Metabolic potential of Nitrososphaera-associated clades.

Soil ammonia-oxidizing archaea (AOA) play a crucial role in converting ammonia to nitrite, thereby mobilizing reactive nitrogen species into their soluble form, with a significant impact on nitrogen losses from terrestrial soils. Yet, our knowledge regarding their diversity and functions remains limited. In this study, we reconstructed 97 high-quality AOA metagenome-assembled genomes (MAGs) from 180 soil samples collected in Central Germany during 2014-2019 summers. These MAGs were affiliated with the order Nitrososphaerales (NS) and clustered into four family-level clades (NS-α/γ/δ/ε). Among these MAGs, 75 belonged to the most abundant but least understood δ-clade. Within the δ-clade, the amoA genes in three MAGs from neutral soils showed a 99.5% similarity to the fosmid clone 54d9, which has served as representative of the δ-clade for the past two decades since even today no cultivated representatives are available. 72 MAGs constituted a distinct δ sub-clade, and their abundance and expression activity were more than twice that of other MAGs in slightly acidic soils. Unlike the less abundant clades (α, γ, and ε), the δ-MAGs possessed multiple highly expressed intracellular and extracellular carbohydrate-active enzymes responsible for carbohydrate binding (CBM32) and degradation (GH5), along with highly expressed genes involved in ammonia oxidation. Together, these results suggest metabolic versatility of uncultured soil AOA and a potential mixotrophic or chemolithoheterotrophic lifestyle among 54d9-like AOA.

Synthesis of recovery patterns in microbial communities across environments.

BACKGROUND: Disturbances alter the diversity and composition of microbial communities. Yet a generalized empirical assessment of microbiome responses to disturbance across different environments is needed to understand the factors driving microbiome recovery, and the role of the environment in driving these patterns. RESULTS: To this end, we combined null models with Bayesian generalized linear models to examine 86 time series of disturbed mammalian, aquatic, and soil microbiomes up to 50 days following disturbance. Overall, disturbances had the strongest effect on mammalian microbiomes, which lost taxa and later recovered their richness, but not their composition. In contrast, following disturbance, aquatic microbiomes tended away from their pre-disturbance composition over time. Surprisingly, across all environments, we found no evidence of increased compositional dispersion (i.e., variance) following disturbance, in contrast to the expectations of the Anna Karenina Principle. CONCLUSIONS: This is the first study to systematically compare secondary successional dynamics across disturbed microbiomes, using a consistent temporal scale and modeling approach. Our findings show that the recovery of microbiomes is environment-specific, and helps to reconcile existing, environment-specific research into a unified perspective. Video Abstract.

Erratum: Universal drivers of cheese microbiomes.

[This corrects the article DOI: 10.1016/j.isci.2022.105744.].

Influence of tree mycorrhizal type, tree species identity, and diversity on forest root-associated mycobiomes.

Understanding the complex interactions between trees and fungi is crucial for forest ecosystem management, yet the influence of tree mycorrhizal types, species identity, and diversity on tree-tree interactions and their root-associated fungal communities remains poorly understood. Our study addresses this gap by investigating root-associated fungal communities of different arbuscular mycorrhizal (AM) and ectomycorrhizal (EcM) tree species pairs (TSPs) in a subtropical tree diversity experiment, spanning monospecific, two-species, and multi-species mixtures, utilizing Illumina sequencing of the ITS2 region. The study reveals that tree mycorrhizal type significantly impacts the alpha diversity of root-associated fungi in monospecific stands. Meanwhile, tree species identity's influence is modulated by overall tree diversity. Tree-related variables and spatial distance emerged as major drivers of variations in fungal community composition. Notably, in multi-species mixtures, compositional differences between root fungal communities of AM and EcM trees diminish, indicating a convergence of fungal communities irrespective of mycorrhizal type. Interestingly, dual mycorrhizal fungal communities were observed in these multi-species mixtures. This research underscores the pivotal role of mycorrhizal partnerships and the interplay of biotic and abiotic factors in shaping root fungal communities, particularly in varied tree diversity settings, and its implications for effective forest management and biodiversity conservation.

Mycorrhizal type and tree diversity affect foliar elemental pools and stoichiometry.

