Nutrient-induced acidification modulates soil biodiversity-function relationships.

Nutrient enrichment is a major global change component that often disrupts the relationship between aboveground biodiversity and ecosystem functions by promoting species dominance, altering trophic interactions, and reducing ecosystem stability. Emerging evidence indicates that nutrient enrichment also reduces soil biodiversity and weakens the relationship between belowground biodiversity and ecosystem functions, but the underlying mechanisms remain largely unclear. Here, we explore the effects of nutrient enrichment on soil properties, soil biodiversity, and multiple ecosystem functions through a 13-year field experiment. We show that soil acidification induced by nutrient enrichment, rather than changes in mineral nutrient and carbon (C) availability, is the primary factor negatively affecting the relationship between soil diversity and ecosystem multifunctionality. Nitrogen and phosphorus additions significantly reduce soil pH, diversity of bacteria, fungi and nematodes, as well as an array of ecosystem functions related to C and nutrient cycling. Effects of nutrient enrichment on microbial diversity also have negative consequences at higher trophic levels on the diversity of microbivorous nematodes. These results indicate that nutrient-induced acidification can cascade up its impacts along the soil food webs and influence ecosystem functioning, providing novel insight into the mechanisms through which nutrient enrichment influences soil community and ecosystem properties.

Metabolic coupling between soil aerobic methanotrophs and denitrifiers in rice paddy fields.

Paddy fields are hotspots of microbial denitrification, which is typically linked to the oxidation of electron donors such as methane (CH4) under anoxic and hypoxic conditions. While several anaerobic methanotrophs can facilitate denitrification intracellularly, whether and how aerobic CH4 oxidation couples with denitrification in hypoxic paddy fields remains virtually unknown. Here we combine a ~3300 km field study across main rice-producing areas of China and 13CH4-DNA-stable isotope probing (SIP) experiments to investigate the role of soil aerobic CH4 oxidation in supporting denitrification. Our results reveal positive relationships between CH4 oxidation and denitrification activities and genes across various climatic regions. Microcosm experiments confirm that CH4 and methanotroph addition promote gene expression involved in denitrification and increase nitrous oxide emissions. Moreover, 13CH4-DNA-SIP analyses identify over 70 phylotypes harboring genes associated with denitrification and assimilating 13C, which are mostly belonged to Rubrivivax, Magnetospirillum, and Bradyrhizobium. Combined analyses of 13C-metagenome-assembled genomes and 13C-metabolomics highlight the importance of intermediates such as acetate, propionate and lactate, released during aerobic CH4 oxidation, for the coupling of CH4 oxidation with denitrification. Our work identifies key microbial taxa and pathways driving coupled aerobic CH4 oxidation and denitrification, with important implications for nitrogen management and greenhouse gas regulation in agroecosystems.

Cyanobacterial and moss biocrusts shape soil nematode community in dryland mountain ecosystems with increasing aridity.

Soil nematodes are the most abundant animals on Earth and play critical roles in regulating numerous ecosystem processes, from enhancing primary productivity to mineralizing multiple nutrients. In dryland soils, a rich community of microphyte organisms (biocrusts) provide critical habitats for soil nematodes, but their presence is being threatened by increasing aridity induced by global climate change. Despite its importance, how types of biocrusts and aridity index influence soil nematode community in dryland mountain ecosystems remains largely unknown. To fill these knowledge gaps, we conducted a field survey with contrasting aridity indexes (0.2, 0.4, and 0.6) and three types of biocrusts (cyanobacterial, cyanobacterial-moss mixed, and moss crusts) in the topsoil (0-5 cm) from the northern Chinese Loess Plateau. We found that the abundance (number of individuals per gram of soil), richness (number of Operational Taxonomic Units; OTUs), and diversity (number of different species) of soil nematodes were remarkably higher under biocrusts than in bare soils, regardless of aridity index and types of biocrusts. Our results also showed that the same variables had the highest values in moss crusts compared to cyanobacterial and cyanobacterial-moss mixed crusts. Structural equation modelling further revealed that biocrust types and traits (i.e., biocrust thickness, chlorophyll content, shear force, and penetration resistance) are the most important factors associated with both nematode abundance and richness. Together, our findings indicate that biocrusts, especially moss cover, and less stressful aridity conditions favor soil nematodes community in dryland mountain regions. Such knowledge is critical for anticipating the distribution of these animals under climate change scenarios and, ultimately, the numerous ecosystem services supported by soil nematodes.

