As the largest available freshwater resource, groundwater provides water for drinking and agricultural irrigation to billions of people worldwide. Subsurface environments are estimated to host over 30% of all microorganisms on Earth, with microbial communities having important roles in various groundwater processes. Discoveries of diverse and novel lineages of archaea, bacteria, microeukaryotes and viruses in groundwater have highlighted the key contributions of groundwater microbiomes to elemental cycling, contaminant degradation, pathogenicity and antimicrobial resistance. In this Review, we summarize the diversity and composition of prokaryotic, microeukaryotic and viral communities in groundwater, and describe the complex interactions between these different microbial groups. Groundwater microbiomes exhibit distinct biogeographic patterns, with key differences and similarities across groundwater types and other habitats. The community assembly of microorganisms across different groundwater environments is driven primarily by stochastic processes, whereas deterministic processes caused by environmental stress further modulate community structure and function. With regard to their function, groundwater microbiomes have crucial roles in shaping ecosystem functioning, including biogeochemical cycling, water quality and One Health. Finally, we highlight several future prospects for research to harness microbiomes as eco-sustainable solutions for groundwater restoration and protection in a changing world. Groundwater hosts a vast array of microbiomes that are essential to global water quality and ecosystem function. This Review discusses the diversity, biogeography and community assembly of the groundwater microbiome, and explores its role in biogeochemical cycling and sustainable groundwater management.

Extracellular vesicles (EVs) mediate critical intercellular interactions, yet their special functions in anaerobic denitrification process remain poorly understood. Utilizing the model denitrifier Pseudomonas aeruginosa PAO1, we investigated how environmental oxygen and nitrate gradients reprogram vesicular cargo and functionality. Proteomic profiling revealed a clear condition-specific cargo: aerobically generated EVs selectively packaged virulence factors and nutrient acquisition proteins. In contrast, imposing severe bioenergetic stress via anaerobic denitrification forced a radical compositional inversion, driving a targeted accumulation of with peptidoglycan-degrading enzymes. Functionally, these EVs exhibited a dose-dependent duality. At physiological EV-to-cell ratios, they facilitated transient denitrification activity and early growth in recipient cohorts. Crossing a critical density threshold, however, they transitioned to cytotoxic effectors, suppressing culture density through a cytotoxic activity that emerged post-denitrification. Notably, despite carrying a full suite of denitrification enzymes, purified EVs displayed no intrinsic activity, indicating their primary roles is that of effector carriers rather than independent catalytic units. Furthermore, a substantial fraction of these bioactive nanoparticulates survived sequential multi-barrier municipal drinking water purification processes. Together, these findings redefine EVs not merely as condition-regulated ecological regulators during severe bioenergetic stress, but also as structurally recalcitrant colloidal entities within engineered aquatic environments.

Modern coexistence theory quantifies niche and fitness differences to elucidate species competition mechanisms, yet its application to temperature-driven shifts in soil microbial competitive outcomes remains limited. Here, we observed that high temperatures intensified competition among abundant bacterial genera in soil incubation experiments, particularly leading to the competitive dominance of Pseudomonas over Rhodococcus. Specifically, in competitive experiments involving Rhodococcus erythropolis NSX2 and Pseudomonas aeruginosa SB, SB successfully outcompeted NSX2, achieving a dominance of 61.6 % at 32 degrees C. This competitive dominance correlated with increased niche differences (from 0.45 to 0.88) and reduced fitness differences (from 0.83 to 0.35) at higher temperatures. Additionally, single-cell Raman spectroscopy and metabolite analysis revealed that high temperature enhanced cross-feeding, resulting in the production of more beneficial metabolites and fewer antibacterial quinolones. When metabolites served as the sole carbon source under high-temperature conditions, the growth and population density of SB were significantly promoted. These findings underscore the pivotal role of temperature in shaping soil microbial competitive dominance by regulating metabolic interactions. This study advances our understanding of soil microbial competition within the framework of modern coexistence theory. By integrating the theory with metabolic analysis, this work highlights the importance of temperature-dependent microbial interactions in changing ecosystems.