Species-specific differences in nutrient acquisition strategies allow for complementary use of resources among plants in mixtures, which may be further shaped by mycorrhizal associations. However, empirical evidence of this potential role of mycorrhizae is scarce, particularly for tree communities. We investigated the impact of tree species richness and mycorrhizal types, arbuscular mycorrhizal fungi (AM) and ectomycorrhizal fungi (EM), on above- and belowground carbon (C), nitrogen (N), and phosphorus (P) dynamics. Soil and soil microbial biomass elemental dynamics showed weak responses to tree species richness and none to mycorrhizal type. However, foliar elemental concentrations, stoichiometry, and pools were significantly affected by both treatments. Tree species richness increased foliar C and P pools but not N pools. Additive partitioning analyses showed that net biodiversity effects of foliar C, N, P pools in EM tree communities were driven by selection effects, but in mixtures of both mycorrhizal types by complementarity effects. Furthermore, increased tree species richness reduced soil nitrate availability, over 2 yr. Our results indicate that positive effects of tree diversity on aboveground nutrient storage are mediated by complementary mycorrhizal strategies and highlight the importance of using mixtures composed of tree species with different types of mycorrhizae to achieve more multifunctional afforestation.

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.

Trophic interactions in soil micro-food webs drive ecosystem multifunctionality along tree species richness.

Rapid biodiversity losses under global climate change threaten forest ecosystem functions. However, our understanding of the patterns and drivers of multiple ecosystem functions across biodiversity gradients remains equivocal. To address this important knowledge gap, we measured simultaneous responses of multiple ecosystem functions (nutrient cycling, soil carbon stocks, organic matter decomposition, plant productivity) to a tree species richness gradient of 1, 4, 8, 16, and 32 species in a young subtropical forest. We found that tree species richness had negligible effects on nutrient cycling, organic matter decomposition, and plant productivity, but soil carbon stocks and ecosystem multifunctionality significantly increased with tree species richness. Linear mixed-effect models showed that soil organisms, particularly arbuscular mycorrhizal fungi (AMF) and soil nematodes, elicited the greatest relative effects on ecosystem multifunctionality. Structural equation models revealed indirect effects of tree species richness on ecosystem multifunctionality mediated by trophic interactions in soil micro-food webs. Specifically, we found a significant negative effect of gram-positive bacteria on soil nematode abundance (a top-down effect), and a significant positive effect of AMF biomass on soil nematode abundance (a bottom-up effect). Overall, our study emphasizes the significance of a multitrophic perspective in elucidating biodiversity-multifunctionality relationships and highlights the conservation of functioning soil micro-food webs to maintain multiple ecosystem functions.

Plant diversity and community age stabilize ecosystem multifunctionality.

It is well known that biodiversity positively affects ecosystem functioning, leading to enhanced ecosystem stability. However, this knowledge is mainly based on analyses using single ecosystem functions, while studies focusing on the stability of ecosystem multifunctionality (EMF) are rare. Taking advantage of a long-term grassland biodiversity experiment, we studied the effect of plant diversity (1-60 species) on EMF over 5 years, its temporal stability, as well as multifunctional resistance and resilience to a 2-year drought event. Using split-plot treatments, we further tested whether a shared history of plants and soil influences the studied relationships. We calculated EMF based on functions related to plants and higher-trophic levels. Plant diversity enhanced EMF in all studied years, and this effect strengthened over the study period. Moreover, plant diversity increased the temporal stability of EMF and fostered resistance to reoccurring drought events. Old plant communities with shared plant and soil history showed a stronger plant diversity-multifunctionality relationship and higher temporal stability of EMF than younger communities without shared histories. Our results highlight the importance of old and biodiverse plant communities for EMF and its stability to extreme climate events in a world increasingly threatened by global change.

Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding.

