Size exclusion experiment in a grassland field unravels top-down control of the soil fauna on microbial community assembly.

Highly diverse and abundant organisms coexist in soils. However, the contribution of biotic interactions between soil organisms to microbial community assembly remains to be explored. Here, we assess the extent to which soil fauna can shape microbial community assembly using an exclusion experiment in a grassland field to sort soil biota based on body size. After 1 year, the exclusion of larger fauna favoured phagotrophic protists, with increases up to 32% in their proportion compared to the no-mesh treatment. In contrast, members of the bacterial community and to a lesser extent of the fungal community were negatively impacted. Shifts in bacterial but not in fungal communities were best explained by the response of the protistan community to exclusion. Our findings provide empirical evidence of top-down control on the soil microbial communities and underline the importance of integrating higher trophic levels for a better understanding of the soil microbiome assembly.

The impact of agricultural management on soil aggregation and carbon storage is regulated by climatic thresholds across a 3000 km European gradient.

Organic carbon and aggregate stability are key features of soil quality and are important to consider when evaluating the potential of agricultural soils as carbon sinks. However, we lack a comprehensive understanding of how soil organic carbon (SOC) and aggregate stability respond to agricultural management across wide environmental gradients. Here, we assessed the impact of climatic factors, soil properties and agricultural management (including land use, crop cover, crop diversity, organic fertilization, and management intensity) on SOC and the mean weight diameter of soil aggregates, commonly used as an indicator for soil aggregate stability, across a 3000 km European gradient. Soil aggregate stability (-56%) and SOC stocks (-35%) in the topsoil (20 cm) were lower in croplands compared with neighboring grassland sites (uncropped sites with perennial vegetation and little or no external inputs). Land use and aridity were strong drivers of soil aggregation explaining 33% and 20% of the variation, respectively. SOC stocks were best explained by calcium content (20% of explained variation) followed by aridity (15%) and mean annual temperature (10%). We also found a threshold-like pattern for SOC stocks and aggregate stability in response to aridity, with lower values at sites with higher aridity. The impact of crop management on aggregate stability and SOC stocks appeared to be regulated by these thresholds, with more pronounced positive effects of crop diversity and more severe negative effects of crop management intensity in nondryland compared with dryland regions. We link the higher sensitivity of SOC stocks and aggregate stability in nondryland regions to a higher climatic potential for aggregate-mediated SOC stabilization. The presented findings are relevant for improving predictions of management effects on soil structure and C storage and highlight the need for site-specific agri-environmental policies to improve soil quality and C sequestration.

Artificial selection of stable rhizosphere microbiota leads to heritable plant phenotype changes.

Artificial selection of microbiota opens new avenues for improving plants. However, reported results lack consistency. We hypothesised that the success in artificial selection of microbiota depends on the stabilisation of community structure. In a ten-generation experiment involving 1,800 plants, we selected rhizosphere microbiota of Brachypodium distachyon associated with high or low leaf greenness, a proxy of plant performance. The microbiota structure showed strong fluctuations during an initial transitory phase, with no detectable leaf greenness heritability. After five generations, the microbiota structure stabilised, concomitantly with heritability in leaf greenness. Selection, initially ineffective, did successfully alter the selected property as intended, especially for high selection. We show a remarkable correlation between the variability in plant traits and selected microbiota structures, revealing two distinct sub-communities associated with high or low leaf greenness, whose abundance was significantly steered by directional selection. Understanding microbiota structure stabilisation will improve the reliability of artificial microbiota selection.

Diversity of archaea and niche preferences among putative ammonia-oxidizing Nitrososphaeria dominating across European arable soils.

