Spores of arbuscular mycorrhizal fungi host surprisingly diverse communities of endobacteria.

Arbuscular mycorrhizal fungi (AMF) are ubiquitous plant root symbionts, which can house two endobacteria: Ca. Moeniiplasma glomeromycotorum (CaMg) and Ca. Glomeribacter gigasporarum (CaGg). However, little is known about their distribution and population structure in natural AMF populations and whether AMF can harbour other endobacteria. We isolated AMF from two environments and conducted detailed analyses of endobacterial communities associated with surface-sterilised AMF spores. Consistent with the previous reports, we found that CaMg were extremely abundant (80%) and CaGg were extremely rare (2%) in both environments. Unexpectedly, we discovered an additional and previously unknown level of bacterial diversity within AMF spores, which extended beyond the known endosymbionts, with bacteria belonging to 10 other phyla detected across our spore data set. Detailed analysis revealed that: CaGg were not limited in distribution to the Gigasporaceae family of AMF, as previously thought; CaMg population structure was driven by AMF host genotype; and a significant inverse correlation existed between the diversity of CaMg and diversity of all other endobacteria. Based on these data, we generate novel testable hypotheses regarding the function of CaMg in AMF biology by proposing that they might act as conditional mutualists of AMF.

Contribution of soil bacteria to the atmosphere across biomes.

The dispersion of microorganisms through the atmosphere is a continual and essential process that underpins biogeography and ecosystem development and function. Despite the ubiquity of atmospheric microorganisms globally, specific knowledge of the determinants of atmospheric microbial diversity at any given location remains unresolved. Here we describe bacterial diversity in the atmospheric boundary layer and underlying soil at twelve globally distributed locations encompassing all major biomes, and characterise the contribution of local and distant soils to the observed atmospheric community. Across biomes the diversity of bacteria in the atmosphere was negatively correlated with mean annual precipitation but positively correlated to mean annual temperature. We identified distinct non-randomly assembled atmosphere and soil communities from each location, and some broad trends persisted across biomes including the enrichment of desiccation and UV tolerant taxa in the atmospheric community. Source tracking revealed that local soils were more influential than distant soil sources in determining observed diversity in the atmosphere, with more emissive semi-arid and arid biomes contributing most to signatures from distant soil. Our findings highlight complexities in the atmospheric microbiota that are relevant to understanding regional and global ecosystem connectivity.

Intensive grassland management disrupts below-ground multi-trophic resource transfer in response to drought.

Modification of soil food webs by land management may alter the response of ecosystem processes to climate extremes, but empirical support is limited and the mechanisms involved remain unclear. Here we quantify how grassland management modifies the transfer of recent photosynthates and soil nitrogen through plants and soil food webs during a post-drought period in a controlled field experiment, using in situ 13C and 15N pulse-labelling in intensively and extensively managed fields. We show that intensive management decrease plant carbon (C) capture and its transfer through components of food webs and soil respiration compared to extensive management. We observe a legacy effect of drought on C transfer pathways mainly in intensively managed grasslands, by increasing plant C assimilation and 13C released as soil CO2 efflux but decreasing its transfer to roots, bacteria and Collembola. Our work provides insight into the interactive effects of grassland management and drought on C transfer pathways, and highlights that capture and rapid transfer of photosynthates through multi-trophic networks are key for maintaining grassland resistance to drought.

Evidence of a selective and bi-directional relationship between arbuscular mycorrhizal fungal and bacterial communities co-inhabiting plant roots.

Arbuscular mycorrhizal fungi (AMF) provide plants with vital mineral nutrients and co-exist inside the roots alongside a complex community of bacterial endophytes. These co-existing AMF and bacterial root communities have been studied individually and are known to be influenced in structure by different environmental parameters. However, the extent to which they are affected by environmental parameters and by each other is completely unknown. The current study addressed this knowledge gap by characterising AMF and bacterial communities inside plant roots from a natural and an agricultural ecosystem. Using multivariate modelling, the relative contribution of environmental parameters in structuring the two communities was quantified at different spatial scales. Using this model, it was possible to then remove the contribution of environmental parameters and show that the co-existing AMF and bacterial communities were significantly correlated with each other, explaining up to 36% of each other's variance. Notably, this was not due to the presence of know AMF endobacteria, as removal of endobacterial reads maintained the significance of correlation. These findings provide the first empirical evidence of a selective and bi-directional relationship between AMF and bacteria co-inhibiting plant roots and indicate that a significant fraction of this covariation is due to biological and ecological interactions between them.