Plant diversity effects on community productivity often increase over time. Whether the strengthening of diversity effects is caused by temporal shifts in species-level overyielding (i.e., higher species-level productivity in diverse communities compared with monocultures) remains unclear. Here, using data from 65 grassland and forest biodiversity experiments, we show that the temporal strength of diversity effects at the community scale is underpinned by temporal changes in the species that yield. These temporal trends of species-level overyielding are shaped by plant ecological strategies, which can be quantitatively delimited by functional traits. In grasslands, the temporal strengthening of biodiversity effects on community productivity was associated with increasing biomass overyielding of resource-conservative species increasing over time, and with overyielding of species characterized by fast resource acquisition either decreasing or increasing. In forests, temporal trends in species overyielding differ when considering above- versus belowground resource acquisition strategies. Overyielding in stem growth decreased for species with high light capture capacity but increased for those with high soil resource acquisition capacity. Our results imply that a diversity of species with different, and potentially complementary, ecological strategies is beneficial for maintaining community productivity over time in both grassland and forest ecosystems.

Invasive earthworms shift soil microbial community structure in northern North American forest ecosystems.

Invasive earthworms colonize ecosystems around the globe. Compared to other species' invasions, earthworm invasions have received little attention. Previous studies indicated their tremendous effects on resident soil biota representing a major part of the terrestrial biodiversity. We investigated effects of earthworm invasion on soil microbial communities in three forests in North America by conducting DNA sequencing of soil bacteria, fungi, and protists in two soil depths. Our study shows that microbial diversity was lower in highly invaded forest areas. While bacterial diversity was strongly affected compared to fungi and protists, fungal community composition and family dominance were strongly affected compared to bacteria and protists. We found most species specialized on invasion in fungi, mainly represented by saprotrophs. Comparably, few protist species, mostly bacterivorous, were specialized on invasion. As one of the first observational studies, we investigated earthworm invasion on three kingdoms showing distinct taxa- and trophic level-specific responses to earthworm invasion.

Invasive earthworms can change understory plant community traits and reduce plant functional diversity.

Among the most important impacts of biological invasions on biodiversity is biotic homogenization, which may further compromise key ecosystem processes. However, the extent to which they homogenize functional diversity and shift dominant ecological strategies of invaded communities remains uncertain. Here, we investigated changes in plant communities in a northern North American forest in response to invasive earthworms, by examining the taxonomic and functional diversity of the plant community and soil ecosystem functions. We found that although plant taxonomic diversity did not change in response to invasive earthworms, they modified the dominance structure of plant functional groups. Invasive earthworms promoted the dominance of fast-growing plants at the expense of slow-growing ones. Moreover, earthworms decreased plant functional diversity, which coincided with changes in abiotic and biotic soil properties. Our study reveals that invasive earthworms erode multiple biodiversity facets of invaded forests, with potential cascading effects on ecosystem functioning.

Microbe-induced phenotypic variation leads to overyielding in clonal plant populations.

Overyielding, the high productivity of multispecies plant communities, is commonly seen as the result of plant genetic diversity. Here we demonstrate that biodiversity-ecosystem functioning relationships can emerge in clonal plant populations through interaction with microorganisms. Using a model clonal plant species, we found that exposure to volatiles of certain microorganisms led to divergent plant phenotypes. Assembling communities out of plants associated with different microorganisms led to transgressive overyielding in both biomass and seed yield. Our results highlight the importance of belowground microbial diversity in plant biodiversity research and open new avenues for precision ecosystem management.

Global fine-resolution data on springtail abundance and community structure.

Springtails (Collembola) inhabit soils from the Arctic to the Antarctic and comprise an estimated ~32% of all terrestrial arthropods on Earth. Here, we present a global, spatially-explicit database on springtail communities that includes 249,912 occurrences from 44,999 samples and 2,990 sites. These data are mainly raw sample-level records at the species level collected predominantly from private archives of the authors that were quality-controlled and taxonomically-standardised. Despite covering all continents, most of the sample-level data come from the European continent (82.5% of all samples) and represent four habitats: woodlands (57.4%), grasslands (14.0%), agrosystems (13.7%) and scrublands (9.0%). We included sampling by soil layers, and across seasons and years, representing temporal and spatial within-site variation in springtail communities. We also provided data use and sharing guidelines and R code to facilitate the use of the database by other researchers. This data paper describes a static version of the database at the publication date, but the database will be further expanded to include underrepresented regions and linked with trait data.

Hill-Chao numbers allow decomposing gamma multifunctionality into alpha and beta components.

