Productivity benefits from diversity can arise when compatible pathogen hosts are buffered by unrelated neighbors, diluting pathogen impacts. However, the generality of pathogen dilution has been controversial and rarely tested within biodiversity manipulations. Here, we test whether soil pathogen dilution generates diversity- productivity relationships using a field biodiversity-manipulation experiment, greenhouse assays, and feedback modeling. We find that the accumulation of specialist pathogens in monocultures decreases host plant yields and that pathogen dilution predicts plant productivity gains derived from diversity. Pathogen specialization predicts the strength of the negative feedback between plant species in greenhouse assays. These feedbacks significantly predict the overyielding measured in the field the following year. This relationship strengthens when accounting for the expected dilution of pathogens in mixtures. Using a feedback model, we corroborate that pathogen dilution drives overyielding. Combined empirical and theoretical evidence indicate that specialist pathogen dilution generates overyielding and suggests that the risk of losing productivity benefits from diversity may be highest where environmental change decouples plant-microbe interactions.

Research suggests that microbiomes play a major role in structuring plant communities and influencing ecosystem processes, however, the relative roles and strength of change of microbial components have not been identified. We measured the response of fungal, arbuscular mycorrhizal fungal (AMF), bacteria, and oomycete composition 4 months after planting of field plots that varied in plant composition and diversity. Plots were planted using 18 prairie plant species from three plant families (Poaceae, Fabaceae, and Asteraceae) in monoculture, 2, 3, or 6 species richness mixtures and either species within multiple families or one family. Soil cores were collected and homogenized per plot and DNA were extracted from soil and roots of each plot. We found that all microbial groups responded to the planting design, indicating rapid microbiome response to plant composition. Fungal pathogen communities were strongly affected by plant diversity. We identified OTUs from genera of putatively pathogenic fungi that increased with plant family, indicating likely pathogen specificity. Bacteria were strongly differentiated by plant family in roots but not soil. Fungal pathogen diversity increased with planted species richness, while oomycete diversity, as well as bacterial diversity in roots, decreased. AMF differentiation in roots was detected with individual plant species, but not plant family or richness. Fungal saprotroph composition differentiated between plant family composition in plots, providing evidence for decomposer home-field advantage. The observed patterns are consistent with rapid microbiome differentiation with plant composition, which could generate rapid feedbacks on plant growth in the field, thereby potentially influencing plant community structure, and influence ecosystem processes. These findings highlight the importance of native microbial inoculation in restoration.

Introduction: Climate change and plant biodiversity loss have large impacts on terrestrial ecosystem function, with the soil microbiome being primary mediators of these effects. The soil microbiome is a complex system, consisting of multiple functional groups with contrasting life histories. Most studies of climate forces and plant biodiversity effects on microbiome consider the perturbations and the microbial functional groups in isolation preventing us from understanding the full picture of the relative and differential impacts of perturbations on microbial functional groups.Methods: We measured changes in multiple microbial communities with different functionality, including plant mutualists and pathogens, after three growing seasons in a full-factorial experiment manipulating precipitation (50%, 150% of ambient), plant diversity, and plant composition. Using amplicon sequencing to characterize the response of fungi, arbuscular mycorrhizal fungi, bacteria and oomycetes, and we found that composition of all microbial groups differentiated strongly between precipitation treatments.Results: Oomycete and bacterial diversity increased with 150% precipitation, while AM and saprotroph fungal diversity decreased. Microbial differentiation in response to plant family and plant species composition was stronger after the third growing season than observed after year one. However, microbial response to plant species richness was weaker in year three. Microbiome response to plant composition was largely independent of the response to precipitation, except for oomycetes, which had greater response to plant composition in high precipitation.Discussion: These findings build upon prior findings that these microbial community members differentially respond to plant community compositional treatments, by measuring the response over 3 years and with the addition of precipitation treatments. We find that both changes in climate and plant composition can drive major differences in soil microbiome composition, which can feed back on plant community structure and alter ecosystem function.