Global precipitation regimes have been shifted in recent decades, imposing significant consequences in water-limited grassland ecosystems. However, the effects of increased precipitation on the succession of soil microbial communities remain unclear, mainly due to the scarcity of long-term experiments with time-series data. Here, we examined temporal succession of grassland soil microbial communities in a long-term increased precipitation experiment. Both soil microbial taxonomic and functional structures were significantly altered by increased precipitation. Increased precipitation significantly decelerated the succession rates of soil microbial functional structure (i.e. time-decay relationships). Consistent with the increased microbial decomposition and heterotrophic respiration, the abundances of soil microbial carbon decomposition genes were markedly enhanced by increased precipitation. Furthermore, increased precipitation stimulated genes involved in nutrient cycling processes, potentially promoting plant growth. Collectively, the contributions of stochastic processes in shaping microbial communities were increased under increased precipitation, suggesting that microbial successional trajectories may shift toward multiple alternative states characterized by greater stochasticity under future altered precipitation regimes.

Soil viruses are crucial for microbial life, biogeochemical cycles of carbon and nutrients, and for microbial necromass formation. We hypothesized that the effects of viruses on these processes depend on organic matter and nutrient availability in soils. Here, we combined a 34-year long-term fertilization trial, 150 sequenced soil metagenomes, and microcosm experiments to explore how viruses modulate carbon and nutrient dynamics depending on resource availability. We uncovered 2789 viral populations (vOTUs) grouping into 301 viral clusters, 91% of which were previously unknown. Organically fertilized soils harbored most lytic viruses carrying diverse element cycling-related auxiliary viral genes (AVGs) acquired through co-evolution and horizontal gene transfer. Synthesis and heterologous expression assays further indicated that four AVGs (i.e., cbhA, pel, wbpD, GT2) had higher transcript levels in Escherichia coli under nutrient rich than nutrient poor conditions. Addition of virus particles to soils raised microbial carbon use efficiency (CUE; biomass production relative to carbon uptake) and accelerated microbial turnover leading to boosted microbial necromass formation by 14%. Conversely, in soils without organic fertilizers, viruses facilitate bacterial adaptation to stress (e.g., defense system and interference competition) and accelerate microbial decomposition of organic matter. 35 days after virus addition, CO2 and N2O emissions increased by 41% and 52%, respectively. Finally, we propose the Viral Entombing-Priming (VEP) framework to describe the contrasting roles of viruses in carbon and nutrient dynamics depending on soil fertility. This work reveals the viral "Matthew effect" (the rich get richer and the poor get poorer) in resource-rich and resource-poor soils and could unlock nature-based pathways to raise carbon and nutrient retention for sustainable agriculture.

Abstract Climate change intensifies grassland drying, which is predicted to decrease soil organic carbon (SOC) storage. Yet how reduced soil water affects the transport and processing of carbon in the rhizosphere — a major source of SOC supporting microbial activities — remains poorly resolved under field conditions. We traced living root-derived carbon (rhizodeposit C) into soils and microbes using ¹³CO₂ labeling in a multi-year precipitation manipulation experiment in a California Mediterranean annual grassland dominated by Avena barbata . Under halved precipitation, season-averaged soil water content was 20% lower and soil matric potential more than threefold lower, without inducing detectable signs of plant stress. Quantitative stable isotope probing (qSIP) of rhizosphere microbial DNA revealed that up to 68% more bacterial and 13% more fungal taxa incorporated rhizodeposit C, and that microbial uptake of rhizodeposit C increased more over time under reduced precipitation, even as total microbial biomass and community composition were unchanged. ¹³C-informed co-occurrence networks of these consumers were larger and more connected under reduced precipitation. The surrounding soils contained less 13 C, and modeled solute transport by soil water was 32-40% lower, implying that rhizodeposit C was retained and intensively processed nearer to roots rather than transported to the wider soil matrix. Our evidence supports that reduced precipitation concentrates rhizodeposit C near roots, increasing the number of distinct consumers and intensifying associations among them. This represents an overlooked mechanism linking precipitation reduction to rhizodeposit C cycling. These findings show that precipitation reduction may reshape rhizosphere C processing before apparent plant stress response, with potential consequences for the fate of rhizodeposit C in grassland soils.

