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.

Soil contamination in nearby natural areas mirrors that in urban greenspaces worldwide.

Soil contamination is one of the main threats to ecosystem health and sustainability. Yet little is known about the extent to which soil contaminants differ between urban greenspaces and natural ecosystems. Here we show that urban greenspaces and adjacent natural areas (i.e., natural/semi-natural ecosystems) shared similar levels of multiple soil contaminants (metal(loid)s, pesticides, microplastics, and antibiotic resistance genes) across the globe. We reveal that human influence explained many forms of soil contamination worldwide. Socio-economic factors were integral to explaining the occurrence of soil contaminants worldwide. We further show that increased levels of multiple soil contaminants were linked with changes in microbial traits including genes associated with environmental stress resistance, nutrient cycling, and pathogenesis. Taken together, our work demonstrates that human-driven soil contamination in nearby natural areas mirrors that in urban greenspaces globally, and highlights that soil contaminants have the potential to cause dire consequences for ecosystem sustainability and human wellbeing.

Soil biodiversity supports the delivery of multiple ecosystem functions in urban greenspaces.

While the contribution of biodiversity to supporting multiple ecosystem functions is well established in natural ecosystems, the relationship of the above- and below-ground diversity with ecosystem multifunctionality remains virtually unknown in urban greenspaces. Here we conducted a standardized survey of urban greenspaces from 56 municipalities across six continents, aiming to investigate the relationships of plant and soil biodiversity (diversity of bacteria, fungi, protists and invertebrates, and metagenomics-based functional diversity) with 18 surrogates of ecosystem functions from nine ecosystem services. We found that soil biodiversity across biomes was significantly and positively correlated with multiple dimensions of ecosystem functions, and contributed to key ecosystem services such as microbially driven carbon pools, organic matter decomposition, plant productivity, nutrient cycling, water regulation, plant-soil mutualism, plant pathogen control and antibiotic resistance regulation. Plant diversity only indirectly influenced multifunctionality in urban greenspaces via changes in soil conditions that were associated with soil biodiversity. These findings were maintained after controlling for climate, spatial context, soil properties, vegetation and management practices. This study provides solid evidence that conserving soil biodiversity in urban greenspaces is key to supporting multiple dimensions of ecosystem functioning, which is critical for the sustainability of urban ecosystems and human wellbeing.

The global distribution and environmental drivers of the soil antibiotic resistome.

BACKGROUND: Little is known about the global distribution and environmental drivers of key microbial functional traits such as antibiotic resistance genes (ARGs). Soils are one of Earth's largest reservoirs of ARGs, which are integral for soil microbial competition, and have potential implications for plant and human health. Yet, their diversity and global patterns remain poorly described. Here, we analyzed 285 ARGs in soils from 1012 sites across all continents and created the first global atlas with the distributions of topsoil ARGs. RESULTS: We show that ARGs peaked in high latitude cold and boreal forests. Climatic seasonality and mobile genetic elements, associated with the transmission of antibiotic resistance, were also key drivers of their global distribution. Dominant ARGs were mainly related to multidrug resistance genes and efflux pump machineries. We further pinpointed the global hotspots of the diversity and proportions of soil ARGs. CONCLUSIONS: Together, our work provides the foundation for a better understanding of the ecology and global distribution of the environmental soil antibiotic resistome. Video Abstract.

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.

Persistence and spread of tetracycline resistance genes and microbial community variations in the soil of animal corrals in a semi-arid planted forest.

