Arbuscular Mycorrhizal Fungi Increase Organic Carbon Decomposition Under Elevated CO2
A Fungal Culprit to Carbon Loss
In some ecosystems, such as in the layer of soil containing plant roots, fungi, and bacteria, increased levels of CO2 should stimulate more efficient aboveground photosynthesis, which in turn should promote increased sequestration of organic carbon in soil through the protective action of arbuscular mycorrhizal fungi. However, in a series of field and microcosm experiments performed under elevated levels of CO2 thought to be consistent with future emissions scenarios, Cheng et al. (p. 1084; see the Perspective by Kowalchuk) observed that these fungi actually promote degradation of soil organic carbon, releasing more CO2 in the process.
Abstract
The extent to which terrestrial ecosystems can sequester carbon to mitigate climate change is a matter of debate. The stimulation of arbuscular mycorrhizal fungi (AMF) by elevated atmospheric carbon dioxide (CO2) has been assumed to be a major mechanism facilitating soil carbon sequestration by increasing carbon inputs to soil and by protecting organic carbon from decomposition via aggregation. We present evidence from four independent microcosm and field experiments demonstrating that CO2 enhancement of AMF results in considerable soil carbon losses. Our findings challenge the assumption that AMF protect against degradation of organic carbon in soil and raise questions about the current prediction of terrestrial ecosystem carbon balance under future climate-change scenarios.
Get full access to this article
View all available purchase options and get full access to this article.
Already a Subscriber?Sign In
Supplementary Material
Summary
Materials and Methods
Figs. S1 to S7
Tables S1 and S2
Resources
File (cheng.sm.pdf)
References and Notes
1
S. E. Smith, D. J. Read, Mycorrhizal Symbiosis (Academic Press, San Diego, ed. 2, 2008).
2
Kiers E. T., et al., Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880 (2011).
3
Drigo B., et al., Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc. Natl. Acad. Sci. U.S.A. 107, 10938 (2010).
4
Jakobsen I., Rosendahl L., Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol. 115, 77 (1990).
5
Wilson G. W. T., Rice C. W., Rillig M. C., Springer A., Hartnett D. C., Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: Results from long-term field experiments. Ecol. Lett. 12, 452 (2009).
6
Tisdall J. M., Smith S. E., Rengasamy P., Aggregation of soil by fungal hyphae. Aust. J. Soil Res. 35, 55 (1997).
7
Sanders I. R., Streitwolf-Engel R., van der Heijden M. G. A., Boller T., Wiemken A., Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO 2 enrichment. Oecologia 117, 496 (1998).
8
Treseder K. K., Allen M. F., Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol. 147, 189 (2000).
9
Alberton O., Kuyper T. W., Gorissen A., Taking mycocentrism seriously: Mycorrhizal fungal and plant responses to elevated CO2. New Phytol. 167, 859 (2005).
10
Rillig M. C., Wright S. F., Allen M. F., Field C. B., Nature 400, 628 (1999).
11
Hu S., Chapin F. S., Firestone M. K., Field C. B., Chiariello N. R., Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409, 188 (2001).
12
Orwin K. H., Kirschbaum M. U. F., St John M. G., Dickie I. A., Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: A model-based assessment. Ecol. Lett. 14, 493 (2011).
13
Hodge A., Fitter A. H., Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc. Natl. Acad. Sci. U.S.A. 107, 13754 (2010).
14
Tu C., et al., Mycorrhizal mediation of plant N acquisition and residue decomposition: Impact of mineral N inputs. Glob. Change Biol. 12, 793 (2006).
15
Hodge A., Campbell C. D., Fitter A. H., An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413, 297 (2001).
16
See supplementary materials on Science Online.
17
S. Solomon et al., 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 Univ. Press, Cambridge, 2007).
18
Cheng L., et al., Soil microbial responses to elevated CO₂ and O₃ in a nitrogen-aggrading agroecosystem. PLoS ONE 6, e21377 (2011).
19
Bloom A. J., Burger M., R. Asensio J. S., Cousins A. B., Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328, 899 (2010).
