Unforeseen plant phenotypic diversity in a dry and grazed world.

Earth harbours an extraordinary plant phenotypic diversity1 that is at risk from ongoing global changes2,3. However, it remains unknown how increasing aridity and livestock grazing pressure-two major drivers of global change4-6-shape the trait covariation that underlies plant phenotypic diversity1,7. Here we assessed how covariation among 20 chemical and morphological traits responds to aridity and grazing pressure within global drylands. Our analysis involved 133,769 trait measurements spanning 1,347 observations of 301 perennial plant species surveyed across 326 plots from 6 continents. Crossing an aridity threshold of approximately 0.7 (close to the transition between semi-arid and arid zones) led to an unexpected 88% increase in trait diversity. This threshold appeared in the presence of grazers, and moved toward lower aridity levels with increasing grazing pressure. Moreover, 57% of observed trait diversity occurred only in the most arid and grazed drylands, highlighting the phenotypic uniqueness of these extreme environments. Our work indicates that drylands act as a global reservoir of plant phenotypic diversity and challenge the pervasive view that harsh environmental conditions reduce plant trait diversity8-10. They also highlight that many alternative strategies may enable plants to cope with increases in environmental stress induced by climate change and land-use intensification.

Global hotspots for soil nature conservation.

Soils are the foundation of all terrestrial ecosystems1. However, unlike for plants and animals, a global assessment of hotspots for soil nature conservation is still lacking2. This hampers our ability to establish nature conservation priorities for the multiple dimensions that support the soil system: from soil biodiversity to ecosystem services. Here, to identify global hotspots for soil nature conservation, we performed a global field survey that includes observations of biodiversity (archaea, bacteria, fungi, protists and invertebrates) and functions (critical for six ecosystem services) in 615 composite samples of topsoil from a standardized survey in all continents. We found that each of the different ecological dimensions of soils-that is, species richness (alpha diversity, measured as amplicon sequence variants), community dissimilarity and ecosystem services-peaked in contrasting regions of the planet, and were associated with different environmental factors. Temperate ecosystems showed the highest species richness, whereas community dissimilarity peaked in the tropics, and colder high-latitudinal ecosystems were identified as hotspots of ecosystem services. These findings highlight the complexities that are involved in simultaneously protecting multiple ecological dimensions of soil. We further show that most of these hotspots are not adequately covered by protected areas (more than 70%), and are vulnerable in the context of several scenarios of global change. Our global estimation of priorities for soil nature conservation highlights the importance of accounting for the multidimensionality of soil biodiversity and ecosystem services to conserve soils for future generations.

Aboveground and belowground biodiversity have complementary effects on ecosystem functions across global grasslands.

Grasslands are integral to maintaining biodiversity and key ecosystem services and are under threat from climate change. Plant and soil microbial diversity, and their interactions, support the provision of multiple ecosystem functions (multifunctionality). However, it remains virtually unknown whether plant and soil microbial diversity explain a unique portion of total variation or shared contributions to supporting multifunctionality across global grasslands. Here, we combine results from a global survey of 101 grasslands with a novel microcosm study, controlling for both plant and soil microbial diversity to identify their individual and interactive contribution to support multifunctionality under aridity and experimental drought. We found that plant and soil microbial diversity independently predict a unique portion of total variation in above- and belowground functioning, suggesting that both types of biodiversity complement each other. Interactions between plant and soil microbial diversity positively impacted multifunctionality including primary production and nutrient storage. Our findings were also climate context dependent, since soil fungal diversity was positively associated with multifunctionality in less arid regions, while plant diversity was strongly and positively linked to multifunctionality in more arid regions. Our results highlight the need to conserve both above- and belowground diversity to sustain grassland multifunctionality in a drier world and indicate climate change may shift the relative contribution of plant and soil biodiversity to multifunctionality across global grasslands.

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.

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.

The global biogeography and environmental drivers of fairy circles.

Fairy circles (FCs) are regular vegetation patterns found in drylands of Namibia and Western Australia. It is virtually unknown whether they are also present in other regions of the world and which environmental factors determine their distribution. We conducted a global systematic survey and found FC-like vegetation patterns in 263 sites from 15 countries and three continents, including the Sahel, Madagascar, and Middle-West Asia. FC-like vegetation patterns are found in environments characterized by a unique combination of soil (including low nutrient levels and high sand content) and climatic (arid regions with high temperatures and high precipitation seasonality) conditions. In addition to these factors, the presence of specific biological elements (termite nests) in certain regions also plays a role in the presence of these patterns. Furthermore, areas with FC-like vegetation patterns also showed more stable temporal productivity patterns than those of surrounding areas. Our study presents a global atlas of FCs and provides unique insights into the ecology and biogeography of these fascinating vegetation patterns.

