Life history strategies of soil microbiomes may determine their environmental adaptability and influence soil carbon-climate feedbacks. Here, we investigate trade-offs among microbial high yield (Y), resource acquisition (A), and stress tolerance (S) strategies and their consequences for soil carbon mineralization potential along an aridity gradient spanning 9.6 million square kilometers. Y-A-S strategies show nonlinear threshold responses to aridity, where a surge in S- and A-strategies and a sharp decline in Y-strategy occur once aridity exceeds critical levels. The aridity threshold for the Y-strategy occurs after those of S- and A-strategies, as increasing carbon allocation into stress tolerance and resource acquisition comes at the expense of growth. The Y-strategy negatively impacts, while A- and S-strategies positively impact soil carbon mineralization potential. Importantly, aridification intensifies these impacts. Overall, our findings suggest that variations in microbial Y-A-S strategies significantly influence soil carbon cycling and should be considered in microbial models.
Agriculture is expected to play a significant role in supporting carbon (C) sequestration globally. Microbial carbon use efficiency (growth yield, Y-strategy) and enzyme production (resource acquisition, A-strategy) are fundamental life history traits that affect soil C balance. Yet, uncertainties persist concerning microbial adaptations to long-term fertilization and the ensuing regulation of C cycling. Here, we investigated the trade-offs between Y-strategy and A-strategy, as well as their impacts on C accumulation in red soils (C-poor) and yellow soils (C-rich) subjected to 30 years of chemical and organic fertilization. We found that long-term fertilization exerts context-dependent effects on microbial Y-strategy (growth yield) and A-strategy (resource acquisition): in red soils, microbial Y- and A-strategies exhibit a significant trade-off—microbial Y-strategy is enhanced whereas A-strategy is reduced, jointly regulating C accumulation. Conversely, in yellow soils, a synergistic trend emerges only under mineral (NPK) and organic (NPKM) fertilization, with Y-strategy alone driving C accumulation. Further analysis revealed that soil stoichiometry and microbial traits strongly account for strategy variations by driving C-stable genes across soils: in red soils, higher C:P and N:P ratios (reflecting nutrient availability) favor dominance of k-strategist Acidobacteria, strengthening microbial A-strategy by upregulating C-stable genes related to resource acquisition, which creates a marked trade-off with the Proteobacteria-dominated Y-strategy. In yellow soils, however, altered nutrient availability weakens such functional differentiation among microbial groups, dissipating the Y-A trade-off. Notably, specific fertilization (e.g., N, NPK, NPKM) drives a synergistic trend via sufficient nutrient supply. Overall, our findings suggest that trade-offs between microbial growth yield and resource acquisition govern soil organic carbon (SOC) after long-term fertilization, revising the previous assumption that a high CUE promotes microbial biomass, enzyme production, and organic matter decomposition.
Microbial physiological traits are key determinants of soil organic carbon (SOC) accumulation under long-term fertilization, yet their adaptability to carbon (C) and nutrient gradients, and the corresponding C feedback effects, remain largely unexplored. Here, we conducted a 33-year field experiment with mineral and mineral-organic combined fertilization (NPKM) across two contrasting soil types (nutrient-rich vs. nutrient-poor). The 18O-H2O tracer method and amino sugar biomarker approaches were used to explore the trends of microbial C use efficiency (CUE) and microbial C pump efficacy (MCP), while metagenomic analysis and environmental variables were integrated to clarify the intrinsic and extrinsic effects of long-term fertilization on these microbial traits. Our results revealed divergent responses of SOC fractions to NPKM across soil types: relative to the control (CK), NPKM increased particulate organic carbon (POC) by 130% in nutrient-rich soils, the 33.46% rise in mineral-associated organic carbon (MAOC); in contrast, only MAOC exhibited a significant increase (80.86%) in nutrient-poor soils. Further analysis confirmed that microbial physiological traits drove the changes in POC and MAOC depending on soil nutrient status under long-term fertilization. Specifically, in nutrient-poor soils, NPKM enhanced MAOC by increasing CUE (100%) and MCP (45.34%), an effect mediated by C-degradation functional genes. In nutrient-rich soils, NPKM promoted POC by improving CUE (48.48%), a process regulated by abiotic factors. These findings highlight that initial nutrient levels regulate microbial physiological traits, thereby dictating the accumulation dynamics of different C fractions, which offers a theoretical basis for targeted agricultural C management strategies.
