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

1 Introduction

Agricultural activities and fossil fuel combustion have disrupted the global nitrogen (N) cycle, resulting in significant increase in atmospheric N deposition across ecosystems, from the tropics to the tundra (Galloway et al., 2008; Penuelas et al., 2020). These elevated levels of N deposition are widely recognized as threats to biodiversity and ecosystem functioning (Bobbink et al., 2010; Stevens et al., 2018; Zhang et al., 2018). However, there is emerging evidence suggesting that N deposition could also play a role in mitigating the negative effects of anthropogenic CO₂ emissions, mainly through its potential to enhance soil carbon (C) sequestration, a process significantly influenced by soil microorganisms, e.g., arbuscular mycorrhizal fungi (AMF) (Lu et al., 2021a, 2021b; Tang et al., 2023). As the largest C sink in terrestrial ecosystems, soil organic carbon (SOC) plays an important role in regulating climate change (Georgiou et al., 2024). Recent studies have further emphasized the role of soil microorganisms as key drivers of soil C cycling (Lavallee et al., 2020).

Among the key player in soil C cycling, mycorrhizal association, particularly those formed by AMF, is an essential pathway for plants to acquire soil nutrients. AMF not only contributes to soil nutrient dynamics but also plays a critical role in soil C storage, which may be influenced by changes in soil N availability. AMF receive photosynthetically derived C from plants in exchange for essential mineral nutrients, such as N and phosphorus (P) (Genre et al., 2020; Duan et al., 2024). Recent studies have highlighted the role of mycorrhizal fungi in terrestrial ecosystem processes, including soil C and N cycling (Rillig, 2004; Averill and Hawkes, 2016; Tedersoo and Bahram, 2019; Zak et al., 2019; Hawkins et al., 2023). For example, AMF can produce glomalin, a glycoprotein that helps bind soil particles, thus preventing soil erosion and leaching (Zheng et al., 2014). A proportion of AMF biomass may remain in the soil, ultimately contributing to the formation of soil organic matter (Wilson et al., 2009). Additionally, AMF can also release labile C compounds, which stimulates microbial enzyme activity and further promotes soil organic matter decomposition (Schmidt et al., 2011). Despite these contributions, the complexity of the pathways through which AMF influences soil C storage and balance remains poorly understood in the context of global change scenarios (Averill et al., 2014; Averill and Hawkes, 2016).

The relationships between AMF and soil C dynamics can be influenced by elevated N deposition (Treseder, 2008; Li et al., 2025). N addition may reduce the mycorrhizal dependency of trees, lower plant investment in these fungi, and trigger shifts in fungal community composition, e.g., the loss of key taxa (Treseder and Allen, 2000; Lilleskov et al., 2019). It may also enhance the photosynthetic capacity of host plants while increasing plant P demand. In such cases, increased N availability prompts plants to allocate more C to AMF in exchange for P from soils (Johnson, 2010). However, the responses of AMF to N addition are often variable, likely due to differences in soil nutrient availability and experimental conditions, such as the form, amount, and duration of N addition (Treseder et al., 2018; Tedersoo and Bahram, 2019; Han et al., 2020). Theoretically, both positive and negative feedback of AMF to N addition can occur, which depend on whether N addition results in a net decrease or increase in the abundance of AMF relative to other microbial functional groups (Averill and Hawkes, 2016). These changes may also depend on factors such as atmospheric N deposition, mean annual temperature (MAT), mean annual precipitation (MAP), and ecosystem types.

Although several studies have investigated the effects of N deposition on mycorrhizal fungi traits (Treseder, 2004; Han et al., 2020; Ma et al., 2021), the potential link between variations in AMF traits and SOC under N deposition remains unclear. To address this knowledge gap, we conducted a global-scale meta-analysis using 438 observations from 45 studies published over the past 20 years. AMF biomass, root colonization, extraradical hyphal length density, and spore density in soils were considered as indicators of fungal abundance, while fungal richness, and Shannon index were used to assess fungal diversity. Our data set includes three major terrestrial ecosystem types: forest, grassland, and desert. The objectives of this meta-analysis are to assess the responses of AMF abundance and diversity and explore their potential linkages to SOC dynamics under simulated N deposition.

