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.

Description, identification, and growth of Tuber borchii Vittad. mycorrhized Pinus sylvestris L. seedlings on different lime contents.

Tuber borchii forms ectomycorrhiza with oaks, hazel, and pines, including Pinus sylvestris. However, its ectomycorrhiza morphotype with P. sylvestris was not comprehensively described so far, and molecular analyses are missing despite a high danger of misidentification of T. borchii ectomycorrhiza with other closely related and less valuable truffle species. We described for the first time the morphology and anatomy of T. borchii-P. sylvestris ectomycorrhiza using differential interference contrast technique and semi-thin sections in combination with molecular confirmation of identity. Color of ectomycorrhiza is reddish to dark brown, and morphotypes are unevenly but densely covered by warts-bearing pin-like cystidia. All layers of the hyphal mantle are pseudoparenchymatous with outer mantle layer formed of epidermoid cells. T. borchii ectomycorrhiza was identified by a molecular comparison with fruitbodies used for inoculation and its respective ectomycorrhizae. T. borchii has a wide ecological amplitude. To get a better insight in mycorrhization requirements, we investigated growth of P. sylvestris and its ectomycorrhiza infection rate with T. borchii in substrate with different lime content. The mycorrhization of P. sylvestris with T. borchii in the mycorrhization substrate and cultivation in greenhouse conditions was successful, with colonization of P. sylvestris varying between 36.5 and 48.1%. There was no significant correlation of mycorrhization to applied lime contents, and consequently to pH in substrate, while the increased levels of lime improved growth of the P. sylvestris seedlings.

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.

Effects of Desiccation and Freezing on Microbial Ionizing Radiation Survivability: Considerations for Mars Sample Return.

Increasingly, national space agencies are expanding their goals to include Mars exploration with sample return. To better protect Earth and its biosphere from potential extraterrestrial sources of contamination, as set forth in the Outer Space Treaty of 1967, international efforts to develop planetary protection measures strive to understand the danger of cross-contamination processes in Mars sample return missions. We aim to better understand the impact of the martian surface on microbial dormancy and survivability. Radiation resistance of microbes is a key parameter in considering survivability of microbes over geologic times on the frigid, arid surface of Mars that is bombarded by solar and galactic cosmic radiation. We tested the influence of desiccation and freezing on the ionizing radiation survival of six model microorganisms: vegetative cells of two bacteria (Deinococcus radiodurans, Escherichia coli) and a strain of budding yeast (Saccharomyces cerevisiae); and vegetative cells and endospores of three Bacillus bacteria (B. subtilis, B. megaterium, B. thuringiensis). Desiccation and freezing greatly increased radiation survival of vegetative polyploid microorganisms when applied separately, and when combined, desiccation and freezing increased radiation survival even more so. Thus, the radiation survival threshold of polyploid D. radiodurans cells can be extended from the already high value of 25 kGy in liquid culture to an astonishing 140 kGy when the cells are both desiccated and frozen. However, such synergistic radioprotective effects of desiccation and freezing were not observed in monogenomic or digenomic Bacillus cells and endospores, which are generally sterilized by 12 kGy. This difference is associated with a critical requirement for survivability under radiation, that is, repair of genome damage caused by radiation. Deinococcus radiodurans and S. cerevisiae accumulate similarly high levels of the Mn antioxidants that are required for extreme radiation resistance, as do endospores, though they greatly exceed spores in radioresistance because they contain multiple identical genome copies, which in D. radiodurans are joined by persistent Holliday junctions. We estimate ionizing radiation survival limits of polyploid DNA-based life-forms to be hundreds of millions of years of background radiation while buried in the martian subsurface. Our findings imply that forward contamination of Mars will essentially be permanent, and backward contamination is a possibility if life ever existed on Mars.

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.

Distribution and phylogeography of the genus Mattirolomyces with a focus on the Asian M. terfezioides haplotypes.

Mattirolomyces is an edible commercial sequestrate genus that is globally distributed. From the five described taxa of this genus, Mattirolomyces terfezioides is the most common species in Asia. Our recent attempts to locate M. terfezioides outside its current distribution area in China documented its first records in areas of poplar trees with the lowest known temperature and precipitation averages ever recorded for this species. This peculiar ecology was not reflected on the species-morphological features nor on its phylogenetic position in the genus. The first attempt to apply the phylogenetic network approach to Mattirolomyces revealed its geographic origin in the Asian-Pacific areas prior to frequent long-distance migration events. Based on data from recent study areas, we found that the collections from Inner Mongolia and the Shanxi province were similar to European collections. Asian haplotypes were less distant from the outgroup comparing to collections from Europe, supporting the hypothesis that M. terfezioides was originated from this Chinese area and was subsequently transported to Europe. Exploring M. terfezioides ecology and its mycorrhiza potential to grow in association with poplars would be of great importance for planning cultivation projects of this valuable desert truffle species in Central and Eastern China, a currently underexploited economic sector that deserves further ecological and M. terfezioides mycorrhizal synthesis investigations.