20
Bloom A. J., Smart D. R., Nguyen D. T., Searles P. S., Nitrogen assimilation and growth of wheat under elevated carbon dioxide. Proc. Natl. Acad. Sci. U.S.A. 99, 1730 (2002).
21
Di H. J., et al., Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2, 621 (2009).
22
Fellbaum C. R., et al., Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 109, 2666 (2012).
23
Govindarajulu M., et al., Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819 (2005).
24
Bonfante P., Anca I.-A., Plants, mycorrhizal fungi, and bacteria: A network of interactions. Annu. Rev. Microbiol. 63, 363 (2009).
25
Phillips R. P., Finzi A. C., Bernhardt E. S., Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol. Lett. 14, 187 (2011).
26
Carney K. M., Hungate B. A., Drake B. G., Megonigal J. P., Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc. Natl. Acad. Sci. U.S.A. 104, 4990 (2007).
27
de Graaff M.-A., Classen A. T., Castro H. F., Schadt C. W., Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol. 188, 1055 (2010).
28
Geisseler D., Horwath W. R., Joergensen R. G., Ludwig B., Pathways of nitrogen utilization by soil microorganisms—a review. Soil Biol. Biochem. 42, 2058 (2010).
29
Davidson E. A., Janssens I. A., Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165 (2006).
30
van Groenigen K. J., Osenberg C. W., Hungate B. A., Increased soil emissions of potent greenhouse gases under increased atmospheric CO2. Nature 475, 214 (2011).
31
Reich P. B., et al., Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440, 922 (2006).
32
Hu S., Wu J., Burkey K. O., Firestone M. K., Plant and microbial N acquisition under elevated atmospheric CO2 in two mesocosm experiments with annual grasses. Glob. Change Biol. 11, 213 (2005).
33
Koide R. T., Li M. G., Appropriate controls for vesicular-arbuscular mycorrhiza research. New Phytol. 111, 35 (1989).
34
D. M. Sylvia, in Methods of Soil Analysis. Part 2. Microbiological and Biochemical Properties, R. W. et al. Waver, Ed. (Soil Science Society of America, Madison, WI, 1994), vol. 2, pp. 351–378.
35
Di H. J., Cameron K. C., Mitigation of nitrous oxide emissions in spray-irrigated grazed grassland by treating the soil with dicyandiamide, a nitrification inhibitor. Soil Use Manage. 19, 284 (2003).
36
O'Callaghan M., et al., Effect of the nitrification inhibitor dicyandiamide (DCD) on microbial communities in a pasture soil amended with bovine urine. Soil Biol. Biochem. 42, 1425 (2010).
37
McCarty G. W., Bremner J. M., Laboratory evaluation of dicyandiamide as a soil nitrification inhibitor. Commun. Soil Sci. Plant Anal. 20, 2049 (1989).
38
Akiyama H., Yan X., Yagi K., Evaluation of effectiveness of enhanced-efficiency fertilizers as mitigation options for N2O and NO emissions from agricultural soils: Meta-analysis. Glob. Change Biol. 16, 1837 (2010).
39
Hedges L. V., Gurevitch J., Curtis P. S., The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150 (1999).
40
M. S. Rosenberg, D. C. Adams, J. Gurevitch, MetaWin. Statistical Software for Meta-analysis. Version 2.0. (Sinauer, Sunderland, MA, 2000).
41
Balser T. C., Treseder K. K., Ekenler M., Using lipid analysis and hyphal length to quantify AM and saprotrophic fungal abundance along a soil chronosequence. Soil Biol. Biochem. 37, 601 (2005).
42
Bossio D. A., Scow K. M., Gunapala N., Graham K. J., Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb. Ecol. 36, 1 (1998).
43
S. C. Hart, J. M. Stark, E. A. Davidson, M. K. Firestone, in Methods of Soil Analysis. Part 2. Microbiological and Biochemical Properties, R. W. Weaver et al., Eds. (Soil Science Society of America, Madison, WI, 1994), pp. 985–1018.