Ecosystem retrogression drives nutrient depletion, reduced productivity, and profound reorganization of soil microbial communities. Using amplicon sequencing and genome-resolved metagenomics, we examined how cross-domain microbial networks and functional gene potential respond to long-term phosphorus and nitrogen limitation along the well-characterized Ecological Staircase chronosequence in Mendocino, California, USA. Microbial diversity and abundance declined sharply with terrace age for prokaryotes, predatory protists, and bacteriophages, whereas fungi and phototrophic protists increased in nutrient-depleted, acidic soils. These compositional shifts were accompanied by major changes in reconstructed microbial networks: relative modularity increased alongside robustness, indicating adaptive reorganization that may sustain ecosystem function under resource scarcity. Fungi emerged as central stabilizers in these restructured networks, carrying enriched genetic potential to degrade plant polymers and mobilize phosphorus and nitrogen. Despite a decline in overall phage diversity, the relative abundance of phages encoding phosphorus-mobilizing auxiliary metabolic genes increased, suggesting that viral contributions to host phosphorus metabolism may be enhanced under nutrient limitation. Together, these results demonstrate that ecosystem retrogression drives cross-domain microbial reorganization toward fewer but more interconnected lineages, characterized by greater integration of functional genetic potential. This reorganization enhances the potential for functional resilience under extreme nutrient limitation, revealing how microbial networks adapt to maintain the capacity for nutrient cycling and stability as soils age and fertility declines.

A key uncertainty in understanding whether warming accelerates soil carbon (C) loss lies in how this response depends on other co-occurring environmental changes and the underlying mechanisms. Here we show that, in a 12-year grassland experiment, warming reduces soil C by 12.2% under drought but increases it by 6.7% under wet conditions. Such C losses during drought primarily result from the declines in mineral-associated organic C. These contrasting responses are closely linked to microbial processes: warming elevates microbial metabolic quotient under drought but suppresses it under wet conditions, accompanied by shifts in microbial community composition and C-degrading genes. Integrating these microbial metrics into an ecosystem model substantially improves predictions of soil C dynamics. These findings demonstrate the pivotal role of microbial processes in mediating soil C-climate feedbacks and underscore their critical importance for accurately projecting soil C dynamics in a warmer, potentially drier world.

Coastal ecosystems play critical roles in biogeochemical cycling, food webs, climate regulation, and aquaculture. Their functions are shaped by multitrophic interactions across microbe-microbe, microbe-plant, and microbe-animal interfaces, yet our understanding of the underlying mechanisms remains limited. Synthetic ecology offers a promising approach to disentangle such interactions using simplified and controllable synthetic communities (SynComs). Here, we review microbe-plant-animal interactions toward ecosystem function improvements and provide a biological foundation for SynCom design. We further propose a framework for coastal synthetic ecology, including SynCom design and construction, experimental validation of SynCom functions, and laboratory scaling-up and field applications with a focus on greenhouse gas reduction, carbon sequestration, and pollutant degradation. Finally, we discuss future directions for coastal synthetic ecology, with a focus on biogeochemical cycling, food web structure and function, and biological stoichiometry. Overall, this review highlights the potential of SynComs to address environmental and ecological challenges in coastal ecosystems.

The growing global plastic waste crisis demands the development of urgent, effective, and sustainable solutions. While conventional recycling methods present intrinsic limitations, microbial biodegradation of plastic waste has emerged as a promising alternative. In this review, we explore the potential of using microorganisms to degrade major hydrocarbon-based plastic polymers and discuss key aspects of this rapidly advancing field, including (i) isolation and characterization of novel microorganisms and enzymes in hydrocarbon-based plastic biodegradation, (ii) development and streamlining of microbial consortia to improve hydrocarbon-based plastic biodegradation efficiency, and (iii) investigation of natural biodegradation processes to illustrate the relationship between plastic degradation and environmental influence. We highlight practical biotechnological approaches and advanced computational tools in hydrocarbon-based plastic degradation, as hydrocarbon-based plastic represents the highest proportion of plastic waste while still lacking effective conversion strategies. Our ultimate goal is to integrate microbial biodegradation strategies into modern waste-management systems and offer a feasible pathway toward a circular bioeconomy, one in which persistent plastic polymers are no longer treated as waste but are converted into renewable feedstocks that support sustainable resource recovery.

