Nitrate Thresholds Control Regime Shifts in Soil Nitrogen Cycling Across a Mangrove–Agricultural Gradient

ABSTRACT

Anthropogenic nitrogen inputs are increasing globally, while the conditions under which ecosystems transition from nitrogen retention to nitrogen loss remain poorly constrained. Environmental proxies commonly used to infer nitrogen loss, including redox status, carbon availability, and microbial gene inventories, provide limited power to predict when nitrate‐reduction pathways are expressed at the ecosystem scale. This limitation is particularly evident in coastal mangrove soils, where anaerobic and carbon‐rich conditions coexist with weak nitrate‐reduction activity. Here, we investigate nitrogen‐cycle organization along a spatially compressed mangrove–agricultural gradient on a Caribbean island by combining soil nitrogen pools, organic nitrogen isotopes (δ ¹⁵ N), inferred microbial metabolic functions putatively related to the microbial community (16S rDNA metabarcoding analysis), and controlled anoxic nitrate‐amended incubations. Across distances of less than 500 m, soils transitioned sharply from nitrogen‐rich, isotopically depleted mangrove sediments (total N up to 1.4%; δ ¹⁵ N≈2‰–3‰) to nitrogen‐poor, isotopically enriched agricultural soils (total N≈0.2%–0.6%; δ ¹⁵ N≈6‰–8‰). Despite widespread microbial functional potential associated with nitrate reduction throughout the transect, nitrate depletion under anoxic conditions remained slow in mangrove and back‐mangrove soils (0.56–1.15 nmol g ⁻¹  min ⁻¹ ) but was more than threefold faster in agricultural soils (2.32 nmol g ⁻¹  min ⁻¹ ). To integrate these long‐term isotopic and stoichiometric signals, we developed the Organic Nitrogen Index coupled to soil C/N ratios (ONI‐CN), an isotopic–stoichiometric framework combining δ ¹⁵ N and soil C/N ratios. Along the studied transects, ONI‐CN captured a sharp transition between two nitrogen‐cycle configurations, with mangrove and back‐mangrove soils clustering within a closed, recycling‐dominated state and agricultural soils in an open, loss‐dominated state, with no intermediate values. These observations support the interpretation that nitrate availability constrains the long‐term expression of nitrate‐loss pathways across the mangrove–agricultural gradient. The results are consistent with the presence of a functional nitrogen bank in mangrove soils, in which microbial nitrate reduction potential remains weakly expressed under chronically nitrate‐limited conditions. This framework highlights the sensitivity of nitrogen‐limited coastal ecosystems to increasing anthropogenic nitrate inputs and provides a conceptual basis for understanding threshold‐like reorganizations of nitrogen cycling under environmental changes.