44
R. C. Littell, G. A. Milliken, W. W. Strooup, R. D. Wolfinger, O. Schabenberger, SAS for Mixed Models (SAS Institute, Cary, NC, ed. 2, 2006).
45
Barnard R., Barthes L., Le Roux X., Leadley P. W., Dynamics of nitrifying activities, denitrifying activities and nitrogen in grassland mesocosms as altered by elevated CO2. New Phytol. 162, 365 (2004).
46
Barnard R., Barthes L., Leadley P. W., Short-term uptake of 15n by a grass and soil micro-organisms after long-term exposure to elevated CO2. Plant Soil 280, 91 (2006).
47
Bassirirad H., Griffin K. L., Strain B. R., Reynolds J. F., Effects of CO2 enrichment on growth and root 15NH4+ uptake rate of loblolly pine and ponderosa pine seedlings. Tree Physiol. 16, 957 (1996).
48
Bassirirad H., Thomas R. B., Reynolds J. F., Strain B. R., Differential responses of root uptake kinetics of NH4+ and NO3– to enriched atmospheric CO2 concentration in field-grown loblolly pine. Plant Cell Environ. 19, 367 (1996).
49
BassiriRad H., Griffin K. L., Reynolds J. F., Strain B. R., Changes in root NH4+ and NO3− absorption rates of loblolly and ponderosa pine in response to CO2 enrichment. Plant Soil 190, 1 (1997).
50
Bassirirad H., Reynolds J. F., Virginia R. A., Brunelle M. H., Growth and root NO3– and PO43– uptake capacity of three desert species in response to atmospheric CO2 enrichment. Aust. J. Plant Physiol. 24, 353 (1997).
51
BassiriRad H., Prior S. A., Norby R. J., Rogers H. H., A field method of determining NH4+ and NO3– uptake kinetics in intact roots: Effects of CO2 enrichment on trees and crop species. Plant Soil 217, 195 (1999).
52
Bauer G. A., Berntson G. M., Ammonium and nitrate acquisition by plants in response to elevated CO2 concentration: The roles of root physiology and architecture. Tree Physiol. 21, 137 (2001).
53
Constable J. V. H., Bassirirad H., Lussenhop J., Zerihun A., Influence of elevated CO2 and mycorrhizae on nitrogen acquisition: Contrasting responses in Pinus taeda and Liquidambar styraciflua. Tree Physiol. 21, 83 (2001).
54
Cruz C., Lips S. H., Martins-Loucao M. A., Changes in the morphology of roots and leaves of carob seedlings induced by nitrogen source and atmospheric carbon dioxide. Ann. Bot. (Lond.) 80, 817 (1997).
55
Gloser V., et al., Soil mineral nitrogen availability was unaffected by elevated atmospheric pCO2 in a four year old field experiment (Swiss FACE). Plant Soil 227, 291 (2000).
56
Hagedorn F., Landolt W., Tarjan D., Egli P., Bucher J. B., Elevated CO2 influences nutrient availability in young beech-spruce communities on two soil types. Oecologia 132, 109 (2002).
57
Hoque M. M., et al., Nitrogen dynamics in paddy field as influenced by free-air CO2 enrichment (FACE) at three levels of nitrogen fertilization. Nutr. Cycl. Agroecosyst. 63, 301 (2002).
58
Hungate B. A., Canadell J., Chapin F. S., Plant species mediate changes in soil microbial N in response to elevated CO2. Ecology 77, 2505 (1996).
59
Hungate B. A., Chapin F. S., Zhong H., Holland E. A., Field C. B., Stimulation of grassland nitrogen cycling under carbon dioxide enrichment. Oecologia 109, 149 (1997).
60
Hungate B. A., Dijkstra P., Johnson D. W., Hinkle C. R., Drake B. G., Elevated CO2 increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Glob. Change Biol. 5, 781 (1999).
61
Jackson R. B., Reynolds H. L., Nitrate and ammonium uptake for single-and mixed-species communities grown at elevated CO2. Oecologia 105, 74 (1996).