Quantifying the biogeography of soil microbial carbon use efficiency (CUE) is crucial for refining terrestrial carbon cycle models and thereby enhancing predictions of soil carbon stocks. Yet systematic characterization of microbial CUE biogeographic distributions and their microbial drivers at the national scale remains limited. To address this gap, a nationwide soil survey of similar to 592 samples from diverse ecosystems across China (including agricultural, forest, grassland, and wetland soils) was conducted to investigate mechanisms driving of microbial CUE at a national scale, with the O-18-H2O tracer method applied for quantification. Results showed significant variation among ecosystems, with grasslands and forests exhibiting higher CUE than farmlands and wetlands. Further analysis of soil microbiome across the gradient of CUE revealed marked differences in the abundance patterns of bacteria and fungi: the relative abundance of bacteria positively correlated with CUE was significantly higher than that of bacteria negatively correlated with CUE, while the fungal communities exhibited the opposite pattern. Across the studied ecosystems, Acidobacteriota and Proteobacteria dominated in the bacterial communities, whereas Ascomycota was the dominant fungal phylum. The key taxonomic pattern was the contrasting abundance dynamics of microbial taxa positively and negatively correlated with CUE. Elevated bacterial alpha-diversity and community complexity were associated with higher CUE. Additional analysis elucidated the regulatory role of environmental factors in microbial CUE: soil organic carbon, pH, and aridity index modulated CUE by shaping the composition and structure of the bacterial and fungal communities. Collectively, our biogeographic analysis highlights the critical role of microbial taxonomic traits in predicting soil carbon sinks across Chinese ecosystems, offering novel insights into how climate change impacts the carbon-sequestering capacity of soil microbes.
Soil microbial heterotrophic respiration (HR), a crucial carbon flux to the atmosphere, is closely related to microbial community traits. However, community level microbial traits associated with such process remain understudied across forest biomes. Here, we accessed microbial traits influence on HR across a forest climatic gradient in China. We found that microbial HR showed distinct differentiation along an environmental gradient, which were highest in temperate forest Maoer mountain (1067.95 mg C kg−1) and lowest in tropical forest Xishuangbanna (178.83 mg C kg−1). At the community level, microbial HR was tightly related to microbial biomass and composition, and genomic traits. Notably, the HR was positively correlated with guanine-cytosine base pair content, but negatively correlated to the average 16S rRNA copy number and the average genome size of microbes (P < 0.05). Moreover, among the forests, soil organic carbon and alkyl-C/O-alkyl-C ratio were the crucial variables in explaining HR, which attributed to their effects on microbial composition and genomic traits. Overall, microbial genomic traits at the community level play an important role in understanding HR. Our findings elucidate new evidence on the mechanisms driving soil carbon fluxes and enhance predictions of soil carbon responses to future climatic change.