Prevalence and drivers of abrupt vegetation shifts in global drylands.

The constant provision of plant productivity is integral to supporting the liability of ecosystems and human wellbeing in global drylands. Drylands are paradigmatic examples of systems prone to experiencing abrupt changes in their functioning. Indeed, space-for-time substitution approaches suggest that abrupt changes in plant productivity are widespread, but this evidence is less clear using observational time series or experimental data at a large scale. Studying the prevalence and, most importantly, the unknown drivers of abrupt (rather than gradual) dynamical patterns in drylands may help to unveil hotspots of current and future dynamical instabilities in drylands. Using a 20-y global satellite-derived temporal assessment of dryland Normalized Difference Vegetation Index (NDVI), we show that 50% of all dryland ecosystems exhibiting gains or losses of NDVI are characterized by abrupt positive/negative temporal dynamics. We further show that abrupt changes are more common among negative than positive NDVI trends and can be found in global regions suffering recent droughts, particularly around critical aridity thresholds. Positive abrupt dynamics are found most in ecosystems with low seasonal variability or high aridity. Our work unveils the high importance of climate variability on triggering abrupt shifts in vegetation and it provides missing evidence of increasing abruptness in systems intensively managed by humans, with low soil organic carbon contents, or around specific aridity thresholds. These results highlight that abrupt changes in dryland dynamics are very common, especially for productivity losses, pinpoint global hotspots of dryland vulnerability, and identify drivers that could be targeted for effective dryland management.

Multikingdom interactions govern the microbiome in subterranean cultural heritage sites.

SignificanceThe conservation of historical relics against microbial biodeterioration is critical to preserving cultural heritages. One major challenge is our limited understanding of microorganisms' dispersal, colonization, and persistence on relics after excavation and opening to external environments. Here, we investigate the ecological and physiological profiles of the microbiome within and outside the Dahuting Han Dynasty Tomb with a 1,800-y history. Actinobacteria dominate the microbiome in this tomb. Via interkingdom signaling mutualism, springtails carry Actinobacteria as one possible source into the tomb from surrounding environments. Subsequently, Actinobacteria produce cellulases combined with antimicrobial substances, which helps them to colonize and thrive in the tomb via intrakingdom competition. Our findings unravel the ecology of the microbiomes colonizing historical relics and provide help for conservation practices.

Unfolding the dynamics of ecosystems undergoing alternating wet-dry transitional states.

A significant fraction of Earth's ecosystems undergoes periodic wet-dry alternating transitional states. These globally distributed water-driven transitional ecosystems, such as intermittent rivers and coastal shorelines, have traditionally been studied as two distinct entities, whereas they constitute a single, interconnected meta-ecosystem. This has resulted in a poor conceptual and empirical understanding of water-driven transitional ecosystems. Here, we develop a conceptual framework that places the temporal availability of water as the core driver of biodiversity and functional patterns of transitional ecosystems at the global scale. Biological covers (e.g., aquatic biofilms and biocrusts) serve as an excellent model system thriving in both aquatic and terrestrial states, where their succession underscores the intricate interplay between these two states. The duration, frequency, and rate of change of wet-dry cycles impose distinct plausible scenarios where different types of biological covers can occur depending on their desiccation/hydration resistance traits. This implies that the distinct eco-evolutionary potential of biological covers, represented by their trait profiles, would support different functions while maintaining similar multifunctionality levels. By embracing multiple alternating transitional states as interconnected entities, our approach can help to better understand and manage global change impacts on biodiversity and multifunctionality in water-driven transitional ecosystems, while providing new avenues for interdisciplinary studies.

The abundant fraction of soil microbiomes regulates the rhizosphere function in crop wild progenitors.

The rhizosphere influence on the soil microbiome and function of crop wild progenitors (CWPs) remains virtually unknown, despite its relevance to develop microbiome-oriented tools in sustainable agriculture. Here, we quantified the rhizosphere influence-a comparison between rhizosphere and bulk soil samples-on bacterial, fungal, protists and invertebrate communities and on soil multifunctionality across nine CWPs at their sites of origin. Overall, rhizosphere influence was higher for abundant taxa across the four microbial groups and had a positive influence on rhizosphere soil organic C and nutrient contents compared to bulk soils. The rhizosphere influence on abundant soil microbiomes was more important for soil multifunctionality than rare taxa and environmental conditions. Our results are a starting point towards the use of CWPs for rhizosphere engineering in modern crops.

Evolutionarily conserved core microbiota as an extended trait in nitrogen acquisition strategy of herbaceous species.