"Jack-of-all-trades" is parthenogenetic.

Sex is evolutionarily more costly than parthenogenesis, evolutionary ecologists therefore wonder why sex is much more frequent than parthenogenesis in the majority of animal lineages. Intriguingly, parthenogenetic individuals and species are as common as or even more common than sexuals in some major and putative ancient animal lineages such as oribatid mites and rotifers. Here, we analyzed oribatid mites (Acari: Oribatida) as a model group because these mites are ancient (early Paleozoic), widely distributed around the globe, and include a high number of parthenogenetic species, which often co-exist with sexual oribatid mite species. There is evidence that the reproductive mode is phylogenetically conserved in oribatid mites, which makes them an ideal model to test hypotheses on the relationship between reproductive mode and species' ecological strategies. We used oribatid mites to test the frozen niche variation hypothesis; we hypothesized that parthenogenetic oribatid mites occupy narrow specialized ecological niches. We used the geographic range of species as a proxy for specialization as specialized species typically do have narrower geographic ranges than generalistic species. After correcting for phylogenetic signal in reproductive mode and demonstrating that geographic range size has no phylogenetic signal, we found that parthenogenetic lineages have a higher probability to have broader geographic ranges than sexual species arguing against the frozen niche variation hypothesis. Rather, the results suggest that parthenogenetic oribatid mite species are more generalistic than sexual species supporting the general-purpose genotype hypothesis. The reason why parthenogenetic oribatid mite species are generalists with wide geographic range sizes might be that they are of ancient origin reflecting that they adapted to varying environmental conditions during evolutionary history. Overall, our findings indicate that parthenogenetic oribatid mite species possess a widely adapted general-purpose genotype and therefore might be viewed as "Jack-of-all-trades."

Local stability properties of complex, species-rich soil food webs with functional block structure.

Ecologists have long debated the properties that confer stability to complex, species-rich ecological networks. Species-level soil food webs are large and structured networks of central importance to ecosystem functioning. Here, we conducted an analysis of the stability properties of an up-to-date set of theoretical soil food web models that account both for realistic levels of species richness and the most recent views on the topological structure (who is connected to whom) of these food webs. The stability of the network was best explained by two factors: strong correlations between interaction strengths and the blocked, nonrandom trophic structure of the web. These two factors could stabilize our model food webs even at the high levels of species richness that are typically found in soil, and that would make random systems very unstable. Also, the stability of our soil food webs is well-approximated by the cascade model. This result suggests that stability could emerge from the hierarchical structure of the functional organization of the web. Our study shows that under the assumption of equilibrium and small perturbations, theoretical soil food webs possess a topological structure that allows them to be complex yet more locally stable than their random counterpart. In particular, results strongly support the general hypothesis that the stability of rich and complex soil food webs is mostly driven by correlations in interaction strength and the organization of the soil food web into functional groups. The implication is that in real-world food web, any force disrupting the functional structure and distribution pattern of interaction strengths (i.e., energy fluxes) of the soil food webs will destabilize the dynamics of the system, leading to species extinction and major changes in the relative abundances of species.

Plastics everywhere: first evidence of polystyrene fragments inside the common Antarctic collembolan Cryptopygus antarcticus.