Hotspots of biogeochemical activity linked to aridity and plant traits across global drylands.

Perennial plants create productive and biodiverse hotspots, known as fertile islands, beneath their canopies. These hotspots largely determine the structure and functioning of drylands worldwide. Despite their ubiquity, the factors controlling fertile islands under conditions of contrasting grazing by livestock, the most prevalent land use in drylands, remain virtually unknown. Here we evaluated the relative importance of grazing pressure and herbivore type, climate and plant functional traits on 24 soil physical and chemical attributes that represent proxies of key ecosystem services related to decomposition, soil fertility, and soil and water conservation. To do this, we conducted a standardized global survey of 288 plots at 88 sites in 25 countries worldwide. We show that aridity and plant traits are the major factors associated with the magnitude of plant effects on fertile islands in grazed drylands worldwide. Grazing pressure had little influence on the capacity of plants to support fertile islands. Taller and wider shrubs and grasses supported stronger island effects. Stable and functional soils tended to be linked to species-rich sites with taller plants. Together, our findings dispel the notion that grazing pressure or herbivore type are linked to the formation or intensification of fertile islands in drylands. Rather, our study suggests that changes in aridity, and processes that alter island identity and therefore plant traits, will have marked effects on how perennial plants support and maintain the functioning of drylands in a more arid and grazed world.

Dryland microbiomes reveal community adaptations to desertification and climate change.

Drylands account for 45% of the Earth's land area, supporting ~40% of the global population. These regions support some of the most extreme environments on Earth, characterized by extreme temperatures, low and variable rainfall, and low soil fertility. In these biomes, microorganisms provide vital ecosystem services and have evolved distinctive adaptation strategies to endure and flourish in the extreme. However, dryland microbiomes and the ecosystem services they provide are under threat due to intensifying desertification and climate change. In this review, we provide a synthesis of our current understanding of microbial life in drylands, emphasizing the remarkable diversity and adaptations of these communities. We then discuss anthropogenic threats, including the influence of climate change on dryland microbiomes and outline current knowledge gaps. Finally, we propose research priorities to address those gaps and safeguard the sustainability of these fragile biomes.

Heritable microbiome variation is correlated with source environment in locally adapted maize varieties.

Beneficial interactions with microorganisms are pivotal for crop performance and resilience. However, it remains unclear how heritable the microbiome is with respect to the host plant genotype and to what extent host genetic mechanisms can modulate plant-microbiota interactions in the face of environmental stresses. Here we surveyed 3,168 root and rhizosphere microbiome samples from 129 accessions of locally adapted Zea, sourced from diverse habitats and grown under control and different stress conditions. We quantified stress treatment and host genotype effects on the microbiome. Plant genotype and source environment were predictive of microbiome abundance. Genome-wide association analysis identified host genetic variants linked to both rhizosphere microbiome abundance and source environment. We identified transposon insertions in a candidate gene linked to both the abundance of a keystone bacterium Massilia in our controlled experiments and total soil nitrogen in the source environment. Isolation and controlled inoculation of Massilia alone can contribute to root development, whole-plant biomass production and adaptation to low nitrogen availability. We conclude that locally adapted maize varieties exert patterns of genetic control on their root and rhizosphere microbiomes that follow variation in their home environments, consistent with a role in tolerance to prevailing stress.

Fostering biodiversity research in post-fire biology.

The impacts of wildfire on vegetation and soil erosion have been studied for decades aiming to bring back ecosystems after fire perturbance. However, the influence of fires on above and belowground biodiversity remains far less understood. Biodiversity is critical for supporting ecosystem function, and this data scarcity is hampering managers in adopting effective practices for a proper restoration of burned ecosystems. This limitation could be overcome by future research that should focus post-fire diversity of plants and soil biota, by (i) analysing the environmental factors driving post-fire evolutionary trends; (ii) exploring their interrelations across different spatial and temporal scales; (iii) identifying the variability across fires of different severities and frequency; (iv) ascertaining the post-fire response of individual plant species and soil taxa to fire with or without application of post-fire restoration actions.

Deforestation impacts soil biodiversity and ecosystem services worldwide.

