Invasive earthworms alter forest soil microbiomes and nitrogen cycling

Northern hardwood forests in formerly glaciated areas had been free of earthworms until exotic European earthworms were introduced by human activities. The invasion of exotic earthworms is known to dramatically alter soil physical, geochemical, and biological properties, but its impacts on soil microbiomes are still unclear. Here we show that the invasive earthworms alter soil microbiomes and ecosystem functioning, especially for nitrogen cycling. We collected soil samples at different depths from three sites across an active earthworm invasion chronosequence in a hardwood forest in Minnesota, USA. We analyzed the structures and the functional potentials of the soil microbiomes by using amplicon sequencing, high-throughput nitrogen cycle gene quantification (NiCE chip), and shotgun metagenomics. Both the levels of earthworm invasion and soil depth influenced the microbiome structures and the functional gene abundances. In the most recently and minimally invaded soils, Nitrososphaera and Nitrospira as well as the genes related to nitrification were more abundant than in the heavily invaded soils. By contrast, genes related to denitrification and nitrogen fixation were more abundant in the heavily invaded than the minimally invaded soils at various depths. Since denitrification can cause a nitrogen loss from the ecosystem, our results suggest the invasion of earthworms could influence the overall forest N cycling. • Both the levels of earthworm invasion and soil depth influenced soil microbiomes. • Earthworm invasion caused the shift in the soil N cycling. • Abundance of Nitrososphaera and Nitrospira decreased after earthworm invasion. • Nitrification gene abundance also decreased after earthworm invasion. • Denitrification and N fixation gene abundances increased after earthworm invasion.