There is evidence and serious concern that microplastics have reached the most remote regions of the planet, but how far have they travelled in terrestrial ecosystems? This study presents the first field-based evidence of plastic ingestion by a common and central component of Antarctic terrestrial food webs, the collembolan Cryptopygus antarcticus. A large piece of polystyrene (PS) foam (34 × 31 × 5 cm) covered by microalgae, moss, lichens and microfauna was found in a fellfield along the shores of the Fildes Peninsula (King George Island). The application of an improved enzymatic digestion coupled with Fourier transform infrared microscopy (µ-FTIR), unequivocally detected traces of PS (less than 100 µm) in the gut of the collembolans associated with the PS foam and documented their ability to ingest plastic. Plastics are thus entering the short Antarctic terrestrial food webs and represent a new potential stressor to polar ecosystems already facing climate change and increasing human activities. Future research should explore the effects of plastics on the composition, structure and functions of polar terrestrial biota.

A global database of soil nematode abundance and functional group composition.

As the most abundant animals on earth, nematodes are a dominant component of the soil community. They play critical roles in regulating biogeochemical cycles and vegetation dynamics within and across landscapes and are an indicator of soil biological activity. Here, we present a comprehensive global dataset of soil nematode abundance and functional group composition. This dataset includes 6,825 georeferenced soil samples from all continents and biomes. For geospatial mapping purposes these samples are aggregated into 1,933 unique 1-km pixels, each of which is linked to 73 global environmental covariate data layers. Altogether, this dataset can help to gain insight into the spatial distribution patterns of soil nematode abundance and community composition, and the environmental drivers shaping these patterns.

Population asynchrony alone does not explain stability in species-rich soil animal assemblages: The stabilizing role of forest age on oribatid mite communities.

The importance of microbial and plant communities in the control of the diversity and structure of soil animal communities has been clarified over the last decade. Previous research focused on abiotic factors, niche separation and spatial patterns. Significant gaps still exist in our knowledge of the factors that control the stability of these communities over time. We analysed a 9-year dataset from the national Long-term Ecological Research Network of Latvia. We focused on 117 oribatid species from three Scots pine forests of different age (<40, 65 and >150 years) and structure. For each forest type, 100 samples were collected each year, providing very high replication and long time series for a soil community. We assessed different aspects of stability: we used a dynamic null model, parameterized on observed growth rates, to test the hypothesis that asynchrony in species populations stabilizes total community size; we also analysed alpha and beta diversity over time to test the hypothesis that temporal variation in species composition and relative abundances is controlled by forest attributes. Real communities can be more stable than their stochastic counterparts if species are asynchronous, confirming for the first time the role of asynchrony in stabilizing soil communities. Yet, while some real communities were more stable and had higher abundance and growth rates than others, they were not necessarily more asynchronous than the less stable communities. Species composition and relative abundances were also less variable in the more stable communities. Species asynchrony generally stabilizes species-rich communities but is not sufficient to explain the different levels of stability between forests. Forest age is a key factor explaining the different levels of overyielding and so stability. Data suggest that both asynchrony and high diversity of microhabitat structure of Scots pine forests promote the stability of soil animal communities.

Soil microbial community responses to climate extremes: resistance, resilience and transitions to alternative states.

A major challenge for advancing our understanding of the functional role of soil microbial communities is to link changes in their structure and function under climate change. To address this challenge requires new understanding of the mechanisms that underlie the capacity of soil microbial communities to resist and recover from climate extremes. Here, we synthesize emerging understanding of the intrinsic and extrinsic factors that influence the resistance and resilience of soil microbial communities to climate extremes, with a focus on drought, and identify drivers that might trigger abrupt changes to alternative states. We highlight research challenges and propose a path for advancing our understanding of the resistance and resilience of soil microbial communities to climate extremes, and of their vulnerability to transitions to alternative states, including the use of trait-based approaches. We identify a need for new approaches to quantify resistance and resilience of soil microbial communities, and to identify thresholds for transitions to alternative states. We show how high-resolution time series coupled with gradient designs will enable detecting response patterns to interacting drivers. Finally, to account for extrinsic factors, we suggest that future studies should use environmental gradients to track soil microbial community responses to climate extremes in space and time. This article is part of the theme issue 'Climate change and ecosystems: threats, opportunities and solutions'.

Improving phosphorus sustainability in intensively managed grasslands: The potential role of arbuscular mycorrhizal fungi.

