Invader-resident relatedness and soil management history shape patterns of invasion of compost microbial populations into agricultural soils

Compost application to soil can have numerous agricultural benefits, but our understanding of the persistence and roles of compost microbes in soil following amendment is limited. Studies of microbial invasion ecology could improve this understanding, yet most studies to date have focused on single invaders in constant environments. In contrast, many real-world microbial invasions - such compost microbes invading agricultural soils - are coalescence events involving the mixing of entire communities as well as their environmental media. In a microcosm experiment, we mixed live composted poultry manure into row crop soils from