Soil microbially derived carbon is essential for soil carbon sequestration, yet its dynamics under organic matter addition in croplands remain poorly understood, largely owing to the interactions among microbial carbon, nitrogen, and phosphorus metabolic functions and their divergent responses to soil environmental changes. Here, based on a long-term field experiment, we investigated the effects of combined application of chemical fertilizer with straw or manure on microbially derived carbon accumulation in soils. The 18O-H2O tracer method and soil extracellular enzyme were used to quantify microbial carbon use efficiency and carbon acquisition capacity, and metagenomic sequencing was performed to determine microbial carbon, nitrogen and phosphorus functional genes, aiming to unravel the intrinsic relationship between microbial metabolism and microbially derived carbon. The results showed that, compared to the chemical fertilizer treatment, the chemical fertilizer treatments with straw or manure both significantly increased the accumulation of microbially derived carbon. Furthermore, the microbially derived carbon was significantly positively correlated with microbial carbon use efficiency but negatively correlated with carbon acquisition capacity. Specifically, chemical fertilizer treatments with straw or manure increased microbial carbon use efficiency but reduced carbon acquisition capacity, thereby shifting the microbial metabolic pattern from a "high decomposition" state to a "high utilization" state, which associated with the retention of microbially derived carbon. Correlation analysis showed that microbial carbon use efficiency was significantly positively correlated with nitrate nitrogen, SOC but negatively with microbial carbon and nitrogen functional genes (e.g., those involved in disaccharide metabolism, dissimilatory nitrate reduction, and nitrogen fixation), whereas carbon acquisition capacity exhibited the opposite pattern. Especially, the increased nitrate nitrogen and SOC under chemical fertilizer with straw or manure effectively alleviated microbial resource limitation and were negatively correlated with both nitrogen and carbon functional genes. These findings elucidate the role of nitrogen and carbon availability in regulating the relationships among microbial metabolic functions, carbon acquisition and utilization, improving our understanding of the mechanisms governing microbial-derived carbon accumulation under organic matter addition.
The synergistic optimisation of agricultural productivity enhancement and N2O emission reduction presents a core challenge in global agricultural sustainability. Integrating 792 field trials (6,678 observations) with meta-analysis and machine learning, this study evaluates nine management practices for their impacts on N2O emissions, crop yields, and yield-scaled N2O emission. Compared to standard synthetic fertilization (SY), biochar (BI), organic fertilizer substitution (OF_SY), and enhanced-efficiency nitrogen fertilizer (EENF) exhibit synergistic effects: reducing N2O emissions (15.6-32.2%), increasing yields (4.6-7.6%), and decreasing yield-scaled N2O emission (23.7-35.2%). In contrast, SY, organic fertilizers, or their combination led to a "high yield-high emission" outcome, elevating yield-scaled N2O emissions (15.7-70.5%). Global spatial projections demonstrate that optimal implementation of OF_SY (-27.6%), EENF (-45.7%), straw return (SR,-8.1%), BI (-23.9%), and reduced/no-tillage (RNT,-16.8%) concurrently enhance yields, with coordinated global deployment further reducing yield-scaled N2O emission by 46.7%. Overall, we establish a framework guiding agricultural practices to mitigate climate change.
Alpine ecosystems exhibit high vulnerability to climatic drought, with plant productivity and ecosystem resilience constrained by soil phosphorus (P) availability. However, the microbially mediated mechanisms driving drought-induced shifts in P speciation remain elusive. Here, we integrated metagenomic profiling and P fractionation across 40 sites along an aridity gradient on the Tibetan Plateau to elucidate the microbial mechanisms driving P transformation in alpine soils. Our results show that drought intensifies the loss of labile and moderately labile P, while promoting the accumulation of stable P, with microbial P-cycling genes exhibiting distinct enrichment and depletion patterns along the aridity gradient. Functionally, these genes were primarily associated with purine metabolism, organic phosphate hydrolysis, phosphate metabolism, and transport, and were closely linked to soil P pools. In particular, increased abundances of purE/S/N/P (intracellular purine synthesis) and phoX/phy (extracellular enzymatic hydrolysis) robustly predicted labile P levels, whereas pit (inorganic phosphate transporter) and phnT (phosphonate transporter) were strongly associated with stable P accumulation. These findings suggest that drought induces a microbial metabolic trade-off, whereby enzymatically released Pi is diverted into intracellular nucleotide pools via assimilation, while transporter-mediated P uptake is suppressed, thereby promoting P stabilization through organo-mineral interactions. Partial least squares path modeling (PLS-PM) further revealed that drought intensity indirectly altered ecosystem P pools through its effects on plant biomass, species richness, soil moisture, soil C:P ratio, and microbial functional gene strategies, with microbial community structure emerging as the key predictor of P pool dynamics. Overall, this study highlights the pivotal role of microbial regulation of P cycling within high-altitude cold soils and provides new insights into strategies for enhancing alpine ecosystem resilience.
