Decoupling of arbuscular mycorrhizal fungi and soil organic carbon under nitrogen addition in terrestrial ecosystems: a meta-analysis

Abstract

Arbuscular mycorrhizal fungi (AMF) play a crucial role in ecosystem carbon storage and climate change mitigation. However, the relationship between AMF and soil organic carbon (SOC) dynamics under nitrogen (N) deposition remains poorly understood. In this global meta-analysis, we synthesized data from 438 observations across 45 studies. Results demonstrated a general decrease in AMF abundance under N addition treatments: both AMF biomass and root colonization rate declined by 11%. Specifically, AMF biomass decreased significantly in temperate (−19%), tropical/subtropical (−10%), and alpine (−8%) ecosystems. Similarly, root colonization rate declined in temperate (−8%), alpine (−3%), and tropical/subtropical (−2%) zones. Interestingly, AMF diversity remained unchanged. Additionally, N addition significantly increased SOC storage (by 3%) and soil available N (by 12%), while it decreased soil available phosphorous (by 5%) and soil pH (by 2%). The responses of AM fungal traits and soil properties varied depending on fertilizer types, ecosystem types, and climate conditions. Meta-regression analysis identified local atmospheric N deposition rates as the most significant factor influencing AM fungal traits (based on multi-model inference). Moreover, we found that AMF abundance, including AMF biomass and root colonization rate, had no significant relationship with SOC variations (p > 0.1, R² < 0.1). This lack of a direct relationship, coupled with the concurrent decline in AMF abundance and increase in SOC, indicates that N deposition may disrupt the typical linkage between AMF and SOC dynamics, potentially leading to their decoupling.

Graphical abstract

Keywords

arbuscular mycorrhizal fungi / meta-analysis / nitrogen addition / soil organic carbon / terrestrial ecosystem

References

[1] Averill C, Turner B L, Finzi A C (2014). Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage.Nature, 505(7484): 543–545

[2] Averill C, Hawkes C V (2016). Ectomycorrhizal fungi slow soil carbon cycling.Ecol Lett, 19(8): 937–947

[3] Babalola B J, Li J, Willing C E, Zheng Y, Wang Y L, Gan H Y, Li X C, Wang C, Adams C A, Gao C, Guo L D (2022). Nitrogen fertilisation disrupts the temporal dynamics of arbuscular mycorrhizal fungal hyphae but not spore density and community composition in a wheat field.New Phytol, 234(6): 2057–2072

[4] Balduzzi S, Ruecker G, Schwarzer G (2019). How to perform a meta-analysis with R: a practical tutorial.BMJ Ment Health, 22(4): 153–160

[5] Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J W, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010). Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis.Ecol Appl, 20(1): 30–59

[6] Chagnon P L, Bradley R L, Maherali H, Klironomos J N (2013). A trait-based framework to understand life history of mycorrhizal fungi.Trends Plant Sci, 18(9): 484–491

[7] Chen J, Luo Y, Van Groenigen K J, Hungate B A, Cao J, Zhou X, Wang R W (2018). A keystone microbial enzyme for nitrogen control of soil carbon storage.Science Advances, 4(8): eaaq1689

[8] Cotton T E A (2018). Arbuscular mycorrhizal fungal communities and global change: an uncertain future.FEMS Microbiol Ecol, 94(11): fiy179

[9] Duan S L, Feng G, Limpens E, Bonfante P, Xie X N, Zhang L (2024). Cross-kingdom nutrient exchange in the plant–arbuscular mycorrhizal fungus–bacterium continuum.Nat Rev Microbiol, 22(12): 773–790

[10] Dickie I A, Koele N, Blum J D, Gleason J D, McGlone M S (2014). Mycorrhizas in changing ecosystems.Botany, 92(2): 149–160

[11] Feng H L, Guo J H, Peng C H, Kneeshaw D, Roberge G, Pan C, Ma X H, Zhou D, Wang W F (2023). Nitrogen addition promotes terrestrial plants to allocate more biomass to aboveground organs: a global meta‐analysis.Glob Change Biol, 29(14): 3970–3989

[12] Galloway J N, Townsend A R, Erisman J W, Bekunda M, Cai Z C, Freney J R, Martinelli L A, Seitzinger S P, Sutton M A (2008). Transformation of the nitrogen cycle: recent trends, questions, and potential solutions.Science, 320(5878): 889–892

[13] Garcia M O, Ovasapyan T, Greas M, Treseder K K (2008). Mycorrhizal dynamics under elevated CO₂ and nitrogen fertilization in a warm temperate forest.Plant Soil, 303(1−2): 301–310

[14] Genre A, Lanfranco L, Perotto S, Bonfante P (2020). Unique and common traits in mycorrhizal symbioses.Nat Rev Microbiol, 18(11): 649–660

[15] Georgiou K, Koven C D, Wieder W R, Hartman M D, Riley W J, Pett-Ridge J, Bouskill N J, Abramoff R Z, Slessarev E W, Ahlström A, Parton W J, Pellegrini A F A, Pierson D, Sulman B N, Zhu Q, Jackson R B (2024). Emergent temperature sensitivity of soil organic carbon driven by mineral associations.Nat Geosci, 17(3): 205–212