Long-term nutrient fertilization of grassland soils greatly increases plant yields but also profoundly alters ecosystem phosphorus (P) dynamics. Here, we addressed how long-term P fertilization may affect ecosystem P budget, P use efficiency (PUE) and the abundance of arbuscular mycorrhizal fungi (AMF), which play a key role in the acquisition of P by plants. We found that 47 years of organic P applications increased soil P availability and total soil P stocks up to 1600% and 400%, respectively, compared to unfertilized-control soils. Grassland soils could retain up to 62% and 48% of P applied since 1970 in organic and inorganic forms, respectively. Nutrient treatments significantly affected rates of AMF root colonization (%), which were higher in control and NPK-fertilized plots when compared to soils receiving increasing applications of organic P. Plant PUE increased with greater AMF root colonization, which remained high (i.e. 50-to-75%) even after ~50 years of continuous 'normal' rates of agronomic P inputs (~30 kg P ha-1 year-1). AMF abundance, however, decreased under higher P applications and we found a negative relationship between soil P availability or soil P stocks and rates of AMF root colonization. Our study demonstrates that (1) AMF root colonization is still high in soils, which have received consistent but moderate P inputs for over four decades, and (2) moderate rates of P fertilization are related to a more conservative P ecosystem budget whereby the amount of P retained in soils and up-taken by plants on an annual basis is higher than the amount of P added through fertilization. This is possible only if extra P is 'mined' from the soil P 'bank' and made available to plant uptake. We suggest that AMF could play a significant role in intensively-managed grasslands contributing to increase P sustainability by reducing the need for extra P fertilizer.

Air mass source determines airborne microbial diversity at the ocean-atmosphere interface of the Great Barrier Reef marine ecosystem.

The atmosphere is the least understood biome on Earth despite its critical role as a microbial transport medium. The influence of surface cover on composition of airborne microbial communities above marine systems is unclear. Here we report evidence for a dynamic microbial presence at the ocean-atmosphere interface of a major marine ecosystem, the Great Barrier Reef, and identify that recent air mass trajectory over an oceanic or continental surface associated with observed shifts in airborne bacterial and fungal diversity. Relative abundance of shared taxa between air and coral microbiomes varied between 2.2 and 8.8% and included those identified as part of the core coral microbiome. We propose that this variable source of atmospheric inputs may in part contribute to the diverse and transient nature of the coral microbiome.

Oribatid mites show that soil food web complexity and close aboveground-belowground linkages emerged in the early Paleozoic.

The early evolution of ecosystems in Palaeozoic soils remains poorly understood because the fossil record is sparse, despite the preservation of soil microarthropods already from the Early Devonian (~410 Mya). The soil food web plays a key role in the functioning of ecosystems and its organisms currently express traits that have evolved over 400 my. Here, we conducted a phylogenetic trait analysis of a major soil animal group (Oribatida) to reveal the deep time story of the soil food web. We conclude that this group, central to the trophic structure of the soil food web, diversified in the early Paleozoic and resulted in functionally complex food webs by the late Devonian. The evolution of body size, form, and an astonishing trophic diversity demonstrates that the soil food web was as structured as current food webs already in the Devonian, facilitating the establishment of higher plants in the late Paleozoic.

Parthenogenetic vs. sexual reproduction in oribatid mite communities.