Global cropland soils possess significant carbon storage potential, yet their storage efficiency is directly regulated by fertilization practices. To elucidate the impact of fertilization on soil organic carbon (SOC) in major cropland systems (paddy/upland), this study leverages a 37-year long-term field experiment. We integrate physical fractionation (particulate organic carbon (POC), mineral-associated organic carbon (MAOC)) and biomarker techniques (plant-derived carbon, microbial necromass carbon) to systematically analyze carbon pool reconfiguration pathways under four fertilization treatments: no fertilizer (CK), nitrogen-only fertilizer (N), NPK fertilizers (NPK), and combined organic-inorganic fertilization (NPKM). Key findings are as follows: NPKM significantly increased SOC by 52.6% in upland and 29.4% in paddy. In contrast, chemical-only fertilization (N/NPK) achieved no increase in carbon storage, confirming the essential role of organic carbon inputs in cropland carbon storage. In paddy soils, flooded conditions suppressed microbial decomposition and saturated the MAOC pool, leading NPKM treatment to drive preferential carbon enrichment into the POC fraction. Conversely, NPKM treatment in upland soils concurrently enhanced both POC and MAOC pools, demonstrating a synergistic dual-pool accumulation mode. NPKM induced substantial increases in plant-derived carbon (lignin phenol biomarkers) in upland (458.9%) and paddy soils (188.1%). This contributed 63.5% and 65.7% of SOC under NPKM in upland and paddy soils, respectively, highlighting its dominant contribution to SOC accumulation. NPKM treatment also increased microbial necromass carbon but shifted its composition toward fungal necromass dominance in upland soils and bacterial necromass dominance in paddy soils. In conclusion, NPKM exhibits prominent carbon storage potential in both upland and paddy systems. However, distinct carbon storage patterns emerge due to differences in water management. This necessitates targeted carbon storage strategies specifically designed for the distinctive characteristics of paddy and upland systems.
The balance of carbon (C), nitrogen (N), and phosphorus (P) stoichiometry fundamentally regulates nutrient cycling and microbial metabolism in terrestrial ecosystems. However, the mechanisms through which long-term fertilization and climate jointly shape multidimensional stoichiometric networks and microbial life history strategies remain unclear. In this study, six long-term (27-44 years) fertilization experiments across a 17 degrees latitudinal gradient in China were examined under three treatments: no fertilizer (CK), mineral fertilizer (CF), and mineral plus manure fertilizer (CFM). By integrating ecological stoichiometry with metagenomic approaches, this study assessed how fertilization and climate affect soil, resource, microbial, and enzyme stoichiometry, and how these stoichiometric shifts influence microbial life history strategies. Results showed that long-term fertilization altered stoichiometric patterns, strengthening network connectivity among soil, resource, microbial, and enzymatic stoichiometry. CFM reduced soil and microbial C:P and N:P ratios by 35-70 % and decreased DOC:Olsen-P and DON:Olsen-P by up to 95 %. These shifts restructured microbial life history strategies, promoting a transition from resource acquisition (A) to growth yield (Y) strategies, with Y strategists increasing to 45-56 % under fertilization. Moreover, available resource and microbial stoichiometry, particularly DOC:Olsen-P and DON:Olsen-P ratios, were the primary predictors of microbial strategies, linking stoichiometric balance to microbial energetic allocation. Fertilization and climate jointly regulated microbial life history strategies by alleviating C:P and N:P imbalances and promoting stoichiometric homeostasis. Overall, these findings establish a mechanistic framework connecting nutrient supply, stoichiometric regulation, and microbial adaptation, thereby providing theoretical guidance for optimizing fertilization practices and maintaining soil nutrient sustainability across climatic regions.
