Nitrogen biogeochemical cycling in forest ecosystems with the globalization of nitrogen deposition

Xiankai Lu; Xiaomin Zhu; Weibin Chen; Yushu Gao; Abdoul Kader Mounkaila Hamani; Lasisi Hammed Tobiloba; Nazar Abbas; Junbing Bai; Zhihao Qiu; Jun Pan; Nimra Maqsood; Zebing Xiao; Yingxue Xuan; Jiangming Mo; Xiankai Lu; Xiaomin Zhu; Weibin Chen; Yushu Gao; Abdoul Kader Mounkaila Hamani; Lasisi Hammed Tobiloba; Nazar Abbas; Junbing Bai; Zhihao Qiu; Jun Pan; Nimra Maqsood; Zebing Xiao; Yingxue Xuan; Jiangming Mo

doi:10.48130/nc-0026-0002

Figures (5) Tables (4)

Figure 1.
Trends in world population and nitrogen deposition flux of world and in China. Data are cited from^{[14,19,124,125]}.
Figure 2.
Key soil gross N transformation and N cycle-associated microbial functional genes.
Figure 3.
Global patterns of SOC, TN, C/N ratio, available N, microbial biomass, and N transformation rates in (a) tropical, (b) subtropical, and (c) temperate forest soils. The red and blue line represents the processes of soil N production and retention, respectively. The thickness of line and arrows refers to the degree of each N transformation rate. GNM, gross N mineralization; GN, gross nitrification; GHN, gross heterotrophic nitrification; GAN, gross autotrophic nitrification; I_NH4, microbial NH₄⁺ immobilization; I_NO3, microbial NO₃⁻ immobilization; DEN, denitrification; MBC, microbial biomass carbon; MBN, microbial biomass nitrogen. SOC, soil organic carbon; NH₄⁺, extractable ammonium; NO₃⁻, extractable nitrate. SOC: g kg⁻¹, TN: g kg⁻¹, NH₄⁺: mg kg⁻¹, NO₃⁻: mg kg⁻¹, MBC and MBN: mg kg⁻¹; GNM, I_NH4, GN (GAN+GHN), I_NO3, DNRA and DEN: mg kg⁻¹day⁻¹. Data are cited from ^{[54,126−133]}.
Figure 4.
The general pattern on the responses of soil microbes-driven gross N transformation to elevated N deposition in forest ecosystems. Red arrows indicate that N deposition exerts stimulatory effects on N pool size, N transformation processes, and associated fluxes, whereas gray arrows represent inhibitory effects of N deposition on these aspects. 'x' symbols denote uncertain effects under N addition.
Figure 5.
Historical perspective on nitrogen biogeochemical cycling.

Region	Estimated total deposition (kg N ha⁻¹ yr⁻¹)	Main forms (NH_x/NO_γ)	Critical load exceedance (% of area)	Ref.
Europe	~10–20 (temperate)	~60% NH₄⁺/40% NO₃⁻	~40% of the forest area	[134]
North America	~5–15 (variable)	Increasing NH_x fraction	~25% of the forest area	[135]
East and South Asia	~15–40 (hotspots > 30)	NH_x dominated in some sites	~60%–70% in hotspot zones	[14]
Sub-Saharan Africa	~2–8 (less measured)	NH_x emerging	Unknown/limited data	[14]
Global average	~8	NH_x:NO_y = 1.5:1	Limited data	[14]
Data compiled from recent monitoring and modelling syntheses.

Table 1.

Selected continental-scale nitrogen deposition fluxes and exceedance of critical loads

Process	Description/transformation	Key controlling factors	Representative indicators/measurements
Biological N₂ fixation (BNF)	Conversion of atmospheric N₂ → NH₃ by diazotrophs or symbiotic bacteria	Soil P and Mo availability, temperature, moisture, and vegetation type	Acetylene-reduction, ¹⁵N₂ tracer, δ¹⁵N natural abundance
Mineralization (ammonification)	Organic N → NH₄⁺	C : N ratio, microbial biomass, temperature	NH₄⁺ flux, gross mineralization (¹⁵N pool dilution)
Nitrification	NH₄⁺ → NO₂⁻ → NO₃⁻ (by AOB/AOA)	O₂ availability, pH, temperature	NO₃⁻ production, nitrifier gene abundance (amoA)
Denitrification	NO₃⁻ → NO → N₂O → N₂ under anoxia	Soil moisture, C availability, redox potential	N₂O/N₂ flux ratios (¹⁵N gas tracing)
DNRA/Anammox	NO₃⁻ → NH₄⁺ (retention)/NH₄⁺ + NO₂⁻ → N₂ (loss)	Organic C : NO₃⁻ ratio, anaerobiosis	Isotope pairing, ¹⁵N mass balance
Plant uptake and resorption	Root/fungal uptake of NH₄⁺, NO₃⁻, or DON; N resorption from senescent leaves	Root traits, mycorrhizae, soil N form availability	Leaf/root N content, resorption efficiency
Leaching and gaseous losses	Export of NO₃⁻/DON; emission of NO, N₂O, N₂	Rainfall, texture, drainage, and land use	Stream NO₃⁻, N₂O flux, NO emission

