 

  • de Graaff M, Schadt CW, Rula K, Six J, Schweitzer JA, Classen AT (2011) Elevated CO2 and plant species diversity interact to slow root decomposition. Soil Biol Biochem 43:2347–2354

    Article  Google Scholar 

  • Drigo B, Kowalchuk GA, Van Veen JA (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679

    Article  Google Scholar 

  • Drigo B, Pijl AS, Duyts H, Kielak A, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, van Veen JA, Kowalchuk GA (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci U S A 107:10938–10942

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB (2012) Global change below ground: Impacts of elevated CO2, nitrogen and summer drought on soil food webs and biodiversity. Glob Chang Biol 18:435–447

    Article  Google Scholar 

  • Emmett BA, Beier C, Estiarte M, Tietema A, Kristensen HL, Williams D, Penuelas J, Schmidt IK, Sowerby A (2004) The response of soil processes to climate change: results from manipulation studies of shrublands across an environmental gradient. Ecosystems 7:625–637

    Article  Google Scholar 

  • Fagúndez J (2013) Heathlands confronting global change: drivers of biodiversity loss from past to future scenarios. Ann Bot 111:151–172

    Article  PubMed  Google Scholar 

  • Field CB, Chapin FS, Chiariello NR, Holland EA, Mooney HA (1996) The Jasper Ridge CO2 experiment: design and motivation. In: Koch GW, Mooney HA (eds) Carbon dioxide and terrestrial ecosystems. Academic, San Diego, pp 121–146

    Chapter  Google Scholar 

  • Fierer N, Allen AS, Schimel JP, Holden PA (2003) Controls on microbial CO2 production: a comparison of surface and subsurface soil horizons. Glob Chang Biol 9:1322–1332

    Article  Google Scholar 

  • Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative pcr assays. Appl Environ Microbiol 71:4117–4120

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frey SD, Elliott ET, Paustian K (1999) Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients. Soil Biol Biochem 31:573–585

    Article  CAS  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes–application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Halverson LJ, Jones TM, Firestone MK (2000) Release of intracellular solutes by four soil bacteria exposed to dilution stress. Soil Sci Soc Am J 64:1630–1637

    Article  CAS  Google Scholar 

  • Haugwitz MS, Michelsen A, Schmidt IK (2011) Long-term microbial control of nutrient availability and plant biomass in a subarctic-alpine heath after addition of carbon, fertilizer and fungicide. Soil Biol Biochem 43:179–187

    Article  CAS  Google Scholar 

  • Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB (2011) Fungal community responses to precipitation. Glob Chang Biol 17:1637–1645

    Article  Google Scholar 

  • He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, Van Nostrand JD, Hobbie SE, Reich PB, Zhou J (2010) Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett 13:564–575

    Article  PubMed  Google Scholar 

  • He Z, Piceno Y, Deng Y, Xu M, Lu Z, DeSantis T, Andersen G, Hobbie SE, Reich PB, Zhou J (2011) The phylogentic composition and structure of soil microbial communities shifts in response to elevated carbon dioxide. ISME J 1–14

  • Heil GW, Aerts R (1993) Synthesis: perspectives for heathlands. In: Heil GW, Aerts R (eds) Heathlands. Patterns and processes in a changing environment. Kluwer Academic Publishers, Dodrecht, pp 201–217

    Google Scholar 

  • Henry HAL, Cleland EE, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2, N deposition and climate change on plant litter quality in a California annual grassland. Oecologia 142:465–473

    Article  PubMed  Google Scholar 

  • Holland EA, Coleman DC (1987) Litter placement effects on microbial and organic-matter dynamics in an agroecosystem. Ecology 68:425–433

    Article  Google Scholar 

  • IPCC (2007) In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group i to the fourth assessment report of the intergovernmental panel on climate change. Cambridge, United Kingdom, p 996

    Google Scholar 

  • Jackson RB, Fierer N, Schimel JP (2007) New directions in microbial ecology. Ecology 88:1343–1344

    Article  Google Scholar 

  • Jensen KD, Beier C, Michelsen A, Emmett BA (2003) Effects of experimental drought on microbial processes in two temperate heathlands at contrasting water conditions. Appl Soil Ecol 24:165–176

    Article  Google Scholar 

  • Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the k(ec) value. Soil Biol Biochem 28:25–31

    Article  CAS  Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK, Nielsen EV, Callaghan TV (1996a) Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: implications for plant nutrient uptake. Oecologia 106:507–515