2 Materials and methods

2.1 Literature search and selection

To assemble a representative sample of meta-analyses, we conducted a systematic search for all relevant studies using Web of Science and Google Scholar, covering the period from January 2000 to September 2024. The search terms/keywords were (‘arbuscular mycorrhizal fungi’ or ‘AMF’) and (‘nitrogen addition’ or ‘nitrogen deposition’) and (‘soil organic carbon’ or ‘SOC’ or ‘soil organic matter’). After removing duplicate studies, we identified a total of 1291 records. We then reviewed the titles and abstracts of these publications to exclude irrelevant literature. The full text of the remaining studies was screened to determine whether they met the following inclusion criteria. 1) All experimental studies must include both control and treatment groups, with at least three replicates in each group; 2) studies involving croplands, laboratory incubations, natural deposition gradients, N addition-terminated studies, and ecosystems affected by other factors (such as fire or fungicide treatment) were excluded; 3) studies that involved compound fertilizers (i.e., containing other nutrients) or combined treatments were excluded; 4) studies that did not distinguish AMF but instead referred to mycorrhizal fungi in general were excluded. After reviewing the publications, 45 studies were included in this synthesis. The selection process followed the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines (Fig. S1).

2.2 Data collection

For each study, we collected the mean values and sample sizes for all selected variables. These included information on mycorrhizal abundance (mycorrhizal biomass based on the phospholipid fatty acid [PLFA] method, spore density in soils, root colonization, and extraradical hyphae length density) and diversity traits (Shannon index, Simpson index, Faith’s phylogenetic diversity [Faith’s PD], and mycorrhizal species richness), soil available nutrients (available N and available P), soil organic matter or C concentrations, and soil pH. Since several variables did not meet the requirements for meta-analysis (i.e., fewer than 10 studies), the Simpson index and Faith’s PD were excluded from the final analysis. If a publication reported multiple experiments conducted at different sites, vegetation types, N addition levels, or N fertilizer types, each was treated as an independent experiment. Data from figures were digitally extracted using WebPlotDigitizer when results were graphically represented. We complied 230 observations of AM fungal traits and 198 observations of SOC and other soil properties from terrestrial ecosystems (Fig. 1). This data set included 54 observations for biomass based on the PLFA method, 25 for spore density, 69 for mycorrhizal colonization, 39 for extraradical hyphae length density, 18 for the Shannon index, 25 for mycorrhizal species richness, 57 for available N, 49 for available P, 37 for SOC, and 55 for soil pH. In addition, we recorded corresponding basic information, including the study site, background atmospheric N deposition rate, climate type, N addition rate, fertilizer type, treatment duration, ecosystem type, mean annual temperature (MAT), and mean annual precipitation (MAP). We collected either standard deviation (SD) or standard error (SE), with unspecified error bars recorded as SE. We calculated SD from the reported SE and sample sizes (n).

(1)SD=SE\times \sqrt{n}.

2.3 Meta-analysis

The natural log-transformed response ratio (lnRR) was used as the effect size to assess the response of mycorrhizal traits, as well as soil chemical properties and SOC, to N addition in each independent study (Hedges et al., 1999). The lnRR was calculated as

(2)\ln RR=\ln \frac{{\overline{x}}_t}{{\overline{x}}_c}=\ln {\overline{x}}_t-\ln {\overline{x}}_c,

where {\overline{x}}_t and {\overline{x}}_c are mean value of each variable in N addition treatment and control, respectively. The weighted response ratio (lnRR_w) was calculated from the individual lnRR_i by giving greater weight to the studies whose estimates have greater precision reflected by smaller v_i^{\ast }. The weighted pooled effect size of a group was

(3)\ln {RR}_W=\frac{{\sum }_{i=1}^m{w}_i^{\ast }\times \ln {RR}_i}{{\sum }_{i=1}^m{w}_i^{\ast }},

where m is the number of studies in the group, and w_i^{\ast } is the weighting factor of the ith experiment, w_i^{\ast } was then

(4)w_i^{\ast }=\frac{1}{v_i^{\ast }},

where v_i^{\ast } is the variance of study (i) in the group. Since random effects models were chose to assess the overall effects and heterogeneity in outcomes. The variance v_i^{\ast } is the sum of within-study variance and between-study variance:

(5)v_i^{\ast }=\frac{S{D}_t^2}{N_t\times {\overline{x}}_t^2}+\frac{S{D}_c^2}{N_c\times {\overline{x}}_c^2},

where SD_t and N_t are the standard deviation and sample size of treatment group, respectively. SD_c and N_c are the standard deviation and sample size of control group, respectively. What’s more, the percentage change (%) of the treatment effects was evaluated as

(6)\mathrm{P}\mathrm{e}\mathrm{r}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{g}\mathrm{e}\text{change}\left(\mathrm{\%}\right)=\left(e^{{\ln RR}_W}-1\right)\times 100\mathrm{\%}.

We performed a sensitivity test using the leave-one-out method, and we conducted Egger’s test and a funnel plot to detect potential publication bias (Table S1). If publication bias was detected, we made the proper adjustment using the trim-and-fill method. All of the above analyses were performed using the “meta” (Balduzzi et al., 2019), “metafor” (Viechtbauer, 2010) and “dmetar” packages in R version 4.4.2 (R Core Team 2024).

2.4 Multiple meta-regression analysis

We conducted multi-model inference to assess the relative importance of all the quantitative environmental variables (atmospheric N deposition, MAT, and MAP) and experimental variables (fertilization rates and duration) by considering all the possible combinations in predicting each weighted response ratio to N addition. Akaike’s Information Criterion Corrected for small samples (AICc) was used to select simpler models. These models were then applied to explain the effects of N addition on mycorrhizal traits, soil chemical properties, and SOC. We also evaluated the relative importance of AM fungal traits and soil properties in explaining SOC dynamics under N addition. Multiple meta-regression analyses were conducted using the “dmetar” package in R version 4.4.2 (R Core Team 2024).

3 Results

3.1 Effects of N addition on AMF traits, SOC, and other soil properties

The results indicated that AMF abundance (i.e., AMF biomass, root colonization, hyphal length density, and spore density) generally decreased following N addition, while fungal diversity (richness and Shannon index) remained unchanged (Fig. 2). Specifically, mycorrhizal root colonization and AMF biomass decreased significantly by 11%, and hyphal length density also declined by 4%, although this change was not statistically significant. N addition had no significant effects on fungal diversity, while the Shannon index showed positive responses to N addition (Fig. 2). N addition significantly affected SOC and other soil properties. Specifically, soil pH and AP decreased by 2% and 5%, respectively, while AN and SOC increased by 12% and 3%, respectively.

Furthermore, subgroup analysis revealed significant variations in the responses of AM fungal traits to N addition across different fertilizer types, ecosystem types, and climate conditions (Fig. 3). For example, AMF biomass (Q = 10.36, p = 0.006), spore density (Q = 50.99, p < 0.001), richness (Q = 36.37, p < 0.001), and the Shannon index (Q = 26.91, p < 0.001) showed notable differences among fertilizer types (Figs. 3(a), 3(d), 3(e), and 3(f)). AMF biomass also varied significantly across ecosystem types (Q = 38.34, p < 0.001), with a positive response in deserts and negative responses in forests and grasslands. Additionally, AMF biomass (Q = 8.70, p = 0.01), root colonization (Q = 21.17, p < 0.001), hyphal length density (Q = 49.87, p < 0.001), spore density (Q = 7.71, p = 0.02), richness (Q = 24.39, p < 0.001), and the Shannon index (Q = 25.43, p < 0.001) responded differently across various climate zones. Soil AN (Q = 6.21, p = 0.04) and pH (Q = 34.13, p < 0.0001) also exhibited variability across different ecosystem types (Fig. S2).

3.2 Regulators of AMF traits, SOC, and other soil properties in response to N addition

Local atmospheric N deposition was the most important factor influencing AMF traits (Fig. 4), particularly for AMF biomass (Fig. 4(a)), root colonization (Fig. 4(b)), hyphal length density (Fig. 4(c)), and richness (Fig. 4(e)). MAT was the second most important factor influencing AMF biomass and root colonization rate (Figs. 4(a) and 4(b)). Soil AN and pH were influenced by fertilization rates (Fig. S3). However, spore density (Fig. 4(d)), the Shannon index (Fig. 4(f)), SOC (Fig. 4(g)), and soil AP (Fig. S3(b)) were not significantly regulated by the environmental and experimental factors.