The dominance of sex in Metazoa is enigmatic. Sexual species allocate resources to the production of males, while potentially facing negative effects such as the loss of well-adapted genotypes due to recombination, and exposure to diseases and predators during mating. Two major hypotheses have been put forward to explain the advantages of parthenogenetic versus sexual reproduction in animals, that is, the Red Queen hypothesis and the Tangled Bank/Structured Resource Theory of Sex. The Red Queen hypothesis assumes that antagonistic predator-prey/ parasite-host interactions favor sex. The Structured Resource Theory of Sex predicts sexual reproduction to be favored if resources are in short supply and aggregated in space. In soil, a remarkable number of invertebrates reproduce by parthenogenesis, and this pattern is most pronounced in oribatid mites (Oribatida, Acari). Oribatid mites are abundant in virtually any soil across very different habitats, and include many sexual and parthenogenetic (thelytokous) species. Thereby, they represent an ideal model group to investigate the role of sexual versus parthenogenetic reproduction across different ecosystems and habitats. Here, we compiled data on oribatid mite communities from different ecosystems and habitats across biomes, including tropical rainforests, temperate forests, grasslands, arable fields, salt marshes, bogs, caves, and deadwood. Based on the compiled dataset, we analyzed if the percentage of parthenogenetic species and the percentage of individuals of parthenogenetic species are related to total oribatid mite density, species number, and other potential driving factors of the reproductive mode including altitude and latitude. We then interpret the results in support of either the Red Queen hypothesis or the Structured Resource Theory of Sex. Overall, the data showed that low density of oribatid mites due to harsh environmental conditions is associated with high frequency of parthenogenesis supporting predictions of the Structured Resource Theory of Sex rather than the Red Queen hypothesis.

Oribatid mites reveal that competition for resources and trophic structure combine to regulate the assembly of diverse soil animal communities.

The role of niche partitioning in structuring species-rich soil animal communities has been debated for decades and generated the "enigma of soil animal diversity." More recently, resource-based niche partitioning has been hypothesized to play a very limited role in the assembly of soil animal communities. To test this hypothesis, we applied a novel combination of stable isotopes and null models of species co-occurrence to quantify the extent of resource niche partitioning on a diverse oribatid mite community sampled from mature oak woodland.We asked whether species aggregate or segregate spatially and how these patterns correlated with the abundance of estimated trophic guilds. We also estimated the effects of environmental variables on community structure.All measured environmental variables accounted for 12% of variance in community structure, including 8% of pure spatial structure unrelated to measured environmental factors and 2% of pure environmental variance unrelated to spatial variation. Co-occurrence analysis revealed 10 pairs of species that aggregated and six pairs of species that were spatially segregated. Values of δ15N indicated that five out of the 10 pairs of aggregated species occupied the same trophic guild, while values of δ13C indicated that species in these five pairs consumed resources of different quality, supporting a significant role of resource-based niche partitioning. Also, one of the five pairs of segregated species occupied the same trophic guild but had overlapping δ13C values suggesting that these species do not co-occur locally and thus minimize competition for shared resources.Partitioning of resources plays an underestimated role in soil microarthropod communities and different local communities consisted of the same trophic guilds with species identity changing from place to place. The sum of resource partitioning, multi-trophic interactions, and microscale environmental variability in the environment is a viable solution to the enigma of soil animal diversity.

Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity.

Theory suggests that more complex food webs promote stability and can buffer the effects of perturbations, such as drought, on soil organisms and ecosystem functions. Here, we tested experimentally how soil food web trophic complexity modulates the response to drought of soil functions related to carbon cycling and the capture and transfer below-ground of recent photosynthate by plants. We constructed experimental systems comprising soil communities with one, two or three trophic levels (microorganisms, detritivores and predators) and subjected them to drought. We investigated how food web trophic complexity in interaction with drought influenced litter decomposition, soil CO2 efflux, mycorrhizal colonization, fungal production, microbial communities and soil fauna biomass. Plants were pulse-labelled after the drought with 13 C-CO2 to quantify the capture of recent photosynthate and its transfer below-ground. Overall, our results show that drought and soil food web trophic complexity do not interact to affect soil functions and microbial community composition, but act independently, with an overall stronger effect of drought. After drought, the net uptake of 13 C by plants was reduced and its retention in plant biomass was greater, leading to a strong decrease in carbon transfer below-ground. Although food web trophic complexity influenced the biomass of Collembola and fungal hyphal length, 13 C enrichment and the net transfer of carbon from plant shoots to microbes and soil CO2 efflux were not affected significantly by varying the number of trophic groups. Our results indicate that drought has a strong effect on above-ground-below-ground linkages by reducing the flow of recent photosynthate. Our results emphasize the sensitivity of the critical pathway of recent photosynthate transfer from plants to soil organisms to a drought perturbation, and show that these effects may not be mitigated by the trophic complexity of soil communities, at least at the level manipulated in this experiment.