Cropland phosphorus (P) is essential for global food security, yet its management remains challenging owing to low phosphorus use efficiency (PUE), leading to resource depletion and nutrient loss from agricultural fields. Although a range of management practices can improve PUE, their effectiveness varies across environmental and socioeconomic contexts, and the absence of a predictive framework has hindered global assessments of their potential. Here we develop a machine learning model to map global PUE geospatial variations for maize, rice and wheat and quantify potential gains under a feasibility-constrained scenario. Our results reveal global average PUEs of 25.1% for maize, 25.0% for rice and 24.2% for wheat. Under three-layer feasibility constraints, management interventions could yield absolute PUE gains of 5.2-6.0%, with adoption barriers as the dominant limiting factor. Changes in cropping system and fertilizer type are the two largest management contributors across all three crops. Our spatially explicit framework evaluates the feasible PUE improvement potential, providing a foundation for regionally differentiated phosphorus management that supports sustainable intensification and food security.

Climate warming-induced disruptions to soil microbial communities have been shown to affect the stability of soil carbon pools within terrestrial ecosystems, yet how these shifts regulate changes in soil organic carbon (SOC) and microbial assembly remains poorly understood. Here, we collected paddy soil samples during the drained fallow phase from thirteen regions across China, and incubated them under five temperature regimens, to investigate how temperature shapes the assembly of bacterial generalists and specialists and its consequences for SOC changes. Our findings revealed a contrasting response to different thermal regimens between generalists and specialists in paddy soils. Generalists showed reduced diversity at higher static incubation temperatures, whereas specialists displayed the opposite trend. Simultaneously, a temperature-dependent divergence in assembly mechanisms between bacterial specialists and generalists, with 15 °C representing the point of maximum deterministic selection for specialists but maximum stochastic processes for generalists. Habitat generalists demonstrated greater network robustness than specialists, while functional capacities related to carbon metabolism were enhanced for both groups under different incubation temperatures. Among the bacterial properties examined, network interactions and diversity of specialists were the strongest biotic predictors of short-term SOC changes, while soil type and nutrients remained the dominant overall drivers. This study provides a mechanistic underpinning for the process of bacterial community assembly in soil carbon metabolism.

Cover crops benefit soil health by promoting microbial soil ecosystem services (SES), yet the intra- and inter-annual variability of cover crop-induced SES benefits are poorly resolved. Thus, land managers lack clarity on whether or how long SES benefits will persist after cover crop termination and how many years of practice are necessary to reap consistent SES benefits across a growing season. We addressed this in a three-year field experiment in a semi-arid California vineyard, comparing interrow spaces under Phacelia or Rye cool-season annual cover crops or bare control. Soils were sampled at three grapevine phenological stages each year, and microbial, physicochemical, and soil respiration indicators were integrated into six SES categories and combined into an integrated soil function score (ISFS) using a multi-metric SES-ISFS framework., Temporal trajectories of SES and ISFS scores revealed a clear transition from strong seasonal variability in year one, likely reflecting post-disturbance reorganization, to treatment-driven patterns in year two, and functional stabilization by year three. ISFS increased significantly under cover crops, particularly Phacelia, supported by gains in plant-growth and energy-related functions and consistent declines in mineral nitrogen pools. In contrast, bacterial and fungal communities remained dynamic across all years, although treatment-related differences became increasingly consistent., Distance-based ordination revealed that SES related to energy availability and carbon turnover were the strongest predictors of microbial community structure. Differential abundance analyses highlighted enrichment of microbial groups associated with nitrogen acquisition and decomposition under cover crops. Our findings demonstrate that cover crops can promote multi-metric functional stability despite persistent microbial community compositional turnover., By integrating diverse indicators into a unified SES-ISFS framework, this study provides a transferable approach for evaluating soil multifunctionality across seasonal and interannual timescales. From a management perspective, tailoring cover crop species or mixtures to enhance nutrient acquisition and the maintenance of key soil functions may support more stable soil functioning in water-limited perennial systems. More broadly, these results emphasize the importance of viewing soil functions as dynamic trajectories rather than static endpoints when assessing agroecosystem sustainability.