The magnitude and persistence of soil organic carbon (SOC) are governed by its microbial carbon use efficiency (CUE) and microbial necromass (MNC). However, whether long-term mineral fertilization builds microbially derived SOC via shared or system-specific mechanisms in paddy versus upland areas remains unresolved. For this study, two >30-year field experiments involving paddies and uplands were conducted under four fertilization treatments (no fertilizer (CK), balanced mineral nitrogen, phosphorous, and potassium (NPK), manure (M), and NPK combined with manure (NPKM)). The application of NPK and NPKM in the uplands significantly increased CUE by 35.4% and 19.9%, respectively, compared with the CK and M. No significant differences in these parameters were observed in the paddies. The enhancing effects of NPK on the upland CUE were associated with the increased availability of soil phosphorus and sustained carbon-degradation capacities, while the anaerobic conditions of the paddy soils under NPK reduced its functional responses. The CUE was positively associated with MNC across both land-use types, but the relationship was significantly stronger in paddy soils (slope = 24.17) than in upland soils (slope = 11.81). In paddy soils, the relationship between CUE and fungal necromass was stronger (slope = 18.87) than that with bacterial necromass (slope = 5.30). These results demonstrated that mineral fertilization affects microbially derived soil organic carbon through land-use–specific mechanisms, which advocates for fertilization strategies that are tailored to hydrologic and phosphorus constraints.
Dormancy, as a microbial survival strategy, plays a crucial role in sustaining microbial diversity. However, the large-scale distribution patterns of microbial dormancy and drivers remain poorly understood. Here, we analyzed 591 soil samples from 197 field sites across China, spanning deserts, croplands, grasslands, and forests, to quantify the proportion of dormant microbial cells (Dormancy%). On average, 95.48% of soil microbial cells were dormant, with the lowest Dormancy% in forests (93.84%) and the highest in deserts (96.81%). This regulation followed a regular mechanism: soil water-holding capacity and beta-1,4-glucosidase activity acted as immediate triggers, while mineral-associated organic carbon, dissolved organic carbon and microbial biomass carbon indirectly governed the process. Overall, this study provides evidence at the China scale for the dominance of dormant microorganisms in terrestrial ecosystems and reveals the environmental regulatory mechanism of dormancy, highlighting its ecological importance for maintaining microbial diversity and ecosystem stability.
Soil salinization is one of the most severe forms of land degradation in arid and semi-arid regions, posing substantial threats to agroecosystem stability and food security. In this study, saline-alkali soil collected from the Wuding River Basin in Yulin, Shaanxi Province was used to construct a three-factor amendment system comprising superabsorbent polymers (SAP), biochar, and humic acid. A systematic assessment was conducted to elucidate their combined effects on soil water-salt transport and crop growth. Results from one-dimensional constant-head infiltration experiments using indoor soil columns demonstrated that the application of amendments significantly increased cumulative infiltration and improved the uniformity of wetting-front advancement. Specifically, the treatments regulated the redistribution of salts within the soil profile; while surface salinity reduction varied, the leaching efficiency was significantly enhanced in the A2B2C2 treatment. Soil bulk density (BD) showed dynamic fluctuations during the growth cycle, peaking at 1.628 cm-3 during the branching stage, while high-rate biochar (A3) reduced BD by up to 13.64% compared to the control by the initial flowering stage. Fitting results based on the Philip and Kostiakov models further indicated that the combined amendment strategy-particularly the A2B2C2 treatment (30 kg/ha SAP, 15,000 kg/ha biochar, and 600 kg/ha humic acid)-markedly enhanced both the initial infiltration rate and the steady infiltration capacity. Field experiments corroborated the indoor findings: plant height and dry biomass of Melilotus officinalis (L.)Lam. were significantly higher under amendment treatments than in the control, driven by improved water availability, mitigated salt stress, and enhanced soil structure. Single-factor and multi-factor interaction analyses revealed that SAP exerted pronounced effects during early growth stages, whereas biochar and humic acid contributed more substantially during the middle to late stages through sustained regulatory functions. Collectively, the results demonstrate that the combined application of SAP, biochar, and humic acid improves the water-salt regime of saline-alkali soils through a coupled "water-salt-structure-plant" mechanism, ultimately enhancing crop productivity. This study provides both theoretical insights and practical guidance for the amelioration of saline-alkali soils.