Interplay of plastic pollution with algae and plants: hidden danger or a blessing?

In the era of plastic pollution, plants have been discarded as a system that is not affected by micro and nanoplastics, but contrary to beliefs that plants cannot absorb plastic particles, recent research proved otherwise. The presented review gives insight into known aspects of plants' interplay with plastics and how plants' ability to absorb plastic particles can be utilized to remove plastics from water and soil systems. Microplastics usually cannot be absorbed by plant root systems due to their size, but some reports indicate they might enter plant tissues through stomata. On the other hand, nanoparticles can enter plant root systems, and reports of their transport via xylem to upper plant parts have been recorded. Bioaccumulation of nanoplastics in upper plant parts is still not confirmed. The prospects of using biosystems for the remediation of soils contaminated with plastics are still unknown. However, algae could be used to degrade plastic particles in water systems through enzyme facilitated degradation processes. Considering the amount of plastic pollution, especially in the oceans, further research is necessary on the utilization of algae in plastic degradation. Special attention should be given to the research concerning utilization of algae with restricted algal growth, ensuring that a different problem is not induced, "sea blooming", during the degradation of plastics.

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.

Effect of earthworms on mycorrhization, root morphology and biomass of silver fir seedlings inoculated with black summer truffle (Tuber aestivum Vittad.).

Species of the genus Tuber have gained a lot of attention in recent decades due to their aromatic hypogenous fruitbodies, which can bring high prices on the market. The tendency in truffle production is to infect oak, hazel, beech, etc. in greenhouse conditions. We aimed to show whether silver fir (Abies alba Mill.) can be an appropriate host partner for commercial mycorrhization with truffles, and how earthworms in the inoculation substrate would affect the mycorrhization dynamics. Silver fir seedlings inoculated with Tuber. aestivum were analyzed for root system parameters and mycorrhization, how earthworms affect the bare root system, and if mycorrhization parameters change when earthworms are added to the inoculation substrate. Seedlings were analyzed 6 and 12 months after spore inoculation. Mycorrhization with or without earthworms revealed contrasting effects on fine root biomass and morphology of silver fir seedlings. Only a few of the assessed fine root parameters showed statistically significant response, namely higher fine root biomass and fine root tip density in inoculated seedlings without earthworms 6 months after inoculation, lower fine root tip density when earthworms were added, the specific root tip density increased in inoculated seedlings without earthworms 12 months after inoculation, and general negative effect of earthworm on branching density. Silver fir was confirmed as a suitable host partner for commercial mycorrhization with truffles, with 6% and 35% mycorrhization 6 months after inoculation and between 36% and 55% mycorrhization 12 months after inoculation. The effect of earthworms on mycorrhization of silver fir with Tuber aestivum was positive only after 6 months of mycorrhization, while this effect disappeared and turned insignificantly negative after 12 months due to the secondary effect of grazing on ectomycorrhizal root tips.

First report of European truffle ectomycorrhiza in the semi-arid climate of Saudi Arabia.

Tuber melanosporum Vittad. (Black or Périgord truffle) is a truffle native to the Mediterranean Southern Europe, popular for its unique flavor, and has great economic importance. The present work focused on assessing the possibility of cultivating T. melanosporum associated with Quercus robur L. in the desert climate of Saudi Arabia. The plantation was initiated in November 2018 by planting 271 oak seedlings in the Al-Qassim desert area and checked for survival and ectomycorrhiza development after 1.5 years of plantation maintenance. Amongst the 271 seedlings planted, 243 plants survived two harsh seasons (2019 and 2020), and the randomly selected and tested seedlings were still mycorrhized with T. melanosporum. The mycorrhization level with T. melanosporum was between 5 and 35% of all fine roots, and the share of contaminant ectomycorrhiza was low. In comparison to other areas where T. melanosporum is successfully cultivated, the Al-Qassim desert area has 10-15 °C higher average summer temperatures and a low total annual precipitation, which necessitates regular irrigation of the plantation. This work opens the avenue for an adapted, yet sustainable cultivation of T. melanosporum-inoculated oak tree in a desert climatic condition and introduces new opportunities of the agro-forest business in Saudi Arabia and GCC region.