Microbiota have co-evolved with plants over millions of years and are intimately linked to plants, ranging from symbiosis to pathogenesis. However, our understanding of the existence of a shared core microbiota across phylogenetically diverse plants remains limited. A common garden field experiment was conducted to investigate the rhizosphere microbial communities of phylogenetically contrasting herbaceous families. Through a combination of metagenomic sequencing, analysis of plant economic traits, and soil biochemical properties, we aimed to elucidate the eco-evolutionary role of the core rhizosphere microbiota in light of plant economic strategies. We identified a conserved core microbiota consisting of 278 taxa that was closely associated with the phylogeny of the plants studied. This core microbiota actively participated in multiple nitrogen metabolic processes and showed a strong correlation with the functional potential of rhizosphere nitrogen cycling, thereby serving as an extended trait in the plant nitrogen acquisition. Furthermore, our examination of simulated species loss revealed the crucial role of the core microbiota in maintaining the rhizosphere community's network stability. Our study highlighted that the core microbiota, which exhibited a phylogenetically conserved association with plants, potentially represented an extension of the plant phenotype and played an important role in nitrogen acquisition. These findings held implications for the utilization of microbiota-mediated plant functions.

Plant species and associated root nutritional traits influence soil dominant bacteria in coastal wetlands across China.

Climate and edaphic properties drive the biogeographic distribution of dominant soil microbial phylotypes in terrestrial ecosystems. However, the impact of plant species and their root nutritional traits on microbial distribution in coastal wetlands remains unclear. Here, we investigated the nutritional traits of 100 halophyte root samples and the bacterial communities in the corresponding soil samples from coastal wetlands across eastern China. This study spans 22° of latitude, covering over 2500 km from north to south. We found that 1% of soil bacterial phylotypes accounted for nearly 30% of the soil bacterial community abundance, suggesting that a few bacterial phylotypes dominated the coastal wetlands. These dominated phylotypes could be grouped into three ecological clusters as per their preference over climatic (temperature and precipitation), edaphic (soil carbon and nitrogen), and plant factors (halophyte vegetation, root carbon, and nitrogen). We further provide novel evidence that plant root nutritional traits, especially root C and N, can strongly influence the distribution of these ecological clusters. Taken together, our study provides solid evidence of revealing the dominance of specific bacterial phylotypes and the complex interactions with their environment, highlighting the importance of plant root nutritional traits on biogeographic distribution of soil microbiome in coastal wetland ecosystems.

Positive soil priming effects are the rule at a global scale.

Priming effects of soil organic matter decomposition are critical to determine carbon budget and turnover in soil. Yet, the overall direction and intensity of soil priming remains under debate. A second-order meta-analysis was performed with 9296-paired observations from 363 primary studies to determine the intensity and general direction of priming effects depending on the compound type, nutrient availability, and ecosystem type. We found that fresh carbon inputs induced positive priming effects (+37%) in 97% of paired observations. Labile compounds induced larger priming effects (+73%) than complex organic compounds (+33%). Nutrients (e.g., N, P) added with organic compounds reduced the intensity of priming effects compared to compounds without N and P, reflecting "nutrient mining from soil organic matter" as one of the main mechanisms of priming effects. Notably, tundra, lakebeds, wetlands, and volcanic soils showed much larger priming effects (+125%) compared to soils under forests, croplands, and grasslands (+24…+32%). Our findings highlight that positive priming effects are predominant in most soils at a global scale. Optimizing strategies to incorporate fresh organic matter and nutrients is urgently needed to offset the priming-induced accelerated organic carbon turnover and possible losses.

Fertilization regulates global thresholds in soil bacteria.

Global patterns in soil microbiomes are driven by non-linear environmental thresholds. Fertilization is known to shape the soil microbiome of terrestrial ecosystems worldwide. Yet, whether fertilization influences global thresholds in soil microbiomes remains virtually unknown. Here, utilizing optimized machine learning models with Shapley additive explanations on a dataset of 10,907 soil samples from 24 countries, we discovered that the microbial community response to fertilization is highly dependent on environmental contexts. Furthermore, the interactions among nitrogen (N) addition, pH, and mean annual temperature contribute to non-linear patterns in soil bacterial diversity. Specifically, we observed positive responses within a soil pH range of 5.2-6.6, with the influence of higher temperature (>15°C) on bacterial diversity being positive within this pH range but reversed in more acidic or alkaline soils. Additionally, we revealed the threshold effect of soil organic carbon and total nitrogen, demonstrating how temperature and N addition amount interacted with microbial communities within specific edaphic concentration ranges. Our findings underscore how complex environmental interactions control soil bacterial diversity under fertilization.

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.

Intrinsic microbial temperature sensitivity and soil organic carbon decomposition in response to climate change.