At the spring, goat and sheep herds are transferred to planted forests, in a semi-arid region in the northern Negev Desert, Israel, to reduce herbaceous biomass and, fire risk. The herds are held overnight in corrals for about 4 months, enriching the soil with organic matter and nitrogen. This research examined the effect of these enrichments on soil bacterial community structure (BCS) and the abundance of tetracycline resistance genes (TRGs) in active and abandoned corrals (1-10-years-old). Based on 16S rRNA gene sequences, the Proteobacteria and Actinobacteria phyla dominated the soil of all corrals. The Actinobacteria were less abundant in the active and 1-year-old corrals (23-26%) than in the other corrals and the control (33-38%). A principal component analysis showed that, the BCS in the active and the 1-year-old abandoned corrals was significantly different from that in the older corrals and the control. The Firmicutes phylum constituted 28% of the BCS in the active corrals, 12.5% in the 1-year-old corrals and 2% in the older corrals and the control. In contrast, the Acidobacteria phylum was hardly detected in the active and 1-year-old abandoned corrals and constituted 10% of the BCS in the older corrals. Genes conferring resistance to tetracycline were detected in high numbers. The tetG and tetW genes were detected in the active and abandoned corrals (1-10 years). The tetQ gene was detected only in the active and 1-year-old abandoned corrals. None of the genes were detected in the control soil. The three genes were detected outside an active corral, in the downstream section of an ephemeral tributary. The results prove that abandoned and unobserved periodic animal corrals are an environmental reservoir for TRGs.

Global homogenization of the structure and function in the soil microbiome of urban greenspaces.

The structure and function of the soil microbiome of urban greenspaces remain largely undetermined. We conducted a global field survey in urban greenspaces and neighboring natural ecosystems across 56 cities from six continents, and found that urban soils are important hotspots for soil bacterial, protist and functional gene diversity, but support highly homogenized microbial communities worldwide. Urban greenspaces had a greater proportion of fast-growing bacteria, algae, amoebae, and fungal pathogens, but a lower proportion of ectomycorrhizal fungi than natural ecosystems. These urban ecosystems also showed higher proportions of genes associated with human pathogens, greenhouse gas emissions, faster nutrient cycling, and more intense abiotic stress than natural environments. City affluence, management practices, and climate were fundamental drivers of urban soil communities. Our work paves the way toward a more comprehensive global-scale perspective on urban greenspaces, which is integral to managing the health of these ecosystems and the well-being of human populations.

Plant species-area relationships are determined by evenness, cover and aggregation in drylands worldwide.

AIM: Species-area relationships (also known as 'species-area curves' and 'species accumulation curves') represent the relationship between species richness and the area sampled in a given community. These relationships can be used to describe diversity patterns while accounting for the well-known scale-dependence of species richness. Despite their value, their functional form and parameters, as well as their determinants, have barely been investigated in drylands. LOCATION: 171 drylands from all continents except Antarctica. TIME PERIOD: 2006-2013. MAJOR TAXA STUDIED: Perennial plants. METHODS: We characterized species-area relationships of plant communities by building accumulation curves describing the expected number of species as a function of the number of sampling units, and later compared the fit of three functions (power-law, logarithmic and Michaelis-Menten). We tested the prediction that the effects of aridity, soil pH on SAR are mediated by vegetation attributes such as evenness, cover, and spatial aggregation. RESULTS: We found that the logarithmic relationship was the most common functional form (c.50%), followed by Michaelis-Menten (c.33%) and power-law (c.17%). Functional form was mainly determined by evenness. Power-law relationships were found mostly under low evenness, logarithmic relationships peaked under intermediate evenness and the Michalis-Menten function increased in frequency with increasing evenness. The SAR parameters approximated by the logarithmic model ('small-scale richness' (b0 ) and 'accumulation coefficient' (b1 )) were determined by vegetation attributes. Increasing spatial aggregation had a negative effect on the small-scale richness and a positive effect on the accumulation coefficient, while evenness had an opposite effect. In addition, accumulation coefficient was positively affected by cover. Interestingly, aridity decreased small scale richness but did not affect the accumulation coefficient. MAIN CONCLUSIONS: Our findings highlight the role of evenness, spatial aggregation and cover as main drivers of species area relationships in drylands, the Earth's largest biome.

In vitro exposure of nasal epithelial cells to atmospheric dust.