Biodiversity-ecosystem functioning (BEF) research has provided strong evidence and mechanistic underpinnings to support positive effects of biodiversity on ecosystem functioning, from single to multiple functions. This research has provided knowledge gained mainly at the local alpha scale (i.e. within ecosystems), but the increasing homogenization of landscapes in the Anthropocene has raised the potential that declining biodiversity at the beta (across ecosystems) and gamma scales is likely to also impact ecosystem functioning. Drawing on biodiversity theory, we propose a new statistical framework based on Hill-Chao numbers. The framework allows decomposition of multifunctionality at gamma scales into alpha and beta components, a critical but hitherto missing tool in BEF research; it also allows weighting of individual ecosystem functions. Through the proposed decomposition, new BEF results for beta and gamma scales are discovered. Our novel approach is applicable across ecosystems and connects local- and landscape-scale BEF assessments from experiments to natural settings.

Effects of climate on the distribution and conservation of commonly observed European earthworms.

Belowground biodiversity distribution does not necessarily reflect aboveground biodiversity patterns, but maps of soil biodiversity remain scarce because of limited data availability. Earthworms belong to the most thoroughly studied soil organisms and-in their role as ecosystem engineers-have a significant impact on ecosystem functioning. We used species distribution modeling (SDMs) and available data sets to map the spatial distribution of commonly observed (i.e., frequently recorded) earthworm species (Annelida, Oligochaeta) across Europe under current and future climate conditions. First, we predicted potential species distributions with commonly used models (i.e., MaxEnt and Biomod) and estimated total species richness (i.e., number of species in a 5 × 5 km grid cell). Second, we determined how much the different types of protected areas covered predicted earthworm richness and species ranges (i.e., distributions) by estimating the respective proportion of the range area. Earthworm species richness was high in central western Europe and low in northeastern Europe. This pattern was mainly associated with annual mean temperature and precipitation seasonality, but the importance of predictor variables to species occurrences varied among species. The geographical ranges of the majority of the earthworm species were predicted to shift to eastern Europe and partly decrease under future climate scenarios. Predicted current and future ranges were only poorly covered by protected areas, such as national parks. More than 80% of future earthworm ranges were on average not protected at all (mean [SD] = 82.6% [0.04]). Overall, our results emphasize the urgency of considering especially vulnerable earthworm species, as well as other soil organisms, in the design of nature conservation measures.

Efectos del clima sobre la distribución y conservación de la lombriz de tierra europea Resumen La distribución de la biodiversidad del subsuelo no refleja necesariamente los patrones de biodiversidad, pero los mapas de la biodiversidad del suelo aún son escasos debido a la disponibilidad limitada de datos. Las lombrices son uno de los organismos del suelo más estudiados a detalle­en su papel de ingenieros del ecosistema­y tienen un impacto significativo sobre el funcionamiento de ecosistema. Usamos modelos de distribución de especies (MDE) y conjuntos de datos disponibles para mapear la distribución espacial de las especies (Annelida, Oligochaeta) de lombrices más observadas (es decir, registradas con frecuencia) en toda Europa bajo el clima actual y el futuro. Primero pronosticamos la distribución potencial de las especies con modelos de uso común (MaxEnt y Biomod) y estimamos la riqueza total de especies (número de especies en una cuadrícula de 5 × 5 km). Después determinamos cuánto pronosticaban los diferentes tipos de áreas protegidas contempladas la riqueza de lombrices y la distribución de las especies mediante la estimación de la proporción respectiva del rango del área. La riqueza de especies fue alta en el occidente central y baja en el noreste de Europa. Este patrón estuvo asociado principalmente con la temperatura media anual y la estacionalidad de la precipitación, aunque la importancia de las variables de pronóstico para la presencia de la especie varió entre especies. Se pronosticó que la distribución geográfica de la mayoría de las especies cambiaría al este de Europa y disminuiría parcialmente bajo los escenarios climáticos futuros. El pronóstico de la distribución actual y futura contaba con una cobertura deficiente de las áreas protegidas, como los parques nacionales. En promedio, más del 80% de la distribución futura de las lombrices no estaba protegido (promedio [SD] = 82.6% [0.04]). En general, nuestros resultados destacan la urgencia por considerar a las especies vulnerables de lombrices, así como a otros organismos del suelo, en el diseño de las medidas de conservación.

