Abstract
General concern about climate change has led to growing interest in the responses of terrestrial ecosystems to elevated concentrations of CO2 in the atmosphere. Experimentation during the last two to three decades using a large variety of approaches has provided sufficient information to conclude that enrichment of atmospheric CO2 may have severe impact on terrestrial ecosystems. This impact is mainly due to the changes in the organic C dynamics as a result of the effects of elevated CO2 on the primary source of organic C in soil, i.e., plant photosynthesis. As the majority of life in soil is heterotrophic and dependent on the input of plant-derived organic C, the activity and functioning of soil organisms will greatly be influenced by changes in the atmospheric CO2 concentration. In this review, we examine the current state of the art with respect to effects of elevated atmospheric CO2 on soil microbial communities, with a focus on microbial community structure. On the basis of the existing information, we conclude that the main effects of elevated atmospheric CO2 on soil microbiota occur via plant metabolism and root secretion, especially in C3 plants, thereby directly affecting the mycorrhizal, bacterial, and fungal communities in the close vicinity of the root. There is little or no direct effect on the microbial community of the bulk soil. In particular, we have explored the impact of these changes on rhizosphere interactions and ecosystem processes, including food web interactions.
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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
Alberton O, Kuyper TW, Gorissen A (2007) Competition for nitrogen between Pinus sylvestris and ectomycorrhizal fungi generates potential for negative feedback under elevated CO2. Plant Soil 296:159–172
Allen MF, Klironomos JN, Treseder KK, Oechel WC (2005) Responses of soil biota to elevated CO2 in a chaparral ecosystem. Ecol Appl 15:1701–1711
Arnone JA III, Gordon JC (1990) Effect of nodulation, nitrogen fixation and CO2 enrichment on the physiology, growth and dry mass allocation of seedlings of Alnus rubra Bong. New Phytol 116:55–66
Berntson GM, Bazzaz FA (1997) Nitrogen cycling in microcosms of yellow birch exposed to elevated CO2: simultaneous positive and negative below-ground feedbacks. Glob Chang Biol 3:247–258
Billes G, Rouhier H, Bottner P (1993) Modifications of the carbon and nitrogen allocations in the plant (Triticum-Aestivum L) soil system in response to increased atmospheric CO2 concentration. Plant Soil 157:215–225
Bruce KD, Jones TH, Bezemer TM, Thompson LJ, Ritchie DA (2000) The effect of elevated atmospheric carbon dioxide levels on soil bacterial communities. Glob Chang Biol 6:427–434
Brussaard L, Behan-Pelletier VM, Bignell DE, Brown VK, Didden W, Folgarait P, Fragroso C, Freckman DW, Gupta V, Hattori T, Hawksworth DL, Klopatek C, Lavelle P, Malloch DW, Rusek J, Soderstrom B, Tiedje JM, Virginia RA (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570
Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Pro Natl Acad Sci U S A 104:4990–4995
Cheng WX, Johnson DW (1998) Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174
Cheng WX, Gershenson A (2007) Carbon fluxes in the rhizosphere. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere: an ecological perspective. Elsevier Academic Press, London, UK, pp 31–56
Cheng WX, Sims DA, Luo YQ, Coleman JS, Johnson DW (2000) Photosynthesis, respiration, and net primary production of sunflower stands in ambient and elevated atmospheric CO2 concentrations: an invariant NPP:GPP ratio? Glob Chang Biol 6:931–941
Chung HG, Zak DR, Lilleskov EA (2006) Fungal community composition and metabolism under elevated CO2 and O-3. Oecologia 147:143–154
Cotrufo MF, Gorissen A (1997) Elevated CO2 enhances below-ground C allocation in three perennial grass species at different levels of N availability. New Phytol 137:421–431
Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob Chang Biol 4:43–54
Coûteaux MM, Kurz C, Bottner P, Raschi A (1999) Influence of the increased atmospheric CO2 concentration on quality of plant material and litter decomposition. Tree Physiol 19:301–311