Dust storms are common phenomena in many parts of the world, and significantly increase the level of atmospheric particulate matter (PM). The soil-derived dust is a mixture of organic and inorganic particles and even remnants of pesticides from agricultural areas nearby. The risk of human exposure to atmospheric dust is well documented, but very little is known on the impact of inhaled PM on the biological lining of the nasal cavity, which is the natural filter between the external environment and the respiratory tract. We developed a new system and methodology for in vitro exposure of cultured nasal epithelial cells (NEC) to atmospheric soil-dust pollutants under realistic and controlled laboratory simulations that mimic nasal breathing. We exposed cultured NEC to clean and dust-polluted airflows that mimic physiological conditions. The results revealed that the secretion of mucin and IL-8 from the NEC exposed to clean and dust-polluted airflows was less than the secretion at static conditions under clean air. The secretion of IL-8 from NEC exposed to dust-polluted air was larger than that of clean air, but not larger than in the static case. The experiments with dust air pollution that also contained agricultural pesticides did not reveal differences in the secretion of mucin and IL-8 as compared to the same pollution without pesticides.

Light asymmetry explains the effect of nutrient enrichment on grassland diversity.

One of the most ubiquitous patterns in plant ecology is species loss following nutrient enrichment. A common explanation for this universal pattern is an increase in the size asymmetry of light partitioning (the degree to which large plants receive more light per unit biomass than smaller plants), which accelerates the rates of competitive exclusions. This 'light asymmetry hypothesis' has been confirmed by mathematical models, but has never been tested in natural communities due to the lack of appropriate methodology for measuring the size asymmetry of light partitioning in natural communities. Here, we use a novel approach for quantifying the asymmetry of light competition which is based on measurements of the vertical distribution of light below the canopy. Using our approach, we demonstrate that an increase in light asymmetry is the main mechanism behind the negative effect of nutrient enrichment on species richness. Our results provide a possible explanation for one of the main sources of contemporary species loss in terrestrial plant communities.

Characterization of Morphology, Volatile Profiles, and Molecular Markers in Edible Desert Truffles from the Negev Desert.

Desert truffles are mycorrhizal, hypogeous fungi considered a delicacy. On the basis of morphological characters, we identified three desert truffle species that grow in the same habitat in the Negev desert. These include Picoa lefebvrei (Pat.), Tirmania nivea (Desf.) Trappe, and Terfezia boudieri (Chatain), all associated with Helianthemum sessiliflorum. Their taxonomy was confirmed by PCR-RFLP. The main volatiles of fruit bodies of T. boudieri and T. nivea were 1-octen-3-ol and hexanal; however, volatiles of the latter species further included branched-chain amino acid derivatives such as 2-methylbutanal and 3-methylbutanal, phenylalanine derivatives such as benzaldehyde and benzenacetaldehyde, and methionine derivatives such as methional and dimethyl disulfide. The least aromatic truffle, P. lefebvrei, contained low levels of 1-octen-3-ol as the main volatile. Axenic mycelia cultures of T. boudieri displayed a simpler volatile profile compared to its fruit bodies. This work highlights differences in the volatile profiles of desert truffles and could hence be of interest for selecting and cultivating genotypes with the most likable aroma.

Livestock grazing impact on soil wettability and erosion risk in post-fire agricultural lands.

Fires in agricultural areas are common, modifying the functioning of agro-ecosystems. Such fires have been extensively studied, and reported to considerably affect soil properties. Yet, understanding of the impact of livestock grazing, or more precisely, trampling, in fire-affected lands is limited. The objective of this study was to assess the impact of low- to moderate-fire severity and livestock trampling (hoof action) on the solid soil's wettability and related properties, and on soil detachment, in burnt vs. non-burnt croplands. The study was implemented by allowing livestock to access plots under high, medium, and low stocking rates in (unintentionally) burnt and non-burnt lands. Also, livestock exclusion plots were assigned as a control treatment. Results showed that fire slightly decreased the soil wettability. At the same time, water drop penetration time (WDPT) was negatively related to the stocking rate, and critical surface tension (CST) was ~13% smaller in the control plots than in the livestock-presence treatments. Also, the results showed that following burning, the resistance of soil to shear decreased by ~70%. Mass of detached material was similar in the control plots of the burnt and non-burnt plots. At the same time, it was three-, eight-, and nine-fold greater in the plots of the burnt×low, burnt×medium, and burnt×high stocking rates, respectively, than in the corresponding non-burnt ones. This study shows that livestock trampling in low- to moderate-intensity fire-affected lands increased the shearing of the ground surface layer. On the one hand, this slightly increased soil wettability. On the other hand, this impact considerably increased risks of soil erosion and land degradation.