Deforestation poses a global threat to biodiversity and its capacity to deliver ecosystem services. Yet, the impacts of deforestation on soil biodiversity and its associated ecosystem services remain virtually unknown. We generated a global dataset including 696 paired-site observations to investigate how native forest conversion to other land uses affects soil properties, biodiversity, and functions associated with the delivery of multiple ecosystem services. The conversion of native forests to plantations, grasslands, and croplands resulted in higher bacterial diversity and more homogeneous fungal communities dominated by pathogens and with a lower abundance of symbionts. Such conversions also resulted in significant reductions in carbon storage, nutrient cycling, and soil functional rates related to organic matter decomposition. Responses of the microbial community to deforestation, including bacterial and fungal diversity and fungal guilds, were predominantly regulated by changes in soil pH and total phosphorus. Moreover, we found that soil fungal diversity and functioning in warmer and wetter native forests is especially vulnerable to deforestation. Our work highlights that the loss of native forests to managed ecosystems poses a major global threat to the biodiversity and functioning of soils and their capacity to deliver ecosystem services.

Biocrusts enhance soil organic carbon stability and regulate the fate of new-input carbon in semiarid desert ecosystems.

Given their global prevalence, dryland (including hyperarid, arid, semiarid, and dry subhumid regions) ecosystems are critical for supporting soil organic carbon (SOC) stocks, with even small changes in such SOC pools affecting the global carbon (C) cycling. Biocrusts play an essential role in supporting C cycling in semiarid ecosystems. However, the influence of biocrusts and their successional stages on SOC and its fraction contents, as well as their role in regulating new input C into SOC fractions remain largely unknown. In this study, we collected continuous samples of bare soil (BS) and three successional stages of biocrust soils (cyanobacterial (CC), low-cover moss (LM), and high-cover moss (HM)) at 0-5 cm depth every month for one year in a semiarid desert ecosystem. We analyzed SOC changes among the samples and their fraction contents including: labile organic C (LOC) (composed of microbial biomass C (MBC), dissolved organic C (DOC), and easily oxidized organic C (EOC)) and recalcitrant organic C (ROC) fractions, soil nutrient content including: ammonium (NH4+-N), nitrate (NO3--N), and available phosphorus (AP), and soil temperature and moisture. We also conducted a 13C pulse-labelling experiment in the field to accurately quantify the effects of biocrust successional stage on exogenous C allocation to SOC fractions. Our results showed that the three successional stages of biocrust (CC-LM-HM) increased SOC and ROC contents by an average of 5.3 ± 3.6 g kg-1 and 4.0 ± 3.0 g kg-1, respectively; and the MBC, DOC, and EOC contents increased by an average of 41.7 ± 24.8 mg kg-1, 28.7 ± 12.6 mg kg-1, and 1.2 ± 0.6 g kg-1, respectively, compared to that of BS. These increases were attributed to an increase in photosynthetic pigment content, higher nutrient levels, and more suitable microclimates (e.g., higher moisture and more moderate temperature) during biocrust succession. More importantly, SOC stability was greatly improved with biocrust succession from cyanobacteria to moss, as evidenced by the reduction in soil EOC:SOC and EOC:ROC ratios by an average of 50 ± 34 % and 99 ± 67 %, respectively, while the ROC:SOC ratio increased by 33 ± 16 % with biocrust succession compared to those of BS. The biocrust SOC, DOC, and MBC 13C contents at different stages were on average 0.096 ± 0.034 mg kg-1, 0.010 ± 0.005 mg kg-1, and 0.014 ± 0.005 mg kg-1 higher than those of BS. Similarly, the allocation of new-input C among the DOC and MBC at different biocrust stages (19 ± 10 %) was significantly higher than that of BS (9 ± 6 %). New-input C into the biocrusts was fixed by microbes (43 ± 18 %) within ∼10 days and converted into other forms of C (85 ± 5 %) after 80 days. Our study provides a new perspective on how biocrusts support C cycling in semiarid desert ecosystems by mediating new C inputs into diverse fractional contents, and highlights the significance of biocrust successional stages in maintaining soil C stocks and stability in the dryland soil system.

Metagenomics untangles potential adaptations of Antarctic endolithic bacteria at the fringe of habitability.

Survival and growth strategies of Antarctic endolithic microbes residing in Earth's driest and coldest desert remain virtually unknown. From 109 endolithic microbiomes, 4539 metagenome-assembled genomes were generated, 49.3 % of which were novel candidate bacterial species. We present evidence that trace gas oxidation and atmospheric chemosynthesis may be the prevalent strategies supporting metabolic activity and persistence of these ecosystems at the fringe of life and the limits of habitability.