Litter decomposition facilitates the recycling of often limiting resources, which may promote plant productivity responses to diversity, that is, overyielding. However, the direct relationship between decomposition, k, and overyielding remains underexplored in grassland diversity manipulations. We test whether local adaptation of microbes, that is, home‐field advantage (HFA), N‐priming from plant inputs or precipitation drive decomposition and whether decomposition generates overyielding. Within a grassland diversity‐manipulation, altering plant richness (1, 2, 3 and 6 species), composition (communities composed of plants from a single‐family or multiple‐families) and precipitation (50% and 150% ambient growing season precipitation), we conducted a litter decomposition experiment. In spring 2020, we deployed four replicate switchgrass, Panicum virgatum, litter bags (1.59 mm mesh opening), collecting them over 7 months to estimate litter k. Precipitation was a strong, independent driver of decomposition. Switchgrass decomposition accelerated with grass richness and decelerated as phylogenetic dissimilarity from switchgrass increased, suggesting decomposition is fastest at ‘home’. However, decomposition slowed with switchgrass density. In plots that contained switchgrass, we observed no relationship between decomposition and fungal saprotroph dissimilarity from switchgrass. However, in plots without switchgrass, decomposition slowed with increasing saprotroph dissimilarity from switchgrass. Combined these findings suggest that HFA is strongest when closely related neighbours, that is, heterospecific neighbours, are present in the community, rather than other individuals of the same species, that is, conspecifics. Legumes accelerated decomposition with more litter N remaining in those plots, suggesting that N‐inputs from planted legumes are priming decomposition of litter C. However, decomposition and overyielding were unrelated in legume communities. While in grass communities, overyielding and decomposition were positively related and the relationship was strongest in plots with low densities of switchgrass, that is, with heterospecific neighbours. Combined these findings suggest that plant species richness and community composition stimulate litter decomposition through multiple mechanisms, including N‐priming, but only HFA from local adaptation of microbes on closely related species correlates with overyielding, likely through resource recycling. Our results link diversity with ecosystem processes facilitating above‐ground productivity. Whether diversity loss will affect litter decomposition, productivity or both is contingent on resident plant traits and whether a locally adapted soil microbiome is maintained. Read the free Plain Language Summary for this article on the Journal blog.

Fungi contribute to ecosystem function through nutrient cycling and decomposition but may be affected by major disturbances such as fire. Some ecosystems are fire-adapted, such as prairies which require cyclical burning to mitigate woody plant encroachment and reduce litter. While fire suppresses fire-sensitive fungi, pyrophilous fungi may continue providing ecosystem functions. Using litter bags, we measured the litter decomposition at three prairies with unburned and burned sections, and we used Illumina sequencing to examine litter communities. We hypothesized that (H1) decomposition would be higher at unburned sites than burned, (H2) increased decomposition at unburned sites would be correlated with higher overall saprotroph diversity, with a lower diversity in autoclaved samples, and (H3) pyrophilous fungal diversity would be higher at burned sites and overall higher in autoclaved samples. H1 was not supported; decomposition was unaffected by burn treatments. H2 and H3 were somewhat supported; saprotroph diversity was lowest in autoclaved litter at burned sites, but pyrophilous fungal diversity was the highest. Pyrophilous fungal diversity significantly contributed to litter decomposition rates, while saprotroph diversity did not. Our findings indicate that fire-adapted prairies host a suite of pyrophilous saprotrophic fungi, and that these fungi play a primary role in litter decomposition post-fire when other fire-sensitive fungal saprotrophs are less abundant.

Understanding how aerial fungal diversity varies across space, habitat, and disturbance is key to linking local‐scale sporocarp (fruiting body) reproduction with continental‐scale biogeography. In this study, we combined passive spore trap metabarcoding with macrofungal sporocarp records from 31 plots in eight sites across North America to quantify how site, habitat, and fire history shape aerial macrofungal communities. From 823 samples, we recovered 7572 OTUs, nearly half belonging to macrofungi. Macrofungal aerial DNA abundance and OTU richness varied strongly among sites and increased significantly with both temperature and precipitation. Across sites, forest habitats had significantly greater macrofungal aerial DNA abundance than grassland habitats, while conifer forests supported significantly higher OTU richness than oak forests or grasslands. Burn history, likely due to lags in the sampling time following fire, did not significantly impact macrofungal aerial DNA abundance and OTU richness and also had limited effects on community composition. Aerial macrofungal community similarity declined with geographic distance, with geography explaining the most variation (16%). Functional guild composition varied across habitats, shifting from higher ectomycorrhizal prevalence in forest habitats to higher soil saprotroph prevalence in grassland habitats, although wood saprotrophs were the most abundant guild across all habitats. Integration with iNaturalist sporocarp records indicated a mean effective spore trap input range of ~3 km, consistent with strong local dispersal limitation. Together, these findings demonstrate that aerial macrofungal assemblages exhibit pronounced continental‐scale structure yet remain locally heterogeneous, shaped primarily by environmental filtering, functional guild association, and limited dispersal.