Archaeal communities in arable soils are dominated by Nitrososphaeria, a class within Thaumarchaeota comprising all known ammonia-oxidizing archaea (AOA). AOA are key players in the nitrogen cycle and defining their niche specialization can help predicting effects of environmental change on these communities. However, hierarchical effects of environmental filters on AOA and the delineation of niche preferences of nitrososphaerial lineages remain poorly understood. We used phylogenetic information at fine scale and machine learning approaches to identify climatic, edaphic and geomorphological drivers of Nitrososphaeria and other archaea along a 3000 km European gradient. Only limited insights into the ecology of the low-abundant archaeal classes could be inferred, but our analyses underlined the multifactorial nature of niche differentiation within Nitrososphaeria. Mean annual temperature, C:N ratio and pH were the best predictors of their diversity, evenness and distribution. Thresholds in the predictions could be defined for C:N ratio and cation exchange capacity. Furthermore, multiple, independent and recent specializations to soil pH were detected in the Nitrososphaeria phylogeny. The coexistence of widespread ecophysiological differences between closely related soil Nitrososphaeria highlights that their ecology is best studied at fine phylogenetic scale.

Differential response of N2O emissions, N2O-producing and N2O-reducing bacteria to varying tetracycline doses in fertilized soil.

Tetracyclines are the most widely used antibiotics worldwide. Their presence in soils could affect nutrient cycling, but our knowledge regarding how they affect soil microbial communities involved in greenhouse gas emissions is limited. The objective of the current study was to evaluate how tetracycline is affecting N2O emissions and the abundance of denitrifiers in fertilized soil. For this purpose, soil mesocosms were treated with only NH4NO3 (100 mg/kg) or NH4NO3 (100 mg/kg) plus three different doses of tetracycline (0.1, 0.5 and 2 mg/kg). Soils that did not receive tetracycline or NH4NO3 were used as controls. Nitrous oxide fluxes were monitored daily for 16 days. The total bacterial (16S rRNA), the abundance of N2O-reducing and -producing bacteria were quantified by qPCR at the end of the experiment. The application of NH4NO3 caused a significant increase of N2O emissions and AOB abundance but did not affect the abundance of denitrifiers and AOA compared to control soils. Different doses of tetracycline in fertilized soils did not mitigate these N2O emissions; instead, higher cumulative emissions were noticed in soils treated with the lowest dose. In these soils the total bacterial abundance was higher compared to soils received higher tetracycline concentration. The abundances of the N2O-producing and N2O-reducing communities were also differently affected by the addition of tetracycline, which was dose-dependent. Higher doses of tetracycline favored N2O-reducers within the total bacterial community, which could be important for mitigating N2O emissions in the long term.

Ecotoxicological risk assessment of wastewater irrigation on soil microorganisms: Fate and impact of wastewater-borne micropollutants in lettuce-soil system.

The implementation of the new Water Reuse regulation in the European Union brings to the forefront the need to evaluate the risks of using wastewater for crop irrigation. Here, a two-tier ecotoxicological risk assessment was performed to evaluate the fate of wastewater-borne micropollutants in soil and their ecotoxicological impact on plants and soil microorganisms. To this end, two successive cultivation campaigns of lettuces were irrigated with wastewater (at agronomical dose (not spiked) and spiked with a mixture of 14 pharmaceuticals at 10 and 100 µg/L each) in a controlled greenhouse experiment. Over the two cultivation campaigns, an accumulation of PPCPs was observed in soil microcosms irrigated with wastewater spiked with 100 µg/L of PPCPs with the highest concentrations detected for clarithromycin, hydrochlorothiazide, citalopram, climbazole and carbamazepine. The abundance of bacterial and fungal communities remained stable over the two cultivation campaigns and was not affected by any of the irrigation regimes applied. Similarly, no changes were observed in the abundance of ammonium oxidizing archaea (AOA) and bacteria (AOB), nor in clade A of commamox no matter the cultivation campaign or the irrigation regime considered. Only a slight increase was detected in clade B of commamox bacteria after the second cultivation campaign. Sulfamethoxazole-resistant and -degrading bacteria were not impacted either. The irrigation regimes had only a limited effect on the bacterial evenness. However, in response to wastewater irrigation the structure of soil bacterial community significantly changed the relative abundance of Acidobacteria, Chloroflexi, Verrucomicrobia, Beta-, Gamma- and Deltaprotebacteria. Twenty-eight operational taxonomic units (OTUs) were identified as responsible for the changes observed within the bacterial communities of soils irrigated with wastewater or with water. Interestingly, the relative abundance of these OTUs was similar in soils irrigated with either spiked or non-spiked irrigation solutions. This indicates that under both agronomical and worst-case scenario the mixture of fourteen PPCPs had no effect on soil bacterial community.