[16] Han Y F, Feng J G, Han M G, Zhu B (2020). Responses of arbuscular mycorrhizal fungi to nitrogen addition: a meta-analysis.Glob Change Biol, 26(12): 7229–7241

[17] Hawkins H J, Cargill R I M, Van Nuland M E, Hagen S C, Field K J, Sheldrake M, Soudzilovskaia N A, Kiers E T (2023). Mycorrhizal mycelium as a global carbon pool.Curr Biol, 33(11): R560–R573

[18] Hedges L V, Gurevitch J, Curtis P S (1999). The meta-analysis of response ratios in experimental ecology.Ecology, 80(4): 1150–1156

[19] Joergensen R G (2022). Phospholipid fatty acids in soil—drawbacks and future prospects.Biol Fertil Soils, 58(1): 1–6

[20] Johnson N C, Rowland D L, Corkidi L, Egerton-Warburton L M, Allen E B (2003). Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands.Ecology, 84(7): 1895–1908

[21] Johnson N C (2010). Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales.New Phytol, 185(3): 631–647

[22] Lavallee J M, Soong J L, Cotrufo M F (2020). Conceptualizing soil organic matter into particulate and mineral‐associated forms to address global change in the 21st century.Glob Change Biol, 26(1): 261–273

[23] Lekberg Y, Bååth E, Frostegård Å, Hammer E, Hedlund K, Jansa J, Kaiser C, Ramsey P W, Řezanka T, Rousk J, Wallander H, Welc M, Olsson P A (2022). Fatty acid 16: 1ω5 as a proxy for arbuscular mycorrhizal fungal biomass: current challenges and ways forward.Biol Fertil Soils, 58(8): 835–842

[24] Li A D, Meidl P, Wang S H, Tang B, Rillig M C, Yu G C, Chen J, Liu R Z, Lie Z Y, Wu A C, Rong L L, Peng C, Liu Z F, Zhang W, Lu X K, Liu J X, Ye Q, Mo J M, Zheng M H (2025). Atmospheric nitrogen deposition has minor impacts on the abundance and diversity of arbuscular mycorrhizal fungi and their contribution to soil carbon stock in tropical forests.Soil Biol Biochem, 204: 109746

[25] Lilleskov E A, Kuyper T W, Bidartondo M I, Hobbie E A (2019). Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review.Environ Pollut, 246: 148–162

[26] Liu C H, Wang B R, Liu J Q, Guo C M, Li H J, Zhang H L, Hu Y, Ao D, Xue Z J, An S S, Zhu Z L (2025). Arbuscular mycorrhizal fungi hyphal density rather than diversity stimulates microbial necromass accumulation after long-term Robinia pseudoacacia plantations.Soil Biol Biochem, 206: 109817

[27] Liu X J, Duan L, Mo J M, Du E Z, Shen J L, Lu X K, Zhang Y, Zhou X B, He C, Zhang F S (2011). Nitrogen deposition and its ecological impact in China: an overview.Environ Pollut, 159(10): 2251–2264

[28] Lu X F, Hou E Q, Guo J Y, Gilliam F S, Li J L, Tang S B, Kuang Y W (2021a). Nitrogen addition stimulates soil aggregation and enhances carbon storage in terrestrial ecosystems of China: a meta‐analysis.Glob Change Biol, 27(12): 2780–2792

[29] Lu X K, Vitousek P M, Mao Q G, Gilliam F S, Luo Y Q, Turner B L, Zhou G Y, Mo J M (2021b). Nitrogen deposition accelerates soil carbon sequestration in tropical forests.Proc Natl Acad Sci USA, 118(16): e2020790118

[30] Ma X C, Geng Q H, Zhang H G, Bian C Y, Chen H Y H, Jiang D L, Xu X (2021). Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multi-functionality.New Phytol, 229(5): 2957–2969

[31] Maitra P, Zheng Y, Wang Y L, Mandal D, Lü P P, Gao C, Babalola B J, Ji N N, Li X C, Guo L D (2021). Phosphorus fertilization rather than nitrogen fertilization, growing season and plant successional stage structures arbuscular mycorrhizal fungal community in a subtropical forest.Biol Fertil Soils, 57(5): 685–697

[32] Niu S L, Song L, Wang J S, Luo Y Q, Yu G R (2023). Dynamic carbon-nitrogen coupling under global change.Sci China Life Sci, 66(4): 771–782

[33] Penuelas J, Janssens I A, Ciais P, Obersteiner M, Sardans J (2020). Anthropogenic global shifts in biospheric N and P concentrations and ratios and their impacts on biodiversity, ecosystem productivity, food security, and human health.Glob Change Biol, 26(4): 1962–1985

[34] Phillips R P, Meier I C, Bernhardt E S, Grandy A S, Wickings K, Finzi A C (2012). Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO₂.Ecol Lett, 15(9): 1042–1049