Climate-dependent plant responses to earthworms in two land-use types.

Plant nutrient uptake and productivity are driven by a multitude of factors that have been modified by human activities, like climate change and the activity of decomposers. However, interactive effects of climate change and key decomposer groups like earthworms have rarely been studied. In a field microcosm experiment, we investigated the effects of a mean future climate scenario with warming (+ 0.50 °C to + 0.62 °C) and altered precipitation (+ 10% in spring and autumn, - 20% in summer) and earthworms (anecic-two Lumbricus terrestris, endogeic-four Allolobophora chlorotica and both together within 10 cm diameter tubes) on plant biomass and stoichiometry in two land-use types (intensively used meadow and conventional farming). We found little evidence for earthworm effects on aboveground biomass. However, future climate increased above- (+40.9%) and belowground biomass (+44.7%) of grass communities, which was mainly driven by production of the dominant Festulolium species during non-summer drought periods, but decreased the aboveground biomass (- 36.9%) of winter wheat. Projected climate change and earthworms interactively affected the N content and C:N ratio of grasses. Earthworms enhanced the N content (+1.2%) thereby decreasing the C:N ratio (- 4.1%) in grasses, but only under ambient climate conditions. The future climate treatment generally decreased the N content of grasses (aboveground: - 1.1%, belowground: - 0.15%) and winter wheat (- 0.14%), resulting in an increase in C:N ratio of grasses (aboveground: + 4.2%, belowground: +6.3%) and wheat (+5.9%). Our results suggest that climate change diminishes the positive effects of earthworms on plant nutrient uptakes due to soil water deficit, especially during summer drought.

Drivers of soil microbial and detritivore activity across global grasslands.

Covering approximately 40% of land surfaces, grasslands provide critical ecosystem services that rely on soil organisms. However, the global determinants of soil biodiversity and functioning remain underexplored. In this study, we investigate the drivers of soil microbial and detritivore activity in grasslands across a wide range of climatic conditions on five continents. We apply standardized treatments of nutrient addition and herbivore reduction, allowing us to disentangle the regional and local drivers of soil organism activity. We use structural equation modeling to assess the direct and indirect effects of local and regional drivers on soil biological activities. Microbial and detritivore activities are positively correlated across global grasslands. These correlations are shaped more by global climatic factors than by local treatments, with annual precipitation and soil water content explaining the majority of the variation. Nutrient addition tends to reduce microbial activity by enhancing plant growth, while herbivore reduction typically increases microbial and detritivore activity through increased soil moisture. Our findings emphasize soil moisture as a key driver of soil biological activity, highlighting the potential impacts of climate change, altered grazing pressure, and eutrophication on nutrient cycling and decomposition within grassland ecosystems.

Plant diversity and soil legacy independently affect the plant metabolome and induced responses following herbivory.

Plant and soil biodiversity can have significant effects on herbivore resistance mediated by plant metabolites. Here, we disentangled the independent effects of plant diversity and soil legacy on constitutive and herbivore-induced plant metabolomes of three plant species in two complementary microcosm experiments. First, we grew plants in sterile soil with three different plant diversity levels. Second, single plant species were grown on soil with different plant diversity-induced soil legacies. We infested a subset of all plants with Spodoptera exigua larvae, a generalist leaf-chewing herbivore, and assessed foliar and root metabolomes. Neither plant diversity nor soil legacy had significant effects on overall foliar, root, or herbivore-induced metabolome composition. Herbivore-induced metabolomes, however, differed from those of control plants. We detected 139 significantly regulated metabolites by comparing plants grown in monocultures with conspecifics growing in plant or soil legacy mixtures. Moreover, plant-plant and plant-soil interactions regulated 141 metabolites in herbivore-induced plants. Taken together, plant diversity and soil legacy independently alter the concentration and induction of plant metabolites, thus affecting the plant's defensive capability. This is a first step toward disentangling plant and soil biodiversity effects on herbivore resistance, thereby improving our understanding of the mechanisms that govern ecosystem functioning.