Physiological significance of pedospheric nitric oxide for root growth, development and organismic interactions.

Nitric oxide (NO) is essential for plant growth and development, as well as interactions with abiotic and biotic environments. Its importance for multiple functions in plants means that tight regulation of NO concentrations is required. This is of particular significance in roots, where NO signalling is involved in processes, such as root growth, lateral root formation, nutrient acquisition, heavy metal homeostasis, symbiotic nitrogen fixation and root-mycorrhizal fungi interactions. The NO signal can also be produced in high levels by microbial processes in the rhizosphere, further impacting root processes. To explore these interesting interactions, in the present review, we firstly summarize current knowledge of physiological processes of NO production and consumption in roots and, thereafter, of processes involved in NO homeostasis in root cells with particular emphasis on root growth, development, nutrient acquisition, environmental stresses and organismic interactions.

Leaf-cutter ants engineer large nitrous oxide hot spots in tropical forests.

Though tropical forest ecosystems are among the largest natural sources of the potent greenhouse gas nitrous oxide (N2O), the spatial distribution of emissions across landscapes is often poorly resolved. Leaf cutter ants (LCA; Atta and Acromyrmex, Myrmicinae) are dominant herbivores throughout Central and South America, and influence multiple aspects of forest structure and function. In particular, their foraging creates spatial heterogeneity by concentrating large quantities of organic matter (including nitrogen, N) from the surrounding canopy into their colonies, and ultimately into colony refuse dumps. Here, we demonstrate that refuse piles created by LCA species Atta colombica in tropical rainforests of Costa Rica provide ideal conditions for extremely high rates of N2O production (high microbial biomass, potential denitrification enzyme activity, N content and anoxia) and may represent an unappreciated source of heterogeneity in tropical forest N2O emissions. Average instantaneous refuse pile N2O fluxes surpassed background emissions by more than three orders of magnitude (in some cases exceeding 80 000 µg N2O-N m-2 h-1) and generating fluxes comparable to or greater than those produced by engineered systems such as wastewater treatment tanks. Refuse-concentrating Atta species are ubiquitous in tropical forests, pastures and production ecosystems, and increase density strongly in response to disturbance. As such, LCA colonies may represent an unrecognized greenhouse gas point source throughout the Neotropics.

Remotely sensed canopy nitrogen correlates with nitrous oxide emissions in a lowland tropical rainforest.

Tropical forests exhibit significant heterogeneity in plant functional and chemical traits that may contribute to spatial patterns of key soil biogeochemical processes, such as carbon storage and greenhouse gas emissions. Although tropical forests are the largest ecosystem source of nitrous oxide (N2 O), drivers of spatial patterns within forests are poorly resolved. Here, we show that local variation in canopy foliar N, mapped by remote-sensing image spectroscopy, correlates with patterns of soil N2 O emission from a lowland tropical rainforest. We identified ten 0.25 ha plots (assemblages of 40-70 individual trees) in which average remotely-sensed canopy N fell above or below the regional mean. The plots were located on a single minimally-dissected terrace (<1 km2 ) where soil type, vegetation structure and climatic conditions were relatively constant. We measured N2 O fluxes monthly for 1 yr and found that high canopy N species assemblages had on average three-fold higher total mean N2 O fluxes than nearby lower canopy N areas. These differences are consistent with strong differences in litter stoichiometry, nitrification rates and soil nitrate concentrations. Canopy N status was also associated with microbial community characteristics: lower canopy N plots had two-fold greater soil fungal to bacterial ratios and a significantly lower abundance of ammonia-oxidizing archaea, although genes associated with denitrification (nirS, nirK, nosZ) showed no relationship with N2 O flux. Overall, landscape emissions from this ecosystem are at the lowest end of the spectrum reported for tropical forests, consist with multiple metrics indicating that these highly productive forests retain N tightly and have low plant-available losses. These data point to connections between canopy and soil processes that have largely been overlooked as a driver of denitrification. Defining relationships between remotely-sensed plant traits and soil processes offers the chance to map these processes at large scales, potentially increasing our ability to predict N2 O emissions in heterogeneous landscapes.