Soil nematode abundance and functional group composition at a global scale.

Soil organisms are a crucial part of the terrestrial biosphere. Despite their importance for ecosystem functioning, few quantitative, spatially explicit models of the active belowground community currently exist. In particular, nematodes are the most abundant animals on Earth, filling all trophic levels in the soil food web. Here we use 6,759 georeferenced samples to generate a mechanistic understanding of the patterns of the global abundance of nematodes in the soil and the composition of their functional groups. The resulting maps show that 4.4 ± 0.64 × 1020 nematodes (with a total biomass of approximately 0.3 gigatonnes) inhabit surface soils across the world, with higher abundances in sub-Arctic regions (38% of total) than in temperate (24%) or tropical (21%) regions. Regional variations in these global trends also provide insights into local patterns of soil fertility and functioning. These high-resolution models provide the first steps towards representing soil ecological processes in global biogeochemical models and will enable the prediction of elemental cycling under current and future climate scenarios.

Airborne microbial transport limitation to isolated Antarctic soil habitats.

Dispersal is a critical yet poorly understood factor underlying macroecological patterns in microbial communities1. Airborne microbial transport is assumed to occupy a central role in determining dispersal outcomes2,3, and extra-range dispersal has important implications for predicting ecosystem resilience and response to environmental change4. One of the most pertinent biomes in this regard is Antarctica, given its geographic isolation and vulnerability to climate change and human disturbance5. Here, we report microbial diversity in near-ground and high-altitude air above the largest ice-free Antarctic habitat, as well as that of underlying soil microbial communities. We found that persistent local airborne inputs were unable to fully explain Antarctic soil community assembly. Comparison with airborne microbial diversity from high-altitude and non-polar sources suggests that strong selection occurs during long-range atmospheric transport. The influence of selection during airborne transit and at sink locations varied between microbial phyla. Overall, the communities from this isolated Antarctic ecosystem displayed limited connectivity to the non-polar microbial pool, and alternative sources of recruitment are necessary to fully explain extant soil diversity. Our findings provide critical insights into the role of airborne transport limitation in determining microbial biogeographic patterns.

Biotic interactions are an unexpected yet critical control on the complexity of an abiotically driven polar ecosystem.

Abiotic and biotic factors control ecosystem biodiversity, but their relative contributions remain unclear. The ultraoligotrophic ecosystem of the Antarctic Dry Valleys, a simple yet highly heterogeneous ecosystem, is a natural laboratory well-suited for resolving the abiotic and biotic controls of community structure. We undertook a multidisciplinary investigation to capture ecologically relevant biotic and abiotic attributes of more than 500 sites in the Dry Valleys, encompassing observed landscape heterogeneities across more than 200 km2. Using richness of autotrophic and heterotrophic taxa as a proxy for functional complexity, we linked measured variables in a parsimonious yet comprehensive structural equation model that explained significant variations in biological complexity and identified landscape-scale and fine-scale abiotic factors as the primary drivers of diversity. However, the inclusion of linkages among functional groups was essential for constructing the best-fitting model. Our findings support the notion that biotic interactions make crucial contributions even in an extremely simple ecosystem.

Nematodes in a polar desert reveal the relative role of biotic interactions in the coexistence of soil animals.

Abiotic factors are major determinants of soil animal distributions and their dominant role is pronounced in extreme ecosystems, with biotic interactions seemingly playing a minor role. We modelled co-occurrence and distribution of the three nematode species that dominate the soil food web of the McMurdo Dry Valleys (Antarctica). Abiotic factors, other biotic groups, and autocorrelation all contributed to structuring nematode species distributions. However, after removing their effects, we found that the presence of the most abundant nematode species greatly, and negatively, affected the probability of detecting one of the other two species. We observed similar patterns in relative abundances for two out of three pairs of species. Harsh abiotic conditions alone are insufficient to explain contemporary nematode distributions whereas the role of negative biotic interactions has been largely underestimated in soil. The future challenge is to understand how the effects of global change on biotic interactions will alter species coexistence.