The role of pre-symbiotic auxin signaling in ectendomycorrhiza formation between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum.

The ectendomycorrhizal fungus Terfezia boudieri is known to secrete auxin. While some of the effects of fungal auxin on the plant root system have been described, a comprehensive understanding is still lacking. A dual culture system to study pre mycorrhizal signal exchange revealed previously unrecognized root-fungus interaction mediated by the fungal auxin. The secreted fungal auxin induced negative taproot gravitropism, attenuated taproot growth rate, and inhibited initial host development. Auxin also induced expression of Arabidopsis carriers AUX1 and PIN1, both of which are involved in the gravitropic response. Exogenous application of auxin led to a root phenotype, which fully mimicked that induced by ectomycorrhizal fungi. Co-cultivation of Arabidopsis auxin receptor mutants tir1-1, tir1-1 afb2-3, tir1-1 afb1-3 afb2-3, and tir1-1 afb2-3 afb3-4 with Terfezia confirmed that auxin induces the observed root phenotype. The finding that auxin both induces taproot deviation from the gravity axis and coordinates growth rate is new. We propose a model in which the fungal auxin induces horizontal root development, as well as the coordination of growth rates between partners, along with the known auxin effect on lateral root induction that increases the availability of accessible sites for colonization at the soil plane of fungal spore abundance. Thus, the newly observed responses described here of the root to Terfezia contribute to a successful encounter between symbionts.

Increasing aridity reduces soil microbial diversity and abundance in global drylands.

Soil bacteria and fungi play key roles in the functioning of terrestrial ecosystems, yet our understanding of their responses to climate change lags significantly behind that of other organisms. This gap in our understanding is particularly true for drylands, which occupy ∼41% of Earth´s surface, because no global, systematic assessments of the joint diversity of soil bacteria and fungi have been conducted in these environments to date. Here we present results from a study conducted across 80 dryland sites from all continents, except Antarctica, to assess how changes in aridity affect the composition, abundance, and diversity of soil bacteria and fungi. The diversity and abundance of soil bacteria and fungi was reduced as aridity increased. These results were largely driven by the negative impacts of aridity on soil organic carbon content, which positively affected the abundance and diversity of both bacteria and fungi. Aridity promoted shifts in the composition of soil bacteria, with increases in the relative abundance of Chloroflexi and α-Proteobacteria and decreases in Acidobacteria and Verrucomicrobia. Contrary to what has been reported by previous continental and global-scale studies, soil pH was not a major driver of bacterial diversity, and fungal communities were dominated by Ascomycota. Our results fill a critical gap in our understanding of soil microbial communities in terrestrial ecosystems. They suggest that changes in aridity, such as those predicted by climate-change models, may reduce microbial abundance and diversity, a response that will likely impact the provision of key ecosystem services by global drylands.

Climate and soil attributes determine plant species turnover in global drylands.