Curtis PS (1996) A meta-analysis of leaf gas exchange and nitrogen in trees grown under elevated carbon dioxide. Plant Cell Environ 19:127–137
Curtis PS, Wang XZ (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313
Curtis PS, Balduman LM, Drake BG, Whigham DF (1990) Elevated atmospheric CO2 effects on belowground processes in C-3 and C-4 estuarine marsh communities. Ecology 71:2001–2006
Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci U S A 99:10494–10499
Diaz S, Grime JP, Harris J, McPherson E (1993) Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364:616–617
Denef K, Bubenheim H, Lenhart K, Vermeulen J, Van Cleemput O, Boeckx P, Muller C (2007) Community shifts and carbon translocation within metabolically-active rhizosphere microorganisms in grasslands under elevated CO2. Biogeosciences 4:769–779
De Ruiter P, Moore J, Zwart K, Bouwman L, Hassink J, Bloem J, De Vos J, Marinissen J, Didden W, Lebbink G, Brussaard L (1993) Simulation of nitrogen mineralization in the belowground food webs of two winter-wheat fields. J. Appl Ecol 30:95–106
Drigo B, Kowalchuk GA, Yergeau E, Bezemer TM, Boschker HTS, Van Veen JA (2007) Impact of elevated carbon dioxide on the rhizosphere communities of Carex arenaria and Festuca rubra. Glob Chang Biol 13:2396–2410
Ebersberger D, Wermbter N, Niklaus P, Kandeler E (2004) Effects of long term CO2 enrichment on microbial community structure in calcareous grassland. Plant Soil 264:313–323
Elhottova D, Triska J, Santruckova H, Kveton J, Santrucek J, Simkova M (1997) Rhizosphere microflora of winter wheat plants cultivated under elevated CO2. Plant Soil 197:51–259
Fitter AH, Heinemeyer A, Staddon PL (2000) The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytol 147:179–187
Fitter AH, Heinemeyer A, Husband R, Olsen E, Ridgway KP, Staddon PL (2004) Global environmental change and the biology of arbuscular mycorrhizas: gaps and challenges. Can J Bot 82:1133–1139
Fransson PMA, Taylor AFS, Finlay RD (2001) Elevated atmospheric CO2 alters root symbiont community structure in forest trees. New Phytol 152:431–442
Fromin N, Tarnawski S, Roussel-Delif L, Hamelin J, Baggs EM, Aragno M (2005) Nitrogen fertiliser rate affects the frequency of nitrate-dissimilating Pseudomonas spp. in the rhizosphere of Lolium perenne grown under elevated pCO2 (Swiss FACE). Soil Biol Biochem 37:1962–1965
Gamper H, Peter M, Jansa J, Luscher A, Hartwig UA, Leuchtmann A (2004) Arbuscular mycorrhizal fungi benefit from 7 years of free air CO2 enrichment in well-fertilized grass and legume monocultures. Glob Chang Biol 10:189–199
Gamper H, Hartwig UA, Leuchtmann A (2005) Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure. New Phytol 167:531–542
Gebauer RLE, Strain BR, Reynolds JF (1997) The effect of elevated CO2 and N availability on tissue concentrations and whole plant pools of carbon-based secondary compounds in loblolly pine (Pinus taeda). Oecologia 113:29–36
Griffiths BS, Ritz K, Ebblewhite N, Paterson E (1998) Ryegrass rhizosphere microbial community structure under elevated C dioxide concentrations, with observations on wheat rhizosphere. Soil Biol Biochem 30:315–321
Hodge A (1996) Impact of elevated CO2 on mycorrhizal associations and implications for plant growth. Biol Fertil Soils 23:388–398
Hodge A, Paterson E, Grayston SJ, Campbell CD, Ord BG, Killham K (1998) Characterisation and microbial utilization of exudate material from the rhizosphere of Lolium perenne grown under CO2 enrichment. Soil Biol Biochem 30:1033
Hoeksema JD, Lussenhop J, Teeri JA (2000) Soil nematodes indicate food web responses to elevated atmospheric CO2. Pedobiologia 44:725–735
Hu S, Chapin FS, Firestone MK, Field CB, Chiariello NR (2001) Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409:188–191
Hu SJ, Firestone MK, Chapin FS (1999) Soil microbial feedbacks to atmospheric CO2 enrichment. TREE 14:433–437
Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774
Hughes JB, Bohannan BJM (2004) Application of ecological diversity statistics in microbial ecology. In: Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans AD, van Elsas JD (eds) Molecular microbial ecology manual, 2nd edition. Kluwer, Dordrecht, The Netherlands, pp 1321–1344