Soils are critical reservoirs of antibiotic-resistance genes (ARGs)1,2, which are strongly shaped by microbial interactions and environmental conditions and are therefore highly sensitive to disturbance2-6. Although climate warming is recognized as one of the most significant disturbances to microbial communities and their functions7-10, its impacts on soil resistomes remain poorly understood. Here we investigated the effects of decade-long experimental warming on ARGs in grassland soils using integrated experimental and computational approaches. Our results revealed that ARG abundance substantially increased (23.9%) under warming-particularly glycopeptide- and rifamycin-resistance genes. Warming specifically enriched Actinomycetota hosts, including various potential plant pathogens, and enhanced ARG mobility. Large-scale unprecedented isolates-based phenotypic analyses also validated that warming increased bacterial resistance to multiple antibiotics. Further mechanistic analyses revealed that warming increased ARG abundance primarily through co-selection of resistance genes physically linked to adaptive traits (for example, thermal tolerance and nitrogen assimilation) and positive selection for thermal tolerance genes, which could be further amplified via horizontal gene transfer. Together, these findings convincingly demonstrate that climate warming substantially accelerates soil antibiotic resistance at genomic, ecological and evolutionary levels, with broad implications for public health and environmental sustainability in a warming world.

Understanding the apparent temperature dependence of wetland methane emissions (EM) is critical for predicting climate-carbon feedbacks, yet current estimates remain constrained by observational limitations and methodological inconsistencies. The inherent biogeographic heterogeneity of wetland ecosystems combined with sparse, unevenly distributed flux measurements introduces substantial uncertainty in characterizing spatial patterns of EM. This knowledge gap impedes accurate projections of wetland methane contributions under climate warming scenarios. Here, we develop a framework that integrates mixed-effects models with artificial intelligence techniques to resolve scale-dependent patterns in methane emission thermodynamics across global wetlands. Our unified framework demonstrates that only 73.6% (5th-95th quantiles: 71.8%-75.4%) of the global wetland area conforms to classical Arrhenius-type temperature dependence. This framework can predict 69.5% (67.9%-71.1%) of the global wetlands with high confidence using the Mahalanobis distance and area of applicability tests. We quantify the weighted mean EM across high-confidence predictable areas of 0.694 eV, with latitudinal differentiation: tropical (0.634 eV), temperate (0.678 eV), and boreal (0.745 eV) wetlands exhibit progressively stronger temperature responses. Ignoring these biogeographic variations could result in underestimation of projected end-century methane emissions by 4.2%-13.3% across selected socioeconomic pathway scenarios. Our study refined the temperature sensitivity parameter in coupled climate-carbon cycle models, thereby enhancing predictive accuracy of future global warming trends and informing strategic responses to climate change mitigation.

Cover crops are widely promoted to improve soil health, yet in the case of seasonal cover crops, it is unclear how cover cropping duration and/or seasonal dynamics shape induced changes to soil microbial ecosystem services. We addressed this in a three-year field experiment in a semi-arid California vineyard, comparing interrow spaces under Phacelia or Rye cool-season annual cover crops or bare control. Soils were sampled at three grapevine phenological stages each year, and microbial, physicochemical, and soil respiration indicators were integrated into six soil ecosystem services (SES) categories and combined into an integrated soil function score (ISFS) using a novel multi-metric SES-ISFS framework., Temporal trajectories of SES and ISFS scores revealed a clear transition from strong seasonal variability in year one, likely reflecting post-disturbance reorganization, to treatment-driven patterns in year two, and functional stabilization by year three. ISFS increased significantly under cover crops, particularly Phacelia, supported by gains in plant-growth and energy-related functions and consistent declines in mineral nitrogen pools. In contrast, bacterial and fungal communities remained dynamic across all years, although treatment-related differences became increasingly consistent., Distance-based ordination showed that SES related to energy availability and carbon turnover were the strongest predictors of microbial community structure. Correlation and differential abundance analyses highlighted enrichment of microbial groups associated with nitrogen acquisition and decomposition under cover crops. Our findings demonstrate that cover crops can promote multi-metric functional stability despite persistent microbial turnover., By integrating diverse indicators into a unified SES-ISFS framework, this study provides a transferable approach for evaluating soil multifunctionality across seasonal and interannual timescales. From a management perspective, tailoring cover crop species or mixtures to enhance nutrient acquisition and stress buffering may improve resilience in water-limited perennial systems. More broadly, these results emphasize the importance of viewing soil functions as dynamic trajectories rather than static endpoints when assessing agroecosystem sustainability.