Peaks of in situ N2 O emissions are influenced by N2 O-producing and reducing microbial communities across arable soils.

Agriculture is the main source of terrestrial N2 O emissions, a potent greenhouse gas and the main cause of ozone depletion. The reduction of N2 O into N2 by microorganisms carrying the nitrous oxide reductase gene (nosZ) is the only known biological process eliminating this greenhouse gas. Recent studies showed that a previously unknown clade of N2 O-reducers (nosZII) was related to the potential capacity of the soil to act as a N2 O sink. However, little is known about how this group responds to different agricultural practices. Here, we investigated how N2 O-producers and N2 O-reducers were affected by agricultural practices across a range of cropping systems in order to evaluate the consequences for N2 O emissions. The abundance of both ammonia-oxidizers and denitrifiers was quantified by real-time qPCR, and the diversity of nosZ clades was determined by 454 pyrosequencing. Denitrification and nitrification potential activities as well as in situ N2 O emissions were also assessed. Overall, greatest differences in microbial activity, diversity, and abundance were observed between sites rather than between agricultural practices at each site. To better understand the contribution of abiotic and biotic factors to the in situ N2 O emissions, we subdivided more than 59,000 field measurements into fractions from low to high rates. We found that the low N2 O emission rates were mainly explained by variation in soil properties (up to 59%), while the high rates were explained by variation in abundance and diversity of microbial communities (up to 68%). Notably, the diversity of the nosZII clade but not of the nosZI clade was important to explain the variation of in situ N2 O emissions. Altogether, these results lay the foundation for a better understanding of the response of N2 O-reducing bacteria to agricultural practices and how it may ultimately affect N2 O emissions.

Spatio-Temporal Variations in the Abundance and Structure of Denitrifier Communities in Sediments Differing in Nitrate Content.

Spatial and temporal variations related to hydric seasonality in abundance and diversity of denitrifier communities were examined in sediments taken from two sites differing in nitrate concentration along a stream Doñana National Park during a 3-year study. We found a positive relationship between the relative abundance of denitrifiers, determined as narG, napA, nirK, nirS and nosZ denitrification genes, and sediment nitrate content, with similar spatial and seasonal variations. However, we did not find association between denitrification activity and the community structure of denitrifiers. Because nosZ showed the strongest correlation with the content of nitrate in sediments, we used this gene as a molecular marker to construct eight genomic libraries. Analysis of these genomic libraries revealed that diversity of the nosZ-bearing communities was higher in the site with higher nitrate content. Regardless of nitrate concentration in the sediments, the Bradyrhizobiaceae and Rhodocyclaceae were the most abundant families. On the contrary, Rhizobiaceae was exclusively present in sediments with higher nitrate content. Results showed that differences in sediment nitrate concentration affect the composition and diversityof nosZ-bearing communities.

Relative Contribution of nirK- and nirS- Bacterial Denitrifiers as Well as Fungal Denitrifiers to Nitrous Oxide Production from Dairy Manure Compost.