62
Jin V. L., Evans R. D., Elevated CO2 increases plant uptake of organic and inorganic N in the desert shrub Larrea tridentata. Oecologia 163, 257 (2010).
63
Johnson D. W., Ball T., Walker R. F., Effects of elevated CO2 and nitrogen on nutrient uptake in ponderosa pine seedlings. Plant Soil 168-169, 535 (1995).
64
Johnson D. W., et al., Effects of elevated CO2 on nutrient cycling in a sweetgum plantation. Biogeochemistry 69, 379 (2004).
65
Kanerva T., et al., A 3-year exposure to CO2 and O3 induced minor changes in soil N cycling in a meadow ecosystem. Plant Soil 286, 61 (2006).
66
Kruse J., et al., Elevated pCO2 favours nitrate reduction in the roots of wild-type tobacco (Nicotiana tabacum cv. Gat.) and significantly alters N-metabolism in transformants lacking functional nitrate reductase in the roots. J. Exp. Bot. 53, 2351 (2002).
67
Kruse J., Hetzger I., Mai C., Polle A., Rennenberg H., Elevated pCO2 affects N-metabolism of young poplar plants (Populus tremula x P. alba) differently at deficient and sufficient N-supply. New Phytol. 157, 65 (2003).
68
Marhan S., et al., Abundance and activity of nitrate reducers in an arable soil are more affected by temporal variation and soil depth than by elevated atmospheric [CO2]. FEMS Microbiol. Ecol. 76, 209 (2011).
69
Matt P., et al., Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate. Plant Cell Environ. 24, 1119 (2001).
70
Rachmilevitch S., Cousins A. B., Bloom A. J., Nitrate assimilation in plant shoots depends on photorespiration. Proc. Natl. Acad. Sci. U.S.A. 101, 11506 (2004).
71
Regan K., et al., Can differences in microbial abundances help explain enhanced N2O emissions in a permanent grassland under elevated atmospheric CO2? Glob. Change Biol. 17, 3176 (2011).
72
Richter M., Hartwig U. A., Frossard E., Nosberger J., Cadisch G., Gross fluxes of nitrogen in grassland soil exposed to elevated atmospheric pCO2 for seven years. Soil Biol. Biochem. 35, 1325 (2003).
73
Rothstein D. E., Zak D. R., Pregitzer K. S., Curtis P. S., Kinetics of nitrogen uptake by Populus tremuloides in relation to atmospheric CO2 and soil nitrogen availability. Tree Physiol. 20, 265 (2000).
74
Shimono H., Bunce J. A., Acclimation of nitrogen uptake capacity of rice to elevated atmospheric CO2 concentration. Ann. Bot. (Lond.) 103, 87 (2009).
75
Wang X. Z., Zhang H. J., Sun W., Feng K., Zhu J. G., Effects of elevated atmospheric CO2 on paddy soil nitrogen content during rice season. Ying Yong Sheng Tai Xue Bao 21, 2161 (2010).
76
Yamakawa Y., Saigusa M., Okada M., Kobayashi K., Nutrient uptake by rice and soil solution composition under atmospheric CO2 enrichment. Plant Soil 259, 367 (2004).
77
Yoder C. K., Vivin P., Defalco L. A., Seemann J. R., Nowak R. S., Root growth and function of three Mojave Desert grasses in response to elevated atmospheric CO2 concentration. New Phytol. 145, 245 (2000).
78
Zak D. R., Holmes W. E., Pregitzer K. S., Atmospheric CO2 and O3 alter the flow of 15N in developing forest ecosystems. Ecology 88, 2630 (2007).
79
Zerihun A., Bassirirad H., Interspecies variation in nitrogen uptake kinetic responses of temperate forest species to elevated CO2: Potential causes and consequences. Glob. Change Biol. 7, 211 (2001).
Information & Authors
Information
Published In
Science
Volume 337 | Issue 6098
31 August 2012
31 August 2012
Copyright
Copyright © 2012, American Association for the Advancement of Science.