Hungate BA, Holland EA, Jackson RB, Chapin FS, Mooney HA, Field CB (1997) The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388:576–579
Hungate BA, Jaeger CH, Gamara G, Chapin FS, Field CB (2000) Soil microbiota in two annual grasslands: responses to elevated atmospheric CO2. Oecologia 124:589–598
Hungate BA, Dukes JS, Shaw MR, Luo Y, Field CB (2003) Atmospheric science: nitrogen and climate change. Science 302:1512–1513
Insam H, Baath E, Berreck M, Frostegard A, Gerzabek MH, Kraft A, Schinner F, Schweiger P, Tschuggnall G (1999) Responses of the soil microbiota to elevated CO2 in an artificial tropical ecosystem. J. Microbiol Methods 36:45
IPCC Climate Change (2007) Synthesis Report. Summary for Policymakers. http://www.ipcc.ch. November 2007
Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci U S A 94:362–7366
Janus L, Angeloni N, McCormack J, Rier S, Tuchman N, Kelly J (2005) Elevated atmospheric CO2 alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots. Microb Ecol 50:102–109
Johnson NC, Gehring CA (2007) Mycorrhizas: symbiotic mediators of rhizosphere and ecosystem processes. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere: an ecological perspective. Elsevier Academic Press, London, UK, pp 31–56
Johnson NC, Wolf J, Koch GW (2003) Interactions among mycorrhizae, atmospheric CO2 and soil N impact plant community composition. Ecol Lett 6:532–540
Jones TH, Thompson TJ, Lawton JH, Bezemer TM, Bardgett RD, Blackburn TM, Bruce KD, Cannon PF, Hall GS, Hartley SE, Howson G, Jones CG, Kampichler C, Kandeler E, Ritchie DA (1998) Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems. Science 280:441–443
Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480
Jongen M, Jones MB, Hebeisen T, Blum H, Hendrey G (1995) The effects of elevated CO2 concentrations on the root growth of Lolium perenne and Trifolium repens grown in a FACE* system. Glob Chang Biol 1:361–371
Jossi M, Fromin N, Tarnawski S, Kohler F, Gillet F, Aragno M, Hamelin J (2006) How elevated pCO2 modifies total and metabolically active bacterial communities in the rhizosphere of two perennial grasses grown under field conditions. FEMS Microbiol Ecol 55:339–350
Kandeler E, Tscherko D, Bardgert 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
Klamer M, Roberts MS, Levine LH, Drake BG, Garland JL (2002) Influence of elevated CO2 on the fungal community in a coastal scrub oak forest soil investigated with terminal-restriction fragment length polymorphism analysis. Appl Environ Microbiol 68:4370–4376
Klironomos JN, Rillig MC, Allen MF (1996) Below-ground microbial and microfaunal responses to Artemisia tridentata grown under elevated atmospheric CO2. Funct Ecol 10:527–534
Klironomos JN, Rillig MC, Allen MF, Zak DR, Kubiske M, Pregitzer KS (1997) Soil fungal-arthropod responses to Populus tremuloides grown under enriched atmospheric CO2 under field conditions. Glob Chang Biol 3:473–478
Klironomos JN, Allen M, Rillig MC, Piotrowski J, Makvandi-Nejad S, Wolfe BE, Powell JR (2005) Abrupt rise in atmospheric CO2 overestimates community response in a model plant–soil system. Nature 433:621–624
King JS, Thomas RB, Strain BR (1997) Morphology and tissue quality of seedling root systems of Pinus taeda and Pinus ponderosa as affected by varying CO2, temperature, and nitrogen. Plant Soil 195:107–119
King JS, Hanson PJ, Bernhardt E, DeAngelis P, Norby RJ, Pregitzer KS (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Glob Chang Biol 10:1027–1042
Körner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl 10:1590–1619
Körner C, Arnone JA (1992) Responses to elevated carbon-dioxide in artificial tropical ecosystems. Science 257:1672–1675
Kreuzer-Martin HW (2007) Stable isotope probing: linking functional activity to specific members of microbial communities. Soil Sci Soc Am J 71:611–619
Kuikman PJ, Lekkerkerk LJA, Van Veen JA (1991) Carbon dynamics of a soil planted with wheat under elevated CO2 concentration. In: Wilson WS (ed) Advances in soil organic matter research: the impact on agriculture and the environment, vol Special Publication 90. The Royal Society of Chemistry, Cambridge, UK, pp 267–274