KEYLINK: towards a more integrative soil representation for inclusion in ecosystem scale models. I. review and model concept.

The relatively poor simulation of the below-ground processes is a severe drawback for many ecosystem models, especially when predicting responses to climate change and management. For a meaningful estimation of ecosystem production and the cycling of water, energy, nutrients and carbon, the integration of soil processes and the exchanges at the surface is crucial. It is increasingly recognized that soil biota play an important role in soil organic carbon and nutrient cycling, shaping soil structure and hydrological properties through their activity, and in water and nutrient uptake by plants through mycorrhizal processes. In this article, we review the main soil biological actors (microbiota, fauna and roots) and their effects on soil functioning. We review to what extent they have been included in soil models and propose which of them could be included in ecosystem models. We show that the model representation of the soil food web, the impact of soil ecosystem engineers on soil structure and the related effects on hydrology and soil organic matter (SOM) stabilization are key issues in improving ecosystem-scale soil representation in models. Finally, we describe a new core model concept (KEYLINK) that integrates insights from SOM models, structural models and food web models to simulate the living soil at an ecosystem scale.

Blind spots in global soil biodiversity and ecosystem function research.

Soils harbor a substantial fraction of the world's biodiversity, contributing to many crucial ecosystem functions. It is thus essential to identify general macroecological patterns related to the distribution and functioning of soil organisms to support their conservation and consideration by governance. These macroecological analyses need to represent the diversity of environmental conditions that can be found worldwide. Here we identify and characterize existing environmental gaps in soil taxa and ecosystem functioning data across soil macroecological studies and 17,186 sampling sites across the globe. These data gaps include important spatial, environmental, taxonomic, and functional gaps, and an almost complete absence of temporally explicit data. We also identify the limitations of soil macroecological studies to explore general patterns in soil biodiversity-ecosystem functioning relationships, with only 0.3% of all sampling sites having both information about biodiversity and function, although with different taxonomic groups and functions at each site. Based on this information, we provide clear priorities to support and expand soil macroecological research.

Diversity trapped in cages: Revision of Blumenavia Möller (Clathraceae, Basidiomycota) reveals three hidden species.

Basidiomata of Phallales have a diversified morphology with adhesive gleba that exudes an odor, usually unpleasant that attracts mainly insects, which disperse the basidiospores. The genus Blumenavia belongs to the family Clathraceae and, based on morphological features, only two species are currently recognized: B. rhacodes and B. angolensis. However, the morphological characters adopted in species delimitations within this genus are inconsistent, and molecular data are scarce. The present study aimed to review and identify informative characters that contribute to the delimitation of Blumenavia species. Exsiccates from America and Africa were analyzed morphologically, and molecularly, using ITS, LSU, ATP6, RPB2 and TEF-1α markers for Maximum Parsimony, Bayesian and Maximum likelihood analyses, and also for coalescent based species delimitations (BP&P), as well as for bPTP, PhyloMap, Topo-phylogenetic and Geophylogenetic reconstructions. According to our studies, seven species can be considered in the genus: B. rhacodes and B. angolensis are maintained, B. usambarensis and B. toribiotalpaensis are reassessed, and three new species are proposed, B. baturitensis Melanda, M.P. Martín & Baseia, sp. nov., B. crucis-hellenicae G. Coelho, Sulzbacher, Grebenc & Cortez, sp. nov., and B. heroica Melanda, Baseia & M.P. Martín, sp. nov. Blumenavia rhacodes is typified by selecting a lectotype and an epitype. Macromorphological characters considered informative to segregate and delimit the species through integrative taxonomy include length of the basidiomata, color, width and presence of grooves on each arm as well as the glebifer position and shape. These must be clearly observed while the basidiomata are still fresh. Since most materials are usually analyzed after dehydration and deposit in collections, field techniques and protocols to describe fugacious characters from fresh specimen are demanded, as well as the use of molecular analysis, in order to better assess recognition and delimitation of species in Blumenavia.

Species and geographic variability in truffle aromas.

The gastronomic relevance and price of truffles are related mainly to its unique aroma. In this study, we explore the impact that different volatile compounds have on the aroma quality of fresh truffles using gas chromatography-mass spectrometry (GC-MS). Four hundred sixty fresh ascocarps of nine truffle species (Tuber aestivum, Tuber magnatum, Tuber melanosporum, Tuber mesentericum, Tuber brumale, Tuber excavatum, Tuber rufum, Tuber indicum and Tuber macrosporum) harvested in 2018/19 and 2019/2020 from 11 different countries (Slovenia, Croatia, Bosnia in Herzegovina, Macedonia, Italy, Spain, France, United Kingdom, Germany, Poland and China) were collected. Our investigation included the classification of species based on their aroma profile, a study of the differences in the volatile organic composition of truffle species over a geographical area, and, in more detail, a study of T. aestivum from four natural truffle growing sites in Slovenia. Our models can distinguish between groups, with small classification error. These models could form the basis of a predictive framework to detect fraud concerning truffle products and to determine the influence of different growing parameters on the aroma profile of truffles.