Gut metabolites and symbionts are indispensable for host health, yet the precise identification of keystone metabolites and construction of synthetic microbial communities (SynComs) to enhance disease resistance remains limited. Using Litopenaeus vannamei as a model, we identified pyruvic acid and DL-glutamine (1:2) as keystone metabolites by borrowing the microbial ecology principles of bio-indicators and driver taxa. Dietary supplementation with these metabolites sufficiently protected shrimp from white feces syndrome (WFS). Multi-omics analyses demonstrated that keystone metabolites exerted positive effects by enriching beneficial Ruegeria lacuscaerulensis, Bacillus subtilis and Nioella nitratireducens, strengthening the gut network stability, and enhancing shrimp immunity, which collectively potentiated WFS resistance. The recruited three strains were consumers and producers of the two keystone metabolites, and discriminative strains between healthy and diseased shrimp across global datasets. A SynCom constructed from the three strains (4:3:2) replicated the efficacy of keystone metabolites. Both keystone metabolites and SynCom elevated shrimp gut and hepatopancreas lipoxin A4 (LXA4) levels, which suppressed the pro-inflammatory transcription factor AP-1, as validated by in vivo inhibition assay. Our findings demonstrate that precisely designed keystone metabolites enhance shrimp disease resistance through the recruitment of key symbionts–LXA4–AP-1 axis. The rationally designed keystone metabolites and SynCom are compelling biocontrol solutions in improving host disease resistance.

Abstract. Field-warming experiments offer insight into the response of ecosystems to rising temperatures, but cross-site comparison is needed to determine both the general tendencies of warming responses and the context dependencies of deviations from those norms. These responses are not limited to the direct effects of temperature but also their indirect effects on soil moisture, a critical factor controlling ecosystem productivity and carbon fluxes. Here we introduce SWEDDIE: the first database to characterize the whole soil profile warming response across 26 distinct soil warming experiments, encompassing forest, grassland, cropland, tundra, and wetland ecosystems. SWEDDIE is needed because prior databases and syntheses of warming effects on ecosystems were dominated by aboveground warming studies, many of which warmed soil modestly or negligibly during much of the growing season and reported only growing season averages. We demonstrate the potential of the SWEDDIE database by quantifying soil temperature and moisture changes for each experiment as a function of depth, warming methodology, ambient climate conditions, and ecosystem, as well as the relationship between soil moisture and imposed warming. Warming attenuated with depth at sites with aboveground warming only but increased with depth at sites with belowground warming only, as hypothesized. Warming led to soil drying at most sites, and drying was positively correlated with the magnitude of warming. However, the relationship between soil warming and soil drying varied by ecosystem: forest soils dried the most, while tundra soils became wetter with warming. Ambient climatic conditions also significantly influenced the relationship between experimental warming and drying, with more drying per degree of warming observed in soils with higher ambient moisture. The inconsistency of soil moisture changes with warming across ecosystems and warming methodologies demonstrates the importance of quantifying shifts in temperature and moisture in both space and time in order to overcome site-specific bias in ecosystem warming responses. The high temporal resolution and depth-resolved observations of the fundamental ecosystem properties of soil temperature and moisture in SWEDDIE v1.0.0 serve as a foundation for future experimental soil warming synthesis efforts and demonstrate the power of this actively growing community resource.