Lekkerkerk LJA, Van de Geijn SC, Van Veen JA (1990) Effects of elevated atmospheric CO2-levels on the carbon economy of a soil planted with wheat. In: Bowman AF (ed) Soils and the greenhouse effect. Wiley, Chichester, pp 423–429
Lipson DA, Wilson RF, Oechel WC (2005) Effects of elevated atmospheric CO2 on soil microbial biomass, activity, and diversity in a chaparral ecosystem. Appl Environ Microbiol 71:8573–8580
Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628
Luo Y, Su B, Currie W, Dukes J, Finzi A, Hartwig U, Hungate B, McMurtrie R, Oren R, Parton W, Pataki D, Shaw M, Zak D, Field C (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739
Lussenhop J, Treonis A, Curtis PS, Teeri JA, Vogel CS (1998) Response of soil biota to elevated atmospheric CO2 in poplar model systems. Oecologia 113:247–251
Marilley L, Hartwig UA, Aragno M (1999) Influence of an elevated atmospheric CO2 content on soil and rhizosphere bacterial communities beneath Lolium perenne and Trifolium repens under field conditions. Microb Ecol 38:39–49
Mayr C, Miller M, Insam H (1999) Elevated CO2 alters community-level physiological profiles and enzyme activities in alpine grassland. J Microbiol Methods 36:35–43
Montealegre CM, Van Kessel C, Blumenthal JM, Hur H-G, Hartwig UA, Sadowsky MJ (2000) Elevated atmospheric CO2 alters microbial population structure in a pasture ecosystem. Glob Chang Biol 6:475–482
Moore JC, Hunt HW (1998) Resource compartmentation and the stability of real ecosystems. Nature 333:261–263
Niklaus PA, Glockler E, Siegwolf R, Korner C (2001) Carbon allocation in calcareous grassland under elevated CO2: a combined 13C-pulse-labelling/soil physical fractionation study. Funct Ecol 15:43–50
Niklaus PA, Alphei J, Ebersberger D, Kamphikler C, Kandler E, Tscherko D (2003) Six years of in situ CO2 enrichment evoke changes in soil structure and soil biota of nutrient-poor grassland. Glob Chang Biol 9:585–600
Neher DA, Weicht TR, Moorhead DL, Sinsabaugh RL (2004) Elevated CO2 alters functional attributes of nematode communities in forest soils. Funct Ecol 18:584–591
Norby RJ (1994) Issues and perspectives for investigating root responses to elevated atmospheric carbon-dioxide. Plant Soil 165:9–20
Olsrud M, Melillo JM, Christensen TR, Michelsen A, Wallander H, Olsson PA (2004) Response of ericoid mycorrhizal colonization and functioning to global change factors. New Phytol 162:459–469
Owen AG, Jones D (2001) Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem 33:651–657
Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740
Parrent JL, Morris WF, Vilgalys R (2006) CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87:2278–2287
Paterson E, Rattray EAS, Killham K (1996) Effect of elevated atmospheric CO2 concentration on C-partitioning and rhizosphere C-flow for three plant species. Soil Biol. Biochem 28:195–201
Paterson E, Hall JM, Rattray EAS, Griffiths BS, Ritz K, Killham K (1997) Effect of elevated CO2 on rhizosphere carbon flow and soil microbial processes. Glob Chang Biol 3:363–377
Pendall E, Bridgham S, Hanson PJ, Hungate B, Kicklighter DW, Johnson DW, Law BE, Luo Y, Megonigal JP, Olsrud M, Ryan MG, Wan S (2004) Below-ground process responses to elevated CO2 and temperature: a discussion of observations, measurement methods, and models. New Phytol 162:311–322
Phillips RP (2007) Towards a rhizo-centric view of plant-microbial feedbacks under elevated atmospheric CO2. New Phytol 173:664–667
Phillips RL, Zak DR, Holmes WE, White DC (2002) Microbial community composition and function beneath temperate trees exposed to elevated atmospheric carbon dioxide and ozone. Oecologia 131:236–244
Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894
Philips DA, Fox TC, Six J (2006a) Root exudation (net efflux of amino acids) may increase rhizodeposition under elevated CO2. Glob Chang Biol 12:561–567
Phillips DA, Fox TC, Ferris H, Moore JC (2006b) The influence of elevated CO2 on diversity, activity and biogeochemical function of rhizosphere and soil bacterial communities. In: Nösberger J, Long SP, Norby RJ et al (eds) Managed ecosystems and CO2—case studies, processes and perspectives. Ecological studies serie, vol 187. Springer, Berlin, pp 413–428
Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR (1998) Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiol 18:665–670
Pregitzer KS, Zak DR, Maziasz J, DeForest J, Curtis PS, Lussenhop J (2000) Interactive effects of atmospheric CO2 and soil-N availability on fine roots of Populus tremuloides. Ecol Appl 10:18–33
Pregitzer KS, Zak DR, Loya WM, Karberg NJ, King JS, Burton AJ (2007) The contribution of root – Rhizosphere biochemical cycles in changing world. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere: an ecological perspective. Elsevier Academic Press, London, UK, pp 155–178
Radajewski S, Ineson P, Parekh NR, Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403:646–649
Randlett DL, Zak DR, Pregitzer KS et al (1996) Elevated atmospheric carbon dioxide and leaf litter chemistry: Influences on microbial respiration and net nitrogen mineralization. Soil Sci Soc Am J 60:1571–1577
Richter M, Hartwig UA, Frossard E, Nosberger J, Cadisch G (2003) Gross fluxes of nitrogen in grassland soil exposed to elevated atmospheric pCO2 for seven years. Soil Biol Biochem 35:1325–1335
Rillig MC, Allen MF (1999) What is the role of arbuscular mycorrhizal fungi in plant-to-ecosystem responses to elevated atmospheric CO2? Mycorrhiza 9:1–8
Rillig MC, Field CB (2003) Arbuscular mycorrhizae respond to plants exposed to elevated atmospheric CO2 as a function of soil depth. Plant Soil 254:383–391
Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53
Rillig MC, Scow KM, Klironomos JN, Allen MF (1997) Microbial carbon-substrate utilization in the rhizosphere of Gutierrezia sarothrae grown in elevated atmospheric carbon dioxide. Soil Biol Biochem 29:1387–1394
Rillig MC, Allen MF, Klironomos JN, Chiariello NR, Field CB (1998) Plant species-specific changes in root-inhabiting fungi in a California annual grassland: responses to elevated CO2 and nutrients. Oecologia 113:252–259
Rillig MC, Wright SF, Kimball BA, Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field: a possible role for arbuscular mycorrhizal fungi. Glob Chang Biol 7:333–337
Rillig MC, Wright SF, Shaw MR, Field CB (2002) Artificial climate warming positively affects arbuscular mycorrhizae but decreases soil aggregate water stability in an annual grassland. Oikos 97:52–58
Rogers HH, Runion GB, Krupa SV (1994) Plant-responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environ Pollut 83:155–189
Ronn R, Gavito M, Larsen J, Jakobsen I, Frederiksen H, Christensen S (2002) Response of free-living soil protozoa and microorganisms to elevated atmospheric CO2 and presence of mycorrhiza. Soil Biol Biochem 34:923–932
Ronn R, Ekelund F, Christensen S (2003) Effects of elevated atmospheric CO2 on protozoan abundance in soil planted with wheat and on decomposition of wheat roots. Plant Soil 251:13–21
Sadowsky MJ, Schortemeyer M (1997) Soil microbial responses to increased concentrations of atmospheric CO2. Glob Chang Biol 3:217–224
Sanders IR, Streitwolf-Engel R, van der Heijden MGA, Boller T, Wiemken A (1998) Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO2 enrichment. Oecologia 117:496–503
Schimel D, Melillo J, Tian H, McGuire AD, Kicklighter D, Kittel T, Rosenbloom N, Running S, Thornton P, Ojima D, Parton W, Kelly R, Sykes M, Neilson R Rizzo B (2000) Contribution of increasing CO2 and climate to carbon storage by ecosystems in the United States. Science 287:2004–2006
Schortemeyer M, Hartwig UA, Hendrey GR, Sadowsky MJ (1996) Microbial community changes in the rhizospheres of white clover and perennial ryegrass exposed to free air carbon dioxide enrichment (FACE). Soil Biol Biochem 28:1717–1724
Sonnemann I, Wolters V (2005) The microfood web of grassland soils responds to a moderate increase in atmospheric CO2. Glob Chang Biol 11:1148–1155
Soussana JF, Hartwig UA (1996) The effects of elevated CO2 on symbiotic N2 fixation: a link between the carbon and nitrogen cycles in grassland ecosystems. Plant Soil 187:321–332
Sowerby A, Blum H, Gray TRG, Ball AS (2000) The decomposition of Lolium perenne in soils exposed to elevated CO2: comparisons of mass loss of litter with soil respiration and soil microbial biomass. Soil Biol Biochem 32:1359
Staddon PL (2005) Mycorrhizal fungi and environmental change: the need for a mycocentric approach. New Phytol 167:635–637