Table 2.

Major nitrogen cycling processes in terrestrial ecosystems, their controlling factors, and representative indicators

N deposition/experiment	N form studied	Findings from studies	Future implications	Ref.
Atmospheric N deposition	NH₄⁺, NO₃⁻	Elevated N deposition increased both NH₄⁺ and NO₃⁻ concentrations in forest soils in the Netherlands forest	Prolonged N loading may lead to N saturation and enhanced nitrate leaching	[30,136]
Atmospheric N deposition (linked to urban/industrial regions)	NH₄⁺, NO₃⁻	Increased soil available nitrogen (mainly NH₄⁺ and NO₃⁻), especially in areas with higher population density and industrialization	Continued emissions may accelerate soil N enrichment and N loss in urban ecosystems	[8,30,31,38]
Atmospheric N deposition	NH₄⁺, NO₃⁻	Chronic high N inputs lead to N saturation and elevated nitrate leaching	Long-term high N deposition disrupts nutrient cycling and soil carbon stability	[32]
Atmospheric N deposition	TN, NH₄⁺, NO₃⁻	Enrichment of total and available inorganic N, accelerating nitrogen cycling and altering soil chemistry even at low deposition rates	Alters ecosystem structure and functioning, e.g., species composition and productivity	[33]
Long-term N deposition	TN, NH₄⁺, NO₃⁻	Significantly higher total and available inorganic N in monsoon evergreen broadleaved forest than in younger successional forests	Indicates older forests accumulate more inorganic N, reflecting stage-dependent N retention	[137]
Atmospheric N deposition	NH₄⁺, NO₃⁻	Enhanced inorganic N quantity and mobility through stimulated mineralization and transformation; older stands showed higher inorganic N fluxes	Ecosystems are still efficient in N retention, but may reach N saturation with continued inputs	[138]
Atmospheric N deposition in Central African tropical forests	DON, NH₄⁺, NO₃⁻	Lowland forests lost N mainly as DON, others as inorganic N; tight N cycling but growing input-output imbalance	Potential for future N saturation or shifts in dominant N forms	[2,35]
Meta-analysis of N deposition studies	NH₄⁺, NO₃⁻	Enhanced mineralization and nitrification increased inorganic N availability and possible N losses	Broad-scale acceleration of N cycling and potential for increased N leaching	[9]
Long-term ammonium nitrate deposition	NH₄⁺, NO₃⁻	Despite long-term deposition, NH₄⁺ and NO₃⁻ remained stable, indicating strong N limitation and ecosystem resilience	Boreal forests remain resistant to N saturation, unlike temperate/tropical systems	[36]

Table 3.

Effects of elevated nitrogen deposition on ecosystem nitrogen forms in forests

Controlling factor	Mechanism of action	Main affected systems	Adaptive responses
Iron deficiency	Limited synthesis of nitrogenase cofactors	Marine systems, calcareous soils	Increased secretion of iron chelators
Phosphorus deficiency	Inadequate ATP supply, constrained energy metabolism	Tropical soils, lateritic soils	Enhanced phosphatase activity, increased phosphorus uptake
Molybdenum limitation	Impaired function of iron-molybdenum cofactors	Acidic soils, marine environments	Alternative pathways (e.g., using iron-vanadium nitrogenase)
Oxygen sensitivity	Nitrogenase deactivation	Aerobic environments	Formation of heterocysts, increased respiration, spatial-temporal separation
Carbon limitation	Insufficient energy supply	Barren soils, deep-sea environments	Symbiosis with photosynthetic organisms, utilization of organic carbon

Table 4.

Limiting factors of biological nitrogen fixation