[35] Reay D S, Dentener F, Smith P, Grace J, Feely R A (2008). Global nitrogen deposition and carbon sinks.Nat Geosci, 1(7): 430–437

[36] Rillig M C, Wright S F, Nichols K A, Schmidt W F, Torn M S (2001). Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils.Plant Soil, 233(2): 167–177

[37] Rillig M C (2004). Arbuscular mycorrhizae and terrestrial ecosystem processes.Ecol Lett, 7(8): 740–754

[38] Rillig M C, Aguilar-Trigueros C A, Bergmann J, Verbruggen E, Veresoglou S D, Lehmann A (2015). Plant root and mycorrhizal fungal traits for understanding soil aggregation.New Phytol, 205(4): 1385–1388

[39] Schmidt M W I, Torn M S, Abiven S, Dittmar T, Guggenberger G, Janssens I A, Kleber M, Kögel-Knabner I, Lehmann J, Manning D A C, Nannipieri P, Rasse D P, Weiner S, Trumbore S E (2011). Persistence of soil organic matter as an ecosystem property.Nature, 478(7367): 49–56

[40] Stevens C J, David T I, Storkey J (2018). Atmospheric nitrogen deposition in terrestrial ecosystems: its impact on plant communities and consequences across trophic levels.Funct Ecol, 32(7): 1757–1769

[41] Tang B, Rocci K S, Lehmann A, Rillig M C (2023). Nitrogen increases soil organic carbon accrual and alters its functionality.Glob Change Biol, 29(7): 1971–1983

[42] Tao J Y, Liu X Y (2024). Does arbuscular mycorrhizal fungi inoculation influence soil carbon sequestration.Biol Fertil Soils, 60(2): 213–225

[43] Tedersoo L, Bahram M (2019). Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes.Biol Rev Camb Philos Soc, 94(5): 1857–1880

[44] Treseder K K, Allen M F (2000). Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO₂ and nitrogen deposition.New Phytol, 147(1): 189–200

[45] Treseder K K (2004). A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO₂ in field studies.New Phytol, 164(2): 347–355

[46] Treseder K K (2008). Nitrogen additions and microbial biomass: a meta‐analysis of ecosystem studies.Ecol Lett, 11(10): 1111–1120

[47] Treseder K K (2013). The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content.Plant Soil, 371(1−2): 1–13

[48] Treseder K K, Allen E B, Egerton-Warburton L M, Hart M M, Klironomos J N, Maherali H, Tedersoo L (2018). Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: a trait-based predictive framework.J Ecol, 106(2): 480–489

[49] Viechtbauer W (2010). Conducting meta-analyses in R with the metafor package.J Stat Softw, 36(3): 1–48

[50] Wilson G W T, Rice C W, Rillig M C, Springer A, Hartnett D C (2009). Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments.Ecol Lett, 12(5): 452–461

[51] Wu H, Yang J J, Fu W, Rillig M C, Cao Z J, Zhao A H, Hao Z P, Zhang X, Chen B D, Han X G (2023). Identifying thresholds of nitrogen enrichment for substantial shifts in arbuscular mycorrhizal fungal community metrics in a temperate grassland of northern China.New Phytol, 237(1): 279–294

[52] Xu C H, Xu X, Ju C H, Chen H Y H, Wilsey B J, Luo Y Q, Fan W (2021). Long‐term, amplified responses of soil organic carbon to nitrogen addition worldwide.Glob Change Biol, 27(6): 1170–1180

[53] Yang Y, Chen X L, Liu L X, Li T, Dou Y X, Qiao J B, Wang Y Q, An S S, Chang S X (2022). Nitrogen fertilization weakens the linkage between soil carbon and microbial diversity: a global meta‐analysis.Glob Change Biol, 28(21): 6446–6461

[54] Zak D R, Pellitier P T, Argiroff W A, Castillo B, James T Y, Nave L E, Averill C, Beidler K V, Bhatnagar J, Blesh J, Classen A T, Craig M, Fernandez C W, Gundersen P, Johansen R, Koide R T, Lilleskov E A, Lindahl B D, Nadelhoffer K J, Phillips R P, Tunlid A (2019). Exploring the role of ectomycorrhizal fungi in soil carbon dynamics.New Phytol, 223(1): 33–39

[55] Zhang T A, Chen H Y H, Ruan H H (2018). Global negative effects of nitrogen deposition on soil microbes.ISME J, 12(7): 1817–1825

[56] Zheng W S, Morris E K, Rillig M C (2014). Ectomycorrhizal fungi in association with Pinus sylvestris seedlings promote soil aggregation and soil water repellency.Soil Biol Biochem, 78: 326–331

[57] Zhou J, Zang H D, Loeppmann S, Gube M, Kuzyakov Y, Pausch J (2020). Arbuscular mycorrhiza enhances rhizodeposition and reduces the rhizosphere priming effect on the decomposition of soil organic matter.Soil Biol Biochem, 140: 107641

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