Positive associations fuel soil biodiversity and ecological networks worldwide.

Microbial interactions are key to maintaining soil biodiversity. However, whether negative or positive associations govern the soil microbial system at a global scale remains virtually unknown, limiting our understanding of how microbes interact to support soil biodiversity and functions. Here, we explored ecological networks among multitrophic soil organisms involving bacteria, protists, fungi, and invertebrates in a global soil survey across 20 regions of the planet and found that positive associations among both pairs and triads of soil taxa governed global soil microbial networks. We further revealed that soil networks with greater levels of positive associations supported larger soil biodiversity and resulted in lower network fragility to withstand potential perturbations of species losses. Our study provides unique evidence of the widespread positive associations between soil organisms and their crucial role in maintaining the multitrophic structure of soil biodiversity worldwide.

New perspectives on microbiome and nutrient sequestration in soil aggregates during long-term grazing exclusion.

Grazing exclusion alters grassland soil aggregation, microbiome composition, and biogeochemical processes. However, the long-term effects of grazing exclusion on the microbial communities and nutrient dynamics within soil aggregates remain unclear. We conducted a 36-year exclusion experiment to investigate how grazing exclusion affects the soil microbial community and the associated soil functions within soil aggregates in a semiarid grassland. Long-term (36 years) grazing exclusion induced a shift in microbial communities, especially in the <2 mm aggregates, from high to low diversity compared to the grazing control. The reduced microbial diversity was accompanied by instability of fungal communities, extended distribution of fungal pathogens to >2 mm aggregates, and reduced carbon (C) sequestration potential thus revealing a negative impact of long-term GE. In contrast, 11-26 years of grazing exclusion greatly increased C sequestration and promoted nutrient cycling in soil aggregates and associated microbial functional genes. Moreover, the environmental characteristics of microhabitats (e.g., soil pH) altered the soil microbiome and strongly contributed to C sequestration. Our findings reveal new evidence from soil microbiology for optimizing grazing exclusion duration to maintain multiple belowground ecosystem functions, providing promising suggestions for climate-smart and resource-efficient grasslands.

Deciphering microbiomes dozens of meters under our feet and their edaphoclimatic and spatial drivers.

Microbes inhabiting deep soil layers are known to be different from their counterpart in topsoil yet remain under investigation in terms of their structure, function, and how their diversity is shaped. The microbiome of deep soils (>1 m) is expected to be relatively stable and highly independent from climatic conditions. Much less is known, however, on how these microbial communities vary along climate gradients. Here, we used amplicon sequencing to investigate bacteria, archaea, and fungi along fifteen 18-m depth profiles at 20-50-cm intervals across contrasting aridity conditions in semi-arid forest ecosystems of China's Loess Plateau. Our results showed that bacterial and fungal α diversity and bacterial and archaeal community similarity declined dramatically in topsoil and remained relatively stable in deep soil. Nevertheless, deep soil microbiome still showed the functional potential of N cycling, plant-derived organic matter degradation, resource exchange, and water coordination. The deep soil microbiome had closer taxa-taxa and bacteria-fungi associations and more influence of dispersal limitation than topsoil microbiome. Geographic distance was more influential in deep soil bacteria and archaea than in topsoil. We further showed that aridity was negatively correlated with deep-soil archaeal and fungal richness, archaeal community similarity, relative abundance of plant saprotroph, and bacteria-fungi associations, but increased the relative abundance of aerobic ammonia oxidation, manganese oxidation, and arbuscular mycorrhizal in the deep soils. Root depth, complexity, soil volumetric moisture, and clay play bridging roles in the indirect effects of aridity on microbes in deep soils. Our work indicates that, even microbial communities and nutrient cycling in deep soil are susceptible to changes in water availability, with consequences for understanding the sustainability of dryland ecosystems and the whole-soil in response to aridification. Moreover, we propose that neglecting soil depth may underestimate the role of soil moisture in dryland ecosystems under future climate scenarios.

Crop rotation and native microbiome inoculation restore soil capacity to suppress a root disease.