    Article  Google Scholar 

  • Jonasson S, Vestergaard P, Jensen M, Michelsen A (1996b) Effects of carbohydrate amendments on nutrient partitioning, plant and microbial performance of a grassland-shrub ecosystem. Oikos 75:220–226

    Article  Google Scholar 

  • Jonasson S, Castro J, Michelsen A (2006) Interactions between plants, litter and microbes in cycling of nitrogen and phosphorus in the arctic. Soil Biol Biochem 38:526–532

    Article  CAS  Google Scholar 

  • Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33

    Article  CAS  Google Scholar 

  • Kandeler E, Tscherko D, Bardgett RD, Hobbs PJ, Kampichler C, Jones TH (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem. Plant Soil 202:251–262

    Article  CAS  Google Scholar 

  • Kandeler E, Mosier AR, Morgan JA, Milchunas DG, King JY, Rudolph S, Tscherko D (2008) Transient elevation of carbon dioxide modifies the microbial community composition in a semi-arid grassland. Soil Biol Biochem 40:162–171

    Article  CAS  Google Scholar 

  • Kardol P, Cregger MA, Campany CE, Classen AT (2010) Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91:767–781

    Article  PubMed  Google Scholar 

  • Kardol P, Reynolds WN, Norby RJ, Classen AT (2011) Climate change effects on soil microarthropod abundance and community structure. Appl Soil Ecol 47:37–44

    Article  Google Scholar 

  • Khalvati MA, Hu Y, Mozafar A, Schmidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–712

    Article  CAS  PubMed  Google Scholar 

  • Kongstad J, Schmidt IK, Riis-Nielsen T, Arndal MF, Mikkelsen TN, Beier C (2012) High resilience in heathland plant to changes in temperature, drought and CO2 in combination: results from the CLIMAITE experiment. Ecosystems 15:269–283

    Article  CAS  Google Scholar 

  • Kristensen HL (2001) High immobilization of NH4+ in Danish heath soil related to succession, soil and nutrients: implications for critical loads of N. Water Air Soil Pollut Focus 1:211–230

    Article  CAS  Google Scholar 

  • Langley JA, Megonigal JP (2010) Ecosystem responses to elevated CO2 levels by limited by nitrogen-induced plant species shift. Nature 466:96–99

    Article  CAS  PubMed  Google Scholar 

  • Larsen KS, Andresen LC, Beier C et al (2011) Reduced N cycling in response to elevated CO2, warming, and drought in a danish heathland: synthesizing results of the climaite project after two years of treatments. Glob Chang Biol 17:1884–1899

    Article  Google Scholar 

  • Luo Y, Su BO, Currie WS et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience 54:731–739

    Article  Google Scholar 

  • Manter DK, Vivanco JM (2007) Use of the its primers, its1f and its4, to characterize fungal abundance and diversity in mixed-template samples by qpcr and length heterogeneity analysis. J Microbiol Methods 71:7–14

    Article  CAS  PubMed  Google Scholar 

  • Mcgill WB, Hunt HW, Woodmansee RG, Reuss JO (1981) Phoenix, a model of the dynamics of carbon and nitrogen in grassland soils. In: Clark FE, Rosswall T (eds) Terrestrial nitrogen cycles. Ecological Bulletins, Stockholm, pp 49–115

    Google Scholar 

  • Melillo JM, Butler S, Johnson J et al (2011) Soil warming, carbon–nitrogen interactions, and forest carbon budgets. PNAS 108:9508–9512

    Article  CAS  PubMed  Google Scholar 

  • Michelsen A, Graglia E, Schmidt IK, Jonasson S, Sleep D, Quarmby C (1999) Differential responses of grass and a dwarf shrub to long-term changes in soil microbial biomass C, N and P following factorial addition of NPK fertilizer, fungicide and labile carbon to a heath. New Phytol 143:523–538

    Article  Google Scholar 

  • Mikkelsen TN, Beier C, Jonasson S et al (2008) Technical report. Experimental design of multifactor climate change experiments with elevated CO2, warming and drought: the climaite project. Funct Ecol 22:185–195

    Google Scholar 

  • Nielsen PL, Andresen LC, Michelsen A, Schmidt IK, Kongstad J (2009) Seasonal variations and effects of nutrient applications on N and P and microbial biomass under two temperate heathland plants. Appl Soil Ecol 42:279–287

    Article  Google Scholar 

  • Park JW, Crowley DE (2005) Normalization of soil DNA extraction for accurate quantification real-time pcr and of target genes by DGGE. Biotechniques 38:579–586