Soil microbes are essential for regulating carbon stocks under climate change. However, the uncertainty surrounding how microbial temperature responses control carbon losses under warming conditions highlights a significant gap in our climate change models. To address this issue, we conducted a fine-scale analysis of soil organic carbon composition under different temperature gradients and characterized the corresponding microbial growth and physiology across various paddy soils spanning 4000 km in China. Our results showed that warming altered the composition of organic matter, resulting in a reduction in carbohydrates of approximately 0.026% to 0.030% from humid subtropical regions to humid continental regions. These changes were attributed to a decrease in the proportion of cold-preferring bacteria, leading to significant soil carbon losses. Our findings suggest that intrinsic microbial temperature sensitivity plays a crucial role in determining the rate of soil organic carbon decomposition, providing insights into the temperature limitations faced by microbial activities and their impact on soil carbon-climate feedback.

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.

Unearthing the soil-borne microbiome of land plants.

Plant-soil biodiversity interactions are fundamental for the functioning of terrestrial ecosystems. Yet, the existence of a set of globally distributed topsoil microbial and small invertebrate organisms consistently associated with land plants (i.e., their consistent soil-borne microbiome), together with the environmental preferences and functional capabilities of these organisms, remains unknown. We conducted a standardized field survey under 150 species of land plants, including 58 species of bryophytes and 92 of vascular plants, across 124 locations from all continents. We found that, despite the immense biodiversity of soil organisms, the land plants evaluated only shared a small fraction (less than 1%) of all microbial and invertebrate taxa that were present across contrasting climatic and soil conditions and vegetation types. These consistent taxa were dominated by generalist decomposers and phagotrophs and their presence was positively correlated with the abundance of functional genes linked to mineralization. Finally, we showed that crossing environmental thresholds in aridity (aridity index of 0.65, i.e., the transition from mesic to dry ecosystems), soil pH (5.5; i.e., the transition from acidic to strongly acidic soils), and carbon (less than 2%, the lower limit of fertile soils) can result in drastic disruptions in the associations between land plants and soil organisms, with potential implications for the delivery of soil ecosystem processes under ongoing global environmental change.

Warming-induced shifts in alpine soil microbiome: An ecosystem-scale study with environmental context-dependent insights.

Climate warming is a pressing global issue with substantial impacts on soil health and function. However, the influence of environmental context on the responses of soil microorganisms to warming remains largely elusive, particularly in alpine ecosystems. This study examined the responses of the soil microbiome to in situ experimental warming across three elevations (3850 m, 4100 m, and 4250 m) in the meadow of Gongga Mountain, eastern Tibetan Plateau. Our findings demonstrate that soil microbial diversity is highly resilient to warming, with significant impacts observed only at specific elevations. Furthermore, the influence of warming on the composition of the soil microbial community is also elevation-dependent, underscoring the importance of local environmental context in shaping microbial evolution in alpine soils under climate warming. Notably, we identified soil moisture at 3850 m and carbon-to-nitrogen ratio at 4250 m as indirect predictors regulating the responses of microbial diversity to warming at specific elevations. These findings underscore the paramount importance of considering pre-existing environmental conditions in predicting the response of alpine soil microbiomes to climate warming. Our study provides novel insights into the intricate interactions between climate warming, soil microbiome, and environmental context in alpine ecosystems, illuminating the complex mechanisms governing soil microbial ecology in these fragile and sensitive environments.

Extreme rainfall events eliminate the response of greenhouse gas fluxes to hydrological alterations and fertilization in a riparian ecosystem.

Riparian ecosystems are essential carbon dioxide (CO2) sources, which considerably promotes climate warming. However, the other greenhouse gas fluxes (GHGs), such as methane (CH4) and nitrous oxide (N2O), in the riparian ecosystems have not been well studied, and it remains unclear whether and how these GHG fluxes respond to extreme weather, fertilization and hydrological alterations associated with reservoir management. Here, we assessed the impacts of hydrological alterations (i.e., flooding frequency) and fertilization (nitrogen and/or phosphorus) induced by human activities (hydroengineering construction and agricultural activities) on GHG fluxes, and further investigated the underlying mechanisms in two contrasting years (normal vs. extreme rainfall years) in a reservoir riparian zone dominated by grasses. The significant combined effects of extreme rainfall events and human activities (hydrological alterations and fertilization) on the GHGs were observed. Continuous flooding reduced CO2 emissions by 24% but increased CH4 emissions by ∼4 times in a normal rainfall year. In addition, nitrogen fertilization promoted CO2 emissions by 37%. However, these phenomena were not observed in the year with extreme rainfall events, which made the flooding levels homogeneous across the treatments. Furthermore, we found that CO2 fluxes were driven by the soil moisture, nutrient content, aboveground biomass, and root carbon content, while CH4 and N2O fluxes were merely driven by the soil properties (pH, moisture, and nutrient content). This study provides valuable insights into the crucial role of extreme rainfall events, hydrological alteration, and fertilization in regulating GHG fluxes in riparian ecosystems, as well as supports the integration of these changes in GHG emission models.