3.3 The potential link between AMF traits and SOC under N addition

Although the variables, such as AN, AP, soil pH, AMF biomass, and root colonization rate exhibited significantly changes following N addition (Fig. 2), our meta-regression results revealed that only AN had a significant positive impact on SOC (Fig. S4). We further conducted linear regression analyses to explore the relationship between AMF biomass, root colonization, and SOC. The results indicated that neither of these two AM fungal traits provided significant (p values > 0.1) or sufficient explanatory power (R² values < 0.1) for SOC variations (Fig. 5).

4 Discussion

4.1 Global responses of AMF traits on N addition

Consistent with previous studies (Treseder, 2004; Han et al., 2020; Ma et al., 2021), our results showed various responses of mycorrhizal traits to N addition (Fig. 2). Specifically, the abundance of mycorrhizal fungi, including root colonization rate and AMF biomass, decreased, while other indicators, such as hyphal length density and spore density, showed no significant change. Several potential mechanisms could explain the decrease in AMF abundance under N addition. First, increased soil AN may reduce below-ground C allocation by plants (Johnson et al., 2003; Johnson, 2010). Second, N addition can alter mycorrhizal-plant trading partnerships, shifting the relative costs and benefits of mycorrhizal symbioses (Johnson, 2010). Third, N addition may disrupt the relationship of AMF with their host plants and the soil microenvironment (Cotton, 2018). Additionally, soil acidification induced by N addition should not be overlooked, as it can suppress AMF colonization, spore production, and extraradical hyphae length growth (Han et al., 2020). Despite these changes in AMF abundance, the indicators of AMF diversity, such as species richness and the Shannon index, showed no significant responses (Fig. 2). This lack of response may result from differences in initial soil N/P ratios and variations in the behavior of different fungal guilds. For example, some AM fungal groups (e.g., Glomus) may be more resilient to N addition, whereas others may be more sensitive, resulting in no net change in community diversity (Garcia et al., 2008; Treseder et al., 2018; Wu et al., 2023).

The response ratio of mycorrhizal fungal traits, including AMF biomass, root colonization rate, hyphal length density, spore density, richness, and the Shannon index, varied significantly under different climatic conditions (Fig. 3). Root colonization showed a negative response to N addition in temperate zones but exhibited no significant responses in tropical/subtropical zones. This variation could be attributed to the already high levels of atmospheric N deposition in subtropical/tropical regions (Liu et al., 2011), where the added N fertilizer may be insufficient to induce notable changes in AMF. Moreover, atmospheric N deposition emerged as the most significant regulator of many AM fungal traits (Fig. 4). This result suggests that soil N availability is a key factor driving mycorrhizal responses, particularly in those regions with elevated N inputs. Additionally, ecosystem type played a critical role in shaping mycorrhizal responses to N addition, likely due to varying nutrient limitations across ecosystems (Han et al., 2020; Ma et al., 2021). Climate factors, such as MAP and MAT, significantly influenced AMF traits (Fig. 4). However, compared to previous findings (Ma et al., 2021), the direction of MAP and MAT effects on mycorrhizal responses to N addition appeared inconsistent. This finding highlights the complex interactions between climate and ecosystem-specific factors that control mycorrhizal dynamics. Overall, the regulators of mycorrhizal responses to N addition are highly complex and should be considered based on ecosystem types, soil resource availability, N addition rate and duration, host plants, and changes of plant species composition.