The relative contribution of fungi, bacteria, and nirS and nirK denirifiers to nitrous oxide (N2O) emission with unknown isotopic signature from dairy manure compost was examined by selective inhibition techniques. Chloramphenicol (CHP), cycloheximide (CYH), and diethyl dithiocarbamate (DDTC) were used to suppress the activity of bacteria, fungi, and nirK-possessing denitrifiers, respectively. Produced N2O were surveyed to isotopocule analysis, and its 15N site preference (SP) and δ18O values were compared. Bacteria, fungi, nirS, and nirK gene abundances were compared by qPCR. The results showed that N2O production was strongly inhibited by CHP addition in surface pile samples (82.2%) as well as in nitrite-amended core samples (98.4%), while CYH addition did not inhibit the N2O production. N2O with unknown isotopic signature (SP = 15.3-16.2‰), accompanied by δ18O (19.0-26.8‰) values which were close to bacterial denitrification, was also suppressed by CHP and DDTC addition (95.3%) indicating that nirK denitrifiers were responsible for this N2O production despite being less abundant than nirS denitrifiers. Altogether, our results suggest that bacteria are important for N2O production with different SP values both from compost surface and pile core. However, further work is required to decipher whether N2O with unknown isotopic signature is mostly due to nirK denitrifiers that are taxonomically different from the SP-characterized strains and therefore have different SP values rather than also being interwoven with the contribution of the NO-detoxifying pathway and/or of co-denitrification.

Plant traits related to nitrogen uptake influence plant-microbe competition.

Plant species are important drivers of soil microbial communities. However, how plant functional traits are shaping these communities has received less attention though linking plant and microbial traits is crucial for better understanding plant-microbe interactions. Our objective was to determine how plant-microbe interactions were affected by plant traits. Specifically we analyzed how interactions between plant species and microbes involved in nitrogen cycling were affected by plant traits related to 'nitrogen nutrition in interaction with soil nitrogen availability. Eleven plant species, selected along an oligotrophic-nitrophilic gradient, were grown individually in a nitrogen-poor soil with two levels of nitrate availability. Plant traits for both carbon and nitrogen nutrition were measured and the genetic structure and abundance of rhizosphere. microbial communities, in particular the ammonia oxidizer and nitrate reducer guilds, were analyzed. The structure of the bacterial community in the rhizosphere differed significantly between plant species and these differences depended on nitrogen availability. The results suggest that the rate of nitrogen uptake per unit of root biomass and per day is a key plant trait, explaining why the effect of nitrogen availability on the structure of the bacterial community depends on the plant species. We also showed that the abundance of nitrate reducing bacteria always decreased with increasing nitrogen uptake per unit of root biomass per day, indicating that there was competition for nitrate between plants and nitrate reducing bacteria. This study demonstrates that nitrate-reducing microorganisms may be adversely affected by plants with a high nitrogen uptake rate. Our work puts forward the role of traits related to nitrogen in plant-microbe interactions, whereas carbon is commonly considered as the main driver. It also suggests that plant traits related to ecophysiological processes, such as nitrogen uptake rates, are more relevant for understanding plant-microbe interactions than composite traits, such as nitrophily, which are related to a number of ecophysiological processes.

The interplay between microbial communities and soil properties.

In recent years, there has been considerable progress in determining the soil properties that influence the structure of the soil microbiome. By contrast, the effects of microorganisms on their soil habitat have received less attention with most previous studies focusing on microbial contributions to soil carbon and nitrogen dynamics. However, soil microorganisms are not only involved in nutrient cycling and organic matter transformations but also alter the soil habitat through various biochemical and biophysical mechanisms. Such microbially mediated modifications of soil properties can have local impacts on microbiome assembly with pronounced ecological ramifications. In this Review, we describe the processes by which microorganisms modify the soil environment, considering soil physics, hydrology and chemistry. We explore how microorganism-soil interactions can generate feedback loops and discuss how microbially mediated modifications of soil properties can serve as an alternative avenue for the management and manipulation of microbiomes to combat soil threats and global change.

Soil microbial community fragmentation reveals indirect effects of fungicide exposure mediated by biotic interactions between microorganisms.