Longistriata flava (Boletaceae, Basidiomycota) - a new monotypic sequestrate genus and species from Brazilian Atlantic Forest.

A new monotypic sequestrate genus, Longistriata is described based on collections from the Neotropical forest of Atlantic forest in Paraíba, Northeast Brazil - an area known for its high degree of endemism. The striking features of this new fungus are the hypogeous habit, the vivid yellow peridium in mature basidiomes, broadly ellipsoid basidiospores with a distinct wall that is ornamented with longitudinal striations and lageniform cystidia with rounded apices. Phylogenetic analysis, based on LSU and tef-1α regions, showed that the type species, Longistriata flava, is phylogenetically sister to the monotypic sequestrate African genus Mackintoshia in Boletaceae. Together these two species formed the earliest diverging lineage in the subfamily Zangioideae. Longistriata flava is found in nutrient-poor white sand habitats where plants in the genera Coccoloba (Polygonaceae) and Guapira (Nyctaginaceae) are the only potential ectomycorrhizal host symbionts.

Root-Associated Fungal Communities From Two Phenologically Contrasting Silver Fir (Abies alba Mill.) Groups of Trees.

Root-associated fungal communities are important components in ecosystem processes, impacting plant growth and vigor by influencing the quality, direction, and flow of nutrients and water between plants and fungi. Linkages of plant phenological characteristics with belowground root-associated fungal communities have rarely been investigated, and thus our aim was to search for an interplay between contrasting phenology of host ectomycorrhizal trees from the same location and root-associated fungal communities (ectomycorrhizal, endophytic, saprotrophic and pathogenic root-associated fungi) in young and in adult silver fir trees. The study was performed in a managed silver fir forest site. Twenty-four soil samples collected under two phenologically contrasting silver fir groups were analyzed for differences in root-associated fungal communities using Illumina sequencing of a total root-associated fungal community. Significant differences in beta diversity and in mean alpha diversity were confirmed for overall community of ectomycorrhizal root-associated fungi, whereas for ecologically different non-ectomycorrhizal root-associated fungal communities the differences were significant only for beta diversity and not for mean alpha diversity. At genus level root-associated fungal communities differed significantly between early and late flushing young and adult silver fir trees. We discuss the interactions through which the phenology of host plants either drives or is driven by the root-associated fungal communities in conditions of a sustainably co-naturally managed silver fir forest.

Different belowground responses to elevated ozone and soil water deficit in three European oak species (Quercus ilex, Q. pubescens and Q. robur).

Effects on roots due to ozone and/or soil water deficit often occur through diminished belowground allocation of carbon. Responses of root biomass, morphology, anatomy and ectomycorrhizal communities were investigated in seedlings of three oak species: Quercus ilex L., Q. pubescens Willd. and Q. robur L., exposed to combined effects of elevated ozone (ambient air and 1.4 × ambient air) and water deficit (100% and 10% irrigation relative to field capacity) for one growing season at a free-air ozone exposure facility. Effects on root biomass were observed as general reduction in coarse root biomass by -26.8% and in fine root biomass by -13.1% due to water deficit. Effect on coarse root biomass was the most prominent in Q. robur (-36.3%). Root morphological changes manifested as changes in proportions of fine root (<2 mm) diameter classes due to ozone and water deficit in Q. pubescens and due to water deficit in Q. robur. In addition, reduced fine root diameter (-8.49%) in Q. robur was observed under water deficit. Changes in root anatomy were observed as increased vessel density (+18.5%) due to ozone in all three species, as reduced vessel tangential diameter (-46.7%) in Q. ilex due to interaction of ozone and water, and as generally increased bark to secondary xylem ratio (+47.0%) due to interaction of ozone and water. Water deficit influenced occurrence of distinct growth ring boundaries in roots of Q. ilex and Q. robur. It shifted the ectomycorrhizal community towards dominance of stress-resistant species, with reduced relative abundance of Tomentella sp. 2 and increased relative abundances of Sphaerosporella brunnea and Thelephora sp. Our results provide evidence that expression of stress effects varies between root traits; therefore the combined analysis of root traits is necessary to obtain a complete picture of belowground responses.