4.2 Effects of N addition on SOC and its potential connections to AMF traits

Among the soil properties examined, all the variables had significant responses to N addition, and particularly SOC showed a pronounced increasing trend (Fig. 2). This result aligns with findings from several previous studies (Xu et al., 2021; Niu et al., 2023; Tang et al., 2023). Increased N deposition generally enhances SOC storage by stimulating the production of aboveground plant biomass, thereby elevating aboveground C inputs to the soil system (Reay et al., 2008; Chen et al., 2018). Our findings support this general trend, as SOC increased by 3% following N addition. However, the complexity of soil C dynamics in response to N addition requires further exploration, given that the interactive effects commonly occur among plant-derived C inputs, microbial activity, and soil nutrient cycling. In our study, when exploring the relationships between soil chemical properties, AM fungal traits, and SOC, we found that none of these factors, except for soil AN, showed significant correlations with SOC (Fig. S4). This is mainly because soil nutrient availability is directly correlated with plant biomass production. Under increased N deposition, the observed SOC increase predominantly results from the enhanced transfer of plant-derived C inputs into the soil, rather than changes in microbial contribution (Xu et al., 2021; Feng et al., 2023). This finding highlights the important role of plant biomass-driven processes in SOC accumulation, while the contributions from microbes may be relatively minor.

Interestingly, we found that the responses of AMF abundance (in terms of AMF biomass and root colonization rate) and SOC to N addition were in opposite directions (Fig. 2), although their relationship was not statistically significant (Fig. 5). This absence of a significant direct link between AMF traits and SOC under N addition contrasts with previous studies that highlighted the critical role of AMF in soil C sequestration (Treseder and Allen, 2000; Rillig et al., 2001; Rillig, 2004; Tao and Liu, 2024; Liu et al., 2025). The lack of a direct relationship may be explained by the fact that the increase in SOC due to N addition is primarily plant-originated (e.g., particulate organic C), with a smaller contribution from microbially-derived C (e.g., mineral-associated organic C) (Tang et al., 2023). Consequently, changes in AMF abundance are less likely to drive the observed SOC increase under N addition. Moreover, N application has been shown to weaken the linkage between soil C and microbes (Yang et al., 2022). Despite this weakening of direct microbial links to SOC under N addition, research suggests that AMF may still contribute to soil C sequestration indirectly. N addition can reduce C flow to belowground pools, retain more plant rhizodeposits, and decrease the rhizosphere priming effect on the decomposition of soil organic matter. Under these conditions, AMF may play a role in mediating these processes by affecting rhizodeposition and microbial activity (Treseder and Allen, 2000; Phillips et al., 2012; Zhou et al., 2020).

4.3 Limitations and implications

While our meta-analysis offers new insights into mycorrhizal responses and SOC changes under N addition, several uncertainties and limitations remain. First, the limited availability of published studies restricted our ability to explore the temporal dynamics of mycorrhizal fungi, which are likely to be highly variable (Maitra et al., 2021; Babalola et al., 2022). Second, the effects of mycorrhizal traits should consider phylogenetic non-independence (Dickie et al., 2014). Moreover, ecosystem models could benefit from more detailed representations of AMF dynamics by incorporating predictions of specific AMF taxa activity, as different taxa vary in their effects on soil processes and responses to environmental changes (Chagnon et al., 2013; Treseder, 2013; Rillig et al., 2015). Recent advancements suggest using neutral lipid fatty acid 16:1ω5 as a reliable biomarker for AMF biomass (Joergensen, 2022; Lekberg et al., 2022). Lastly, future research should prioritize developing labeling techniques that directly quantify C allocation to AMF, providing stronger evidence of their role in SOC storage.

5 Conclusions

In summary, this meta-analysis highlights the variability in mycorrhizal abundance and diversity and their potential link to SOC storage under N addition in terrestrial ecosystems. Our findings emphasize the complex, context-dependent responses of AMF to N addition, with their influence on SOC dynamics often indirect rather than direct. While N deposition significantly affects AMF abundance and soil properties, a clear and direct relationship between AM fungal traits and SOC remains elusive, pointing to the need for further exploration into the underlying mechanisms. The observed variability in AMF responses across different ecosystems, climatic conditions, and experimental factors highlights the importance of considering these factors in future studies. Given the increasing concerns about N deposition and its potential impacts on ecosystem functioning, future research should prioritize long-term, comprehensive evaluations of the role of AMF in C cycling, particularly under diverse environmental conditions. Overall, this meta-analysis suggests that N addition may lead to the decoupling of AMF and SOC storage, providing new insights into the understanding of the N deposition impacts on mycorrhizal fungi traits and soil C sequestration in terrestrial ecosystems.

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

RIGHTS & PERMISSIONS

Higher Education Press