Fungicides are used worldwide to improve crop yields, but they can affect non-target soil microorganisms which are essential for ecosystem functioning. Microorganisms form complex communities characterized by a myriad of interspecies interactions, yet it remains unclear to what extent non-target microorganisms are indirectly affected by fungicides through biotic interactions with sensitive taxa. To quantify such indirect effects, we fragmented a soil microbial community by filtration to alter biotic interactions and compared the effect of the fungicide hymexazol between fractions in soil microcosms. We postulated that OTUs which are indirectly affected would exhibit a different response to the fungicide across the fragmented communities. We found that hymexazol primarily affected bacterial and fungal communities through indirect effects, which were responsible for more than 75% of the shifts in relative abundance of the dominant microbial OTUs after exposure to an agronomic dose of hymexazol. However, these indirect effects decreased for the bacterial community when hymexazol doses increased. Our results also suggest that N-cycling processes such as ammonia oxidation can be impacted indirectly by fungicide application. This work sheds light on the indirect impact of fungicide exposure on soil microorganisms through biotic interactions, which underscores the need for higher-tier risk assessment. ENVIRONMENTAL IMPLICATION: In this study, we used a novel approach based on the fragmentation of the soil microbial community to determine to which extent fungicide application could indirectly affect fungi and bacteria through biotic interactions. To assess off-target effects of fungicide on soil microorganisms, we selected hymexazol, which is used worldwide to control a variety of fungal plant pathogens, and exposed arable soil to the recommended field rate, as well as to higher rates. Our findings show that at least 75% of hymexazol-impacted microbial OTUs were indirectly affected, therefore emphasizing the importance of tiered risk assessment.

Manipulating the physical distance between cells during soil colonization reveals the importance of biotic interactions in microbial community assembly.

BACKGROUND: Microbial communities are of tremendous importance for ecosystem functioning and yet we know little about the ecological processes driving the assembly of these communities in the environment. Here, we used an unprecedented experimental approach based on the manipulation of physical distance between neighboring cells during soil colonization to determine the role of bacterial interactions in soil community assembly. We hypothesized that experimentally manipulating the physical distance between bacterial cells will modify the interaction strengths leading to differences in microbial community composition, with increasing distance between neighbors favoring poor competitors. RESULTS: We found significant differences in both bacterial community diversity, composition and co-occurrence networks after soil colonization that were related to physical distancing. We show that reducing distances between cells resulted in a loss of bacterial diversity, with at least 41% of the dominant OTUs being significantly affected by physical distancing. Our results suggest that physical distancing may differentially modulate competitiveness between neighboring species depending on the taxa present in the community. The mixing of communities that assembled at high and low cell densities did not reveal any "home field advantage" during coalescence. This confirms that the observed differences in competitiveness were due to biotic rather than abiotic filtering. CONCLUSIONS: Our study demonstrates that the competitiveness of bacteria strongly depends on cell density and community membership, therefore highlighting the fundamental role of microbial interactions in the assembly of soil communities.

Deciphering the biotic and abiotic drivers of coalescence asymmetry between soil and manure microbiomes.

Manure application improves soil fertility, yet its implications on the success of invasion of manure-borne microorganisms in the soil are poorly understood. Here, we assessed the importance of abiotic and biotic factors in modulating the extent to which manure-borne fungal and bacterial communities can invade resident soil microbial communities. For this purpose, we applied varying frequencies of two different amounts of manure to nine soils differing in physico-chemical properties, as well as in land-use history, over 180 days and monitored changes in bacterial and fungal communities. Variance partitioning revealed differential contributions of abiotic and biotic factors to invasion success, which together accounted for up to 82 % of the variance explained. We showed that the effects of interactions between biotic and abiotic factors increased with coalescence frequency and manure amount for the bacterial and fungal communities, respectively. Both abiotic and biotic factors were important for modulating coalescence asymmetry for the bacterial community, whereas abiotic factors had a greater effect on the fungal community. These results provide new insights into the drivers of coalescence events between manure and resident soil microbial communities. Moreover, our findings highlight the roles of the mixing ratio and frequency of coalescence events in modulating the survival of manure-borne microorganisms.