    Article  CAS  PubMed  Google Scholar 

  • Parton W, Morgan J, Smith D et al (2012) Impact of precipitation dynamics on net ecosystem productivity. Glob Chang Biol 18:915–927

    Article  Google Scholar 

  • Penuelas P, Prieto P, Beier C et al (2007) Responses of shrubland species richness and primary productivity to six-years experimental warming and drought in a North–south European gradient. Glob Chang Biol 13:2563–2581

    Article  Google Scholar 

  • Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562

    Article  Google Scholar 

  • Sardans J, Penuelas J, Estiarte M (2008) Changes in soil enzymes related to C and N cycle and in soil C and N content under prolonged warming and drought in a mediterranean shrubland. Appl Soil Ecol 39:223–235

    Article  Google Scholar 

  • Scheu S (1993) Analysis of the microbial nutrient status in soil microcompartments: earthworm faeces from a basalt–limestone gradient. Geoderma 56:575–586

    Article  CAS  Google Scholar 

  • Schimel J (2004) Playing scales in the methane cycle: from microbial ecology to the globe. Proc Natl Acad Sci U S A 101:12400–12401

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implictions for ecosystem function. Ecology 88:1386–1394

    Article  PubMed  Google Scholar 

  • Schmidt IK, Tietema A, Williams D, Gundersen P, Beier C, Emmett BA, Estiarte M (2004) Soil solution chemistry and element fluxes in three european heathlands and their responses to warming and drought. Ecosystems 7:638–649

    Article  CAS  Google Scholar 

  • Selsted M, van der Linden L, Ibrom A, Michelsen A, Larsen KS, Pedersen JK, Mikkelsen TN, Pilegaard K, Beier C, Ambus P (2012) Soil respiration is stimulated by elevated CO2 and reduced by summer drought: three years of measurements in a multifactor ecosystem manipulation experiment in a temperate heathland (CLIMAITE). Glob Chang Biol 18:1216–1230

    Article  Google Scholar 

  • Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB (2002) Grassland responses to global environmental changes supressed by elevated CO2. Science 298:1987–1990

    Article  CAS  PubMed  Google Scholar 

  • Sowerby A, Emmett B, Beier C, Tietema A, Penuelas J, Estiarte M, Van Meeteren MJM, Hughes S, Freeman C (2005) Microbial community changes in heathland soil communities along a geographical gradient: interaction with climate change manipulations. Soil Biol Biochem 37:1805–1813

    Article  CAS  Google Scholar 

  • Sowerby A, Emmett BA, Tietma A, Beier C (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils. Glob Chang Biol 14:2388–2404

    Article  Google Scholar 

  • Staddon PL, Thompson K, Jakobsen I, Grime JP, Askew AP, Fitter AH (2003) Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Glob Chang Biol 9:186–194

    Article  Google Scholar 

  • Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395

    Article  CAS  Google Scholar 

  • Suseela V, Conant RT, Wallenstein MD, Dukes JS (2012) Effects of soil moisture on temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob Chang Biol 18:336–348

    Article  Google Scholar 

  • Van Meeteren MJM, Tietema A, Westerveld JW (2007) Regulation of microbial carbon, nitrogen, and phosphorus transformations by temperature and moisture during decomposition of calluna vulgaris litter. Biol Fertil Soils 44:103–112

    Article  Google Scholar 

  • VanGuilder HD, Vrana KE, Freeman WM (2008) Twenty-five years of quantitative pcr for gene expression analysis. Biotechniques 44:619–626

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal rna genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCRprotocols—a guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

  • Yu Z, Mohn WW (1999) Killing two birds with one stone: simultanous extraction of DNA and RNA from activated sludge biomass. Can J Microbiol 45:269–272

    Article  CAS  Google Scholar 

  • Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob Chang Biol 11:266–277

    Article  CAS  Google Scholar 

  • Zogg GP, Zak DR, Ringelberg DB, White DC, MacDonald NW, Pregitzer KS (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61:475–481

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Esben V. Nielsen, Anette Hørdum Løth and Karin Vestberg are thanked for assistance with samples and analyses. The work was conducted as part of the CLIMAITE research center which is supported by the Villum Kann Rasmussen foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Merian Skouw Haugwitz.

Additional information

Responsible Editor: Hans Lambers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haugwitz, M.S., Bergmark, L., Priemé, A. et al. Soil microorganisms respond to five years of climate change manipulations and elevated atmospheric CO2 in a temperate heath ecosystem. Plant Soil 374, 211–222 (2014). https://doi.org/10.1007/s11104-013-1855-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1855-1

Keywords

Navigation