Garlic mustard invasion increases fungal richness and restructures fungal communities

Background/Question/Methods

Fungi form ubiquitous symbiotic relationships with plants and are important regulators over nutrient cycling through their function as decomposers. One way non-native plants can become highly abundant in the introduced range is by restructuring soil fungal communities in order to suppress native mutualisms and enhance nutrient synchronization with invasion. The non-native plant, Alliaria petiolata (garlic mustard) produces toxic biochemicals that disrupt mycorrhizae. While this has led to the success of garlic mustard in North America, we do not understand how specific mycorrhizal groups and taxonomic guilds respond to invasion. As a non-mycorrhizal plant, we hypothesized that invasion would suppress competing mycorrhizal fungi and restructure saprotrophic fungi in order to meet nutritional requirements. To address this, we studied the effects of garlic mustard invasion at six forests in Northeastern USA. We collected soil samples from three long-term uninvaded and invaded plots in June, 2013. We measured microbial biomass (phospholipid fatty acid analysis), nutrient cycling (nitrogen mineralization and proteolysis) and fungal community structure (ITS2 metabarcoding). Our statistical repertoire consisted of mixed effect models, partial least squares regression and permutation-based analyses of variance.

Results/Conclusions

Invasion was associated with higher soil nitrate concentrations and lower soil carbon and C:N ratios. While changes in the biomass of different microbial groups varied across sites, uninvaded and invaded fungal community structures were significantly different. The degree of fungal responses to invasion was strongly effected by garlic mustard abundances (R² = 0.69). We found that two of the most abundant orders of fungi, a clade of mycorrhizal Agaricales and saprotrophic Russulales were suppressed in invaded soils and this coincided with overall lower relative abundances of the Basidiomycetes. In contrast, the abundance of Zygomycetes + unresolved fungi, Chytridiomycetes and Glomeromycetes were higher in invaded soils. Fungal richness also increased in invaded soils (+400 OTUs) and there were 307 and 12 indicators species in invaded and uninvaded soils, respectively. Overall, we unveiled dramatic shifts in taxonomic guilds of ecto-, arbuscular mycorrhizal and saprotrophic fungi. Many novel fungal species emerged in face of invasion and carry implications for mycorrhizae and nutrient cycling. For example, both the abundance of Basidiomycetes and the C:N ratio were reduced in invaded soils, and these two shifts were highly correlated (R² = 0.54).  Disentangling how changes belowground manifest aboveground can enhance our knowledge of the factors promoting non-native plant invasions.