Although soil fungi play a crucial role in straw decomposition, mineralization, nutrient cycling, and soil fertility, soil nitrogen and carbon stoichiometry across crop growth stages under long-term straw retention and wheat-soybean rotation remains poorly understood. We assessed the dynamic changes in soil fungal communities under no straw (NS) retention, half straw (HS) retention, and total straw (TS) retention in winter wheat and summer soybean rotation. Compared with the NS treatment, average total nitrogen (TN) increased by 11.86% and 17.71% and mean soil organic carbon (SOC) increased by 4.10% and 13.08% under the HS and TS treatments, respectively. NO3--N/TN and microbial biomass nitrogen (MBN)/TN ratios increased with the increase in straw retention; NH4+-N/TN and dissolved organic carbon/SOC ratios decreased. Microbial biomass carbon (MBC)/SOC increased and subsequently decreased as straw retention increased. The mean soil C:N ratio increased, and the MBC/MBN ratio decreased as straw retention increased. Crop growth stage and straw retention treatments significantly influenced soil fungal diversity and abundance; while they did not induce changes in the dominant species, they affected relative abundance. Soil fungal relative abundance and community dynamics were more sensitive to crop growth than to straw retention treatments. Mantel's r statistic and Pearson correlation coefficient suggest that soil chemical stoichiometric ratios are useful indicators of relationships among the fungal community, soil nutrient status, and crop cultivation. Therefore, straw retention may be suitable for long-term wheat-soybean rotation.
Agricultural management is critical in shaping soil carbon (C) stocks, pools and fluxes. The soil priming effect (PE) is known as a key component of the global C cycle that reflects alterations in soil organic carbon (SOC) mineralization induced by fresh C inputs. Here, we show that priming can help to predict soil C content across European Long-Term Experiments (LTEs), a result which was maintained at continental and global scales. Results reveal that lower-intensity management significantly enhances PE in soils from European croplands. Conversely, high-intensity management led to lower or even negative PE. Management intensity influences PE directly through alterations in SOC and indirectly by modifying aggregates stability and microbial biomass. Both fertilization and tillage affect PE, with soils under organic fertilization and no-tillage showing higher values of PE. These findings advance our understanding of the long-term impacts of agricultural management on the C cycle at the continental scale.
Glomalin-related soil protein (GRSP), a key glycoprotein metabolite of arbuscular mycorrhizal fungi (AMF), plays a central role in soil carbon and nitrogen sequestration and aggregate stability. However, a systematic understanding of its response patterns and driving mechanisms under diverse global change factors (GCFs) remains limited. This study conducted a global meta-analysis to assess the effects of 14 GCFs (including land-use conversion, fertilization, and climate change) on the two GRSP fractions: easily extractable GRSP (EE-GRSP) and total GRSP (T-GRSP). The results demonstrated that T-GRSP exhibited more pronounced responses to GCFs than EE-GRSP, making it a superior indicator for characterizing long-term changes. Specifically, fertilization (nitrogen +28%; phosphorus +12%; nitrogen and phosphorus +44%; nitrogen, phosphorus and potassium +33%) and elevated CO2 (eCO2 +7%) significantly promoted T-GRSP accumulation (all relative to control, p < 0.05). In contrast, land-use conversions such as forest to bare land (-91%), farmland (-33%), shrubland (-36%), and grassland to farmland (-43%) significantly reduced T-GRSP. Warming, fire, and forest-to-grassland conversion showed no significant effects. Soil pH change was identified as the pivotal hub regulating GRSP responses to GCFs, governing GRSP accumulation dynamics by influencing its mineral adsorption and microbial decomposition. Furthermore, changes in T-GRSP were tightly coupled with soil organic carbon (SOC) and total nitrogen (TN), directly contributing to the stable C and N pool and indirectly enhancing physical protection through promoting aggregate formation. Notably, under climate change, the relationship between SOC, TN and T-GRSP showed "decoupling". Concurrently, a significant negative correlation emerged between the proportion of T-GRSP in SOC, TN and their actual contents, revealing an adaptive strategy in which T-GRSP serves as a stable component for "core protection". This study systematically elucidates the response patterns and mechanisms of GRSP to global change, highlighting its dual role in maintaining the stability of soil carbon and nitrogen pools.