AIM: Geographic, climatic, and soil factors are major drivers of plant beta diversity, but their importance for dryland plant communities is poorly known. This study aims to: i) characterize patterns of beta diversity in global drylands, ii) detect common environmental drivers of beta diversity, and iii) test for thresholds in environmental conditions driving potential shifts in plant species composition. LOCATION: 224 sites in diverse dryland plant communities from 22 geographical regions in six continents. METHODS: Beta diversity was quantified with four complementary measures: the percentage of singletons (species occurring at only one site), Whittake's beta diversity (ß(W)), a directional beta diversity metric based on the correlation in species occurrences among spatially contiguous sites (ß(R2)), and a multivariate abundance-based metric (ß(MV)). We used linear modelling to quantify the relationships between these metrics of beta diversity and geographic, climatic, and soil variables. RESULTS: Soil fertility and variability in temperature and rainfall, and to a lesser extent latitude, were the most important environmental predictors of beta diversity. Metrics related to species identity (percentage of singletons and ß(W)) were most sensitive to soil fertility, whereas those metrics related to environmental gradients and abundance ((ß(R2)) and ß(MV)) were more associated with climate variability. Interactions among soil variables, climatic factors, and plant cover were not important determinants of beta diversity. Sites receiving less than 178 mm of annual rainfall differed sharply in species composition from more mesic sites (> 200 mm). MAIN CONCLUSIONS: Soil fertility and variability in temperature and rainfall are the most important environmental predictors of variation in plant beta diversity in global drylands. Our results suggest that those sites annually receiving ~ 178 mm of rainfall will be especially sensitive to future climate changes. These findings may help to define appropriate conservation strategies for mitigating effects of climate change on dryland vegetation.

Spatial and temporal diversity and abundance of ammonia oxidizers in semi-arid and arid soils: indications for a differential seasonal effect on archaeal and bacterial ammonia oxidizers.

Besides water, nitrogen is the limiting factor for biomass production in arid ecosystems. Global climatic changes are exacerbating aridity levels, and the response of nitrogen-transforming microorganisms to these changes is not clear yet. Using semi-arid and arid ecosystems as surrogates for conditions of increased aridity, we investigated the activity, abundance, and diversity of ammonia-oxidizing bacteria (AOB) and archaea (AOA) in arid and semi-arid soils. Ammonia oxidation potentials were higher during the winter in both sites than in the summer, and higher nitrate concentrations were measured in the arid soil than in the semi-arid soil. Denaturing gradient gel electrophoresis (DGGE) patterns of AOB 16S rRNA gene fragments were similar for the arid and semi-arid soils with no seasonal variations. In contrast, the DGGE patterns of the AOA amoA gene fragments differed between the sites and a soil transfer experiment suggested that these differences are possibly associated with soil type. AOB numbers were higher during the winter than in the summer, while AOA numbers were higher during the summer. The results indicate the resistance of AOB and AOA community structure to arid conditions, albeit with seasonal variations in their abundance. Together, the results suggest the resilience of nitrification activity to increased aridity level.

Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses.

Arid and semi-arid ecosystems are often characterized by vegetation patchiness and variable availability of resources. Phospholipid fatty acid (PLFA) and 16S rRNA gene fragment analyses were used to compare the bulk soil microbial community structure at patchy arid and semi-arid landscapes. Multivariate analyses of the PLFA data and the 16S rRNA gene fragments were in agreement with each other, suggesting that the differences between bulk soil microbial communities were primarily related to shrub vs intershrub patches, irrespective of climatic or site differences. This suggests that the mere presence of a living shrub is the dominant driving factor for the differential adaptation of the microbial communities. Lipid markers suggested as indicators of Gram-positive bacteria were higher in soils under the shrub canopies, while markers suggested as indicators of cyanobacteria and anaerobic bacteria were elevated in the intershrub soils. Secondary differences between soil microbial communities were associated with intershrub characteristics and to a lesser extent with the shrub species. This study provides an insight into the multifaceted nature of the factors that shape the microbial community structure in patchy desert landscapes. It further suggests that these drivers not only act in concert but also in a way that is dependent on the aridity level.

Weekly variation of atmospheric particle micromorphology and chemistry in Brussels urban environment.

The purpose of this study was to measure the impact of urban activities on airborne particle dynamics during weekend periods in Brussels urban area. Differences in the granulometry and micromorphology between particles sampled on working days and weekends were studied. We quantified the area, size, number, and the chemistry parameters of the airborne particles and compared between Saturday, Sunday, and Monday. We report and analyze data on airborne particles up to PM10, measured in the Brussels region from October 2002 to September 2003. Our investigation reveals detailed information regarding chemical composition of the airborne particles over the weekend period in the Brussels urban area. Furthermore, the majority of the airborne particles in the Brussels region may belong to sources geographically outside the (in situ) Brussels area.