Submission history
Received: 4 May 2012
Accepted: 10 July 2012
Published in print: 31 August 2012
Acknowledgments
We thank F. Chapin III, D. Coleman, Y. Luo, R. Miller, and M. Rillig for valuable comments; M. Gumpertz for advice on statistical analyses; J. Barton, W. Pursley, and E. Silva for technical assistance; and D. Watson and J. Morton for providing mycorrhizal inoculum. L.C. was primarily supported by a fellowship from U.S. Department of Agriculture (USDA)–Agricultural Research Service Plant Science Research Unit (Raleigh, NC) and in part by a USDA grant to S.H. (2009-35101-05351). S.H., L.C. and C.T. conceived experiments 1 to 4. K.O.B. and F.L.B. designed and maintained the long-term CO2 and O3 study. H.D.S and T.W.R. contributed to design of experiments 1 and 2. L.C. performed experiments 1 to 3 and the meta-analysis study; and C.T., F.L.B., and L.Z. performed experiment 4. L.C. and S.H. analyzed the data and mainly wrote the manuscript with inputs from all coauthors. The data reported in this paper are deposited in the Dryad Repository (http://dx.doi.org/10.5061/dryad.b7f53).
Authors
Metrics & Citations
Metrics
Article Usage
Altmetrics
Citations
Export citation
Select the format you want to export the citation of this publication.
Cited by
- Warming and elevated ozone induce tradeoffs between fine roots and mycorrhizal fungi and stimulate organic carbon decomposition, Science Advances, 7, 28, (2021)./doi/10.1126/sciadv.abe9256
- Fine root trait-function relationships affected by mycorrhizal type and climate, Geoderma, 394, (115011), (2021).https://doi.org/10.1016/j.geoderma.2021.115011
- Variations in glomalin-related soil protein in Vicia faba rhizosphere depending upon interactions among mycorrhization, daytime and/or nighttime elevated CO2 levels, Geoderma, 404, (115283), (2021).https://doi.org/10.1016/j.geoderma.2021.115283
- Plant phosphorus-acquisition and -use strategies affect soil carbon cycling, Trends in Ecology & Evolution, (2021).https://doi.org/10.1016/j.tree.2021.06.005
- Straw incorporation with ridge–furrow plastic film mulch alters soil fungal community and increases maize yield in a semiarid region of China, Applied Soil Ecology, 167, (104038), (2021).https://doi.org/10.1016/j.apsoil.2021.104038
- Arbuscular mycorrhizal fungi and biochar influence simazine decomposition and leaching, GCB Bioenergy, 13, 4, (708-718), (2021).https://doi.org/10.1111/gcbb.12802
- Plant Diversity Enhances Soil Fungal Diversity and Microbial Resistance to Plant Invasion, Applied and Environmental Microbiology, 87, 11, (2021).https://doi.org/10.1128/AEM.00251-21
- Arbuscular Mycorrhiza in Sustainable Plant Nitrogen Nutrition: Mechanisms and Impact, Soil Nitrogen Ecology, (407-436), (2021).https://doi.org/10.1007/978-3-030-71206-8_21
- Plant carbon inputs through shoot, root, and mycorrhizal pathways affect soil organic carbon turnover differently, Soil Biology and Biochemistry, 160, (108322), (2021).https://doi.org/10.1016/j.soilbio.2021.108322
- Effects of natural vegetation restoration on dissolved organic matter (DOM) biodegradability and its temperature sensitivity, Water Research, 191, (116792), (2021).https://doi.org/10.1016/j.watres.2020.116792
- See more
Loading...
View Options
Get Access
Log in to view the full text
AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.
- Become a AAAS Member
- Activate your AAAS ID
- Purchase Access to Other Journals in the Science Family
- Account Help
Log in via OpenAthens.
Log in via Shibboleth.
More options
Register for free to read this article
As a service to the community, this article is available for free. Login or register for free to read this article.
Buy a single issue of Science for just $15 USD.
View options
PDF format
Download this article as a PDF file
Download PDF