Biotic homogenization, lower soil fungal diversity and fewer rare taxa in arable soils across Europe.

Soil fungi are a key constituent of global biodiversity and play a pivotal role in agroecosystems. How arable farming affects soil fungal biogeography and whether it has a disproportional impact on rare taxa is poorly understood. Here, we used the high-resolution PacBio Sequel targeting the entire ITS region to investigate the distribution of soil fungi in 217 sites across a 3000 km gradient in Europe. We found a consistently lower diversity of fungi in arable lands than grasslands, with geographic locations significantly impacting fungal community structures. Prevalent fungal groups became even more abundant, whereas rare groups became fewer or absent in arable lands, suggesting a biotic homogenization due to arable farming. The rare fungal groups were narrowly distributed and more common in grasslands. Our findings suggest that rare soil fungi are disproportionally affected by arable farming, and sustainable farming practices should protect rare taxa and the ecosystem services they support.

Experimental community coalescence sheds light on microbial interactions in soil and restores impaired functions.

BACKGROUND: Microbes typically live in communities where individuals can interact with each other in numerous ways. However, knowledge on the importance of these interactions is limited and derives mainly from studies using a limited number of species grown in coculture. Here, we manipulated soil microbial communities to assess the contribution of interactions between microorganisms for assembly of the soil microbiome. RESULTS: By combining experimental removal (taxa depletion in the community) and coalescence (mixing of manipulated and control communities) approaches, we demonstrated that interactions between microorganisms can play a key role in determining their fitness during soil recolonization. The coalescence approach not only revealed the importance of density-dependent interactions in microbial community assembly but also allowed to restore partly or fully community diversity and soil functions. Microbial community manipulation resulted in shifts in both inorganic nitrogen pools and soil pH, which were related to the proportion of ammonia-oxidizing bacteria. CONCLUSIONS: Our work provides new insights into the understanding of the importance of microbial interactions in soil. Our top-down approach combining removal and coalescence manipulation also allowed linking community structure and ecosystem functions. Furthermore, these results highlight the potential of manipulating microbial communities for the restoration of soil ecosystems. Video Abstract.

Microbial ecological clusters structured by environments drive maize residue decomposition at the continental scale.

Environmental factors (e.g., climate and edaphic factors) indirectly regulate residue decomposition via microbial communities. Microbial ecological clusters (eco-clusters) structured by specific environmental factors have consequences for ecosystem functions. However, less is known about how microbial eco-clusters affect residue decomposition, especially over broad geographic scales. We collected agricultural soils from adjacent pairs of upland and paddy fields along a latitudinal gradient from the cold-temperature zone to the tropical zone, and conducted a microcosm experiment with 13C-labelled maize residue to explore the continental pattern of maize residue-derived 13CO2 (RDC), and whether and how microbial eco-clusters drive and predict RDC. Results showed that RDC decreased with latitude in both upland and paddy fields. Further, we identified 21 well-defined eco-clusters according to microbial environmental preferences, which explained 51.15 % of the spatial variations in RDC. The eco-clusters of high-total annual precipitation (TAP), high-mean annual temperature (MAT), low-pH, and some low-nutrient-associated exerted a positive effect on RDC. These eco-clusters contained many taxa belonging to the Actinobacteriota, Firmicutes, and Sordariomycetes, and their relative abundance decreased with latitude. Upland soils displayed 2.40-fold of RDC over paddy soils. Low-pH and high-organic matter (OM) eco-clusters were found to be the most prominent predictors of RDC in upland and paddy fields, respectively. Finally, we constructed a continental atlas of RDC in both upland and paddy fields based on eco-clusters and high-resolution climate and soil data. Overall, our study provides important evidence that historical environment-shaped microbial eco-clusters can drive and predict residue decomposition, providing new insights into how environmental factors indirectly regulate residue decomposition.