Plant invasion (garlic mustard; Alliaria petiolata) alters fungal community composition, increases fungal diversity, and shifts dominant fungal trophic strategy

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The non-mycorrhizal herb garlic mustard (Alliaria petiolata) produces glucosinolates that reduce plant diversity by inhibiting mycorrhizal fungal colonization. The plant is native to Europe and Asia and was introduced into North America in the late 1800’s, where it is now a destructive invasive species. Invasion can suppress root mycorrhizal communities, but little is known about how invasion impacts the entire soil fungal community, where saprotrophs, plant pathogens, parasites, and mycorrhizal hyphae reside. Our objective was to characterize the fungal community structure of uninvaded an invaded soils from replicate plots established in six deciduous forest understories in the Northeastern USA. We used Illumina metabarcoding (ITS2), phospholipid fatty acid analysis, and characterized edaphic soil properties. Fungal genera were also annotated by trophic strategy (saprotroph, symbiotroph, & biotroph) and mycorrhizal type (ectomycorrhizal; EcM or arbuscular mycorrhizal; AMF). In terms of soil properties, invasion was associated with lower organic carbon content, elevated soil pH, and higher soil nitrate concentrations, but no difference in fungal or bacterial phospholipid fatty acid abundances. The fungal community in invaded organic horizon and mineral soil was more diverse, compositionally distinct, and homogenous relative to uninvaded communities. Uninvaded soil was also dominated by EcM fungi, while invaded soil was dominated by saprotrophic fungi. The ratio of EcM to non-EcM was positively correlated with soil C:N ratios and this correlation was significantly impacted by invasion. The transition from biotrophic to heterotrophic carbon metabolism dominance may explain this correlation, as the lower C:N ratios in association with invasion were due to reduced organic carbon, not higher nitrogen. Finally, saprotrophic and biotropic (including plant pathogens, mycoparasites, and nematophagous fungi) abundances and richness were higher in association with invasion, and the richness of these two groups was positively correlated with the density of garlic mustard at a plot. Shifts in saprotrophic fungi could affect decomposition while biotrophic fungi may further suppress native plants suffering from dismantled mycorrhizae. In conclusion, invasion was linked with severely transformed soil fungal communities, comprised of fewer EcM and enriched with saprotrophs and biotrophs that may distress native above-belowground interactions and alter soil processes.