Staddon PL, Fitter AH, Graves JD (1999) Effect of elevated atmospheric CO2 on mycorrhizal colonization, external mycorrhizal hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal fungus Glomus mosseae. Glob Chang Biol 5:347–358
Staddon PL, Heinemeyer A, Fitter AH (2002) Mycorrhizas and global environmental change: research at different scales. Plant Soil 244:253–261
Tarnawski S, Aragno M (2006) The influence of elevated CO2 on diversity, activity and biogeochemical function of rhizosphere and soil bacterial communities. In: Nösberger J, Long SP, Norby RJ et al (eds) Managed ecosystems and CO2-case studies, processes and perspectives. Ecological studies serie, vol 187. Springer, Berlin, pp 393–409
Tenuta M, Ferris H (2004) Relationship between nematode like-history classification and sensitivity to stressor: ionic and osmotic effects of nitrogenous solutions. J Nematol 36:85–94
Thomas RB, Richter DD, Ye H, Heine PR, Strain BR (1991) Nitrogen dynamics and growth of seedlings of an N-fixing tree (Gliricidia sepium (Jacq.) Walp.) exposed to elevated atmospheric carbon dioxide. Oecologia 88:415–421
Tissue DT, Megonigal JP, Thomas RB (1996) Nitrogenase activity and N2 fixation are stimulated by elevated CO2 in a tropical N2-fixing tree. Oecologia 109:28–33
Treonis AM, Lussenhop JF (1997) Rapid response of soil protozoa to elevated CO2. Biol Fertil Soils 25:60–62
Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200
Van Ginkel JH, Gorissen A (1998) In situ decomposition of grass roots as affected by elevated atmospheric carbon dioxide. Soil Sci Soc Am J 62:951–958
Van Ginkel JH, Gorissen A, Polci D (2000) Elevated atmospheric carbon dioxide concentration: effects of increased carbon input in a Lolium perenne soil on microorganisms and decomposition. Soil Biol Biochem 32:449–456
Van Veen JA, Morgan JAW, Whipps JM (2007) Methodological approaches to the study of carbon flow and the associated microbial population dynamics in the rhizosphere. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere. CRC, Boca Raton, pp 371–399
Walker RF, Geisinger DR, Johnson DW, Ball JT (1997) Elevated atmospheric CO2 and soil N fertility effects on growth, mycorrhizal colonization, and xylem water potential of juvenile ponderosa pine in a field soil. Plant Soil 195:25–36
Wan S, Norby RJ, Pregitzer KS, Ledford J, O'Neill EG (2004) CO2 enrichment and warming of the atmosphere enhance both productivity and mortality of maple tree fine roots. New Phytol 162:437–446
Wiemken V, Laczko E, Ineichen K, Boller T (2001) Effects of elevated carbon dioxide and nitrogen fertilization on mycorrhizal fine roots and the soil microbial community in beech-spruce ecosystems on siliceous and calcareous soil. Microb Ecol 42:126–135
Williams MAC, Rice W, Owensby WE (2000) C dynamics and microbial activity in tallgrass prairie exposed to elevated CO2 for 8 years. Plant Soil 227:127–137
Wolf J, Johnson NC, Rowland DL, Reich PB (2003) Elevated CO2 and plant species richness impact arbuscular mycorrhizal fungal spore communities. New Phytol 157:579–588
Yeates GW, Tate KR, Newton PCD (1997) Response of the fauna of a grassland soil to doubling of atmospheric carbon dioxide concentration. Biol Fertil Soils 25:307–315
Yeates GW, Newton PCD, Ross DJ (2003) Significant changes in soil microfauna in grazed pasture under elevated carbon dioxide. Biol Fertil Soils 38:319–326
Zak DR, Pregitzer KS, Curtis PS, Teeri JA, Fogel R, Randlett DL (1993) Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant Soil 151:105–117
Zak DR, Ringelberg DB, Pregitzer KS, Randlett DL, White DC, Curtis PS (1996) Soil microbial communities beneath Populus grandidentata grown under elevated atmospheric CO2. Ecol Appl 6:257–262
Zak DR, Pregitzer KS, Curtis PS, Holmes WE (2000) Atmospheric CO2 and the composition and function of soil microbial communities. Ecol Appl 10:47–59
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Drigo, B., Kowalchuk, G.A. & van Veen, J.A. Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44, 667–679 (2008). https://doi.org/10.1007/s00374-008-0277-3
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DOI: https://doi.org/10.1007/s00374-008-0277-3