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Evidence is accumulating that the soil microbiome—the community of microorganisms living in soils—has a major effect on plant traits and fitness. However, most work to date has taken place under controlled laboratory conditions and has not experimentally disentangled the effect of the soil microbiome on plant performance from the effects of key endosymbiotic constituents. As a result, it is difficult to extrapolate from existing data to understand the role of the soil microbiome in natural plant populations. To address this gap, we performed a field experiment using the black medick Medicago lupulina to test how the soil microbiome influences plant performance and colonization by two root endosymbionts (the mutualistic nitrogen‐fixing bacteria Ensifer spp. and the parasitic root‐knot nematode Meloidogyne hapla) under natural conditions. We inoculated all plants with nitrogen‐fixing bacteria and factorially manipulated the soil microbiome and nematode infection. We found that plants grown in microbe‐depleted soil exhibit greater mortality, but that among the survivors, there was no effect of the soil microbiome on plant performance (shoot biomass, root biomass, or shoot‐to‐root ratio). The soil microbiome also impacted parasitic nematode infection and affected colonization by mutualistic nitrogen‐fixing bacteria in a plant genotype‐dependent manner, increasing colonization in some plant genotypes and decreasing it in others. Our results demonstrate the soil microbiome has complex effects on plant–endosymbiont interactions and may be critical for survival under natural conditions., We show that the soil microbial community affects survival and interactions with two major root endosymbionts (nitrogen‐fixing bacteria and parasitic root‐knot nematodes) in the field in the legume Medicago lupulina. Our experiment demonstrates that the significant fitness consequences of host‐associated microbial communities that have been observed in the laboratory persist under natural conditions, and suggests that the role of soil microbial communities in mediating key endosymbioses merits future research.

The invasive plant, garlic mustard (Alliaria petiolata), has the potential to affect soil microbial communities and ecosystem processes in temperate hardwood forests primarily through the release of allelopathic chemicals into the soil. These forest soils are also often affected (directly and indirectly) by the high abundance of white-tailed deer (Odocoileus virginianus), which can alter plant community composition and productivity. We examined the joint effects of deer and garlic mustard on soil microbial communities, soil nutrients and a native plant species’ vital rates in a temperate forest 8 years after initiation of a paired plot deer exclusion/access study where garlic mustard was either removed from half of each plot or remained at ambient level in the other plot half. We examined soil microbial communities using DNA-based techniques and quantified nutrient availability and physicochemical properties. Deer exclusion affected the community structure of AM fungi, particularly when garlic mustard was present, but had no effect on soil chemistry. Garlic mustard removal plots showed no changes for soil fungi, but displayed higher soil carbon content. Interestingly, we found significant changes to native plant vital rates that mirrored soil responses; the presence of garlic mustard led to higher mortality of large, mature plants and reduced native plant cover and biomass. Our data suggest herbivore-plant-soil feedbacks and synergies can interact to negatively affect the soil ecology of forests. Management activities that reduce deer or invasive plant abundance may positively affect soil microbial communities and chemistry in temperate forests.

Despite widespread evidence that biological invasion influences both the biotic and abiotic soil environments, the extent to which these two pathways underpin the effects of invasion on plant traits and performance remains unknown. Leveraging a long-term (14-year) field experiment, we show that an allelochemical-producing invader affects plants through biotic mechanisms, altering the soil fungal community composition, with no apparent shifts in soil nutrient availability. Changes in belowground fungal communities resulted in high costs of nutrient uptake for native perennials and a shift in plant traits linked to their water and nutrient use efficiencies. Some plants in the invaded community compensate for the disruption of nutritional symbionts and reduced nutrient provisioning by sanctioning more nitrogen to photosynthesis and expending more water, which demonstrates a trade-off in trait investment. For the first time, we show that the disruption of belowground nutritional symbionts can drive plants towards alternative regions of their trait space in order to maintain water and nutrient economics.

Despite widespread evidence that biological invasion influences both the biotic and abiotic soil environments, the extent to which these two pathways underpin the effects of invasion on plant traits and performance is unknown. Leveraging a long-term (14-yr) field experiment, we show that an allelochemical-producing invader affects plants through biotic mechanisms, altering the soil fungal community composition, with no apparent shifts in soil nutrient availability. Changes in belowground fungal communities result in high costs of nutrient uptake for native perennials and a shift in functional traits linked to their water and nutrient use efficiencies. Some species in the invaded community compensate for high nutrient costs by reducing nutrient uptake and maintaining photosynthesis by expending more water, which demonstrates a trade-off in trait investment. For the first time, we show that the disruption of belowground nutritional symbionts can drive native plants toward novel regions in order to maintain their water and nutrient economics.