It is widely known that some soils have strong levels of disease suppression and prevent the establishment of pathogens in the rhizosphere of plants. However, what soils are better suppressing disease, and how management can help us to boost disease suppression remain unclear. Here, we used field, greenhouse and laboratory experiments to investigate the effect of management (monocropping and rotation) on the capacity of rhizosphere microbiomes in suppressing peanut root rot disease. Compared with crop rotations, monocropping resulted in microbial assemblies that were less effective in suppressing root rot diseases. Further, the depletion of key rhizosphere taxa in monocropping, which were at a disadvantage in the competition for limited exudates resources, reduced capacity to protect plants against pathogen invasion. However, the supplementation of depleted strains restored rhizosphere resistance to pathogen. Taken together, our findings highlight the role of native soil microbes in fighting disease and supporting plant health, and indicate the potential of using microbial inocula to regenerate the natural capacity of soil to fight disease.

Biocrusts protect the Great Wall of China from erosion.

The Great Wall of China, one of the most emblematic and historical structures built by humankind throughout all of history, is suffering from rain and wind erosion and is largely colonized by biocrusts. However, how biocrusts influence the conservation and longevity of this structure is virtually unknown. Here, we conducted an extensive biocrust survey across the Great Wall and found that biocrusts cover 67% of the studied sections. Biocrusts enhance the mechanical stability and reduce the erodibility of the Great Wall. Compared with bare rammed earth, the biocrust-covered sections exhibited reduced porosity, water-holding capacity, erodibility, and salinity by 2 to 48%, while increasing compressive strength, penetration resistance, shear strength, and aggregate stability by 37 to 321%. We further found that the protective function of biocrusts mainly depended on biocrust features, climatic conditions, and structure types. Our work highlights the fundamental importance of biocrusts as a nature-based intervention to the conservation of the Great Wall, protecting this monumental heritage from erosion.

Metallic micronutrients are associated with the structure and function of the soil microbiome.

The relationship between metallic micronutrients and soil microorganisms, and thereby soil functioning, has been little explored. Here, we investigate the relationship between metallic micronutrients (Fe, Mn, Cu, Zn, Mo and Ni) and the abundance, diversity and function of soil microbiomes. In a survey across 180 sites in China, covering a wide range of soil conditions the structure and function of the soil microbiome are highly correlated with metallic micronutrients, especially Fe, followed by Mn, Cu and Zn. These results are robust to controlling for soil pH, which is often reported as the most important predictor of the soil microbiome. An incubation experiment with Fe and Zn additions for five different soil types also shows that increased micronutrient concentration affects microbial community composition and functional genes. In addition, structural equation models indicate that micronutrients positively contribute to the ecosystem productivity, both directly (micronutrient availability to plants) and, to a lesser extent, indirectly (via affecting the microbiome). Our findings highlight the importance of micronutrients in explaining soil microbiome structure and ecosystem functioning.

Connecting the multiple dimensions of global soil fungal diversity.

How the multiple facets of soil fungal diversity vary worldwide remains virtually unknown, hindering the management of this essential species-rich group. By sequencing high-resolution DNA markers in over 4000 topsoil samples from natural and human-altered ecosystems across all continents, we illustrate the distributions and drivers of different levels of taxonomic and phylogenetic diversity of fungi and their ecological groups. We show the impact of precipitation and temperature interactions on local fungal species richness (alpha diversity) across different climates. Our findings reveal how temperature drives fungal compositional turnover (beta diversity) and phylogenetic diversity, linking them with regional species richness (gamma diversity). We integrate fungi into the principles of global biodiversity distribution and present detailed maps for biodiversity conservation and modeling of global ecological processes.

Optimizing cropping systems to close the gap between economic profitability and environmental health.

Supporting food security while maintaining ecosystem sustainability is one of the most important global challenges for humanity. Optimization of cropping systems is expected to promote the ecosystem services of agroecosystems. Yet, how and why cropping system influences the trade-offs between economic profitability and multiple ecosystem services remain poorly understood. We investigate the influence of six cropping systems on trade-offs between economic profitability and multiple ecosystem services after considering 36 agricultural ecosystem properties using field experiment data from 2020 to 2022. We show that designing cropping system is a critical tool to closing the gap between ecosystem sustainability and commercial profitability. Cropping system with three harvests within 2 yr had higher performance in overall ecosystem multiple services through enhancement of supporting, regulating, and economic performance without compromising provisioning compared with four other systems. These systems diminished the trade-off among multiple services, resulting in a 'win-win' situation for economics and multiple services. By contrast, the monoculture and double cropping systems lead to a strong trade-off between pairwise services including ecosystem health and profitability. Our work illustrates the substantial potential of rotation systems with three harvests within 2 yr in enforcing ecosystem services and closing the trade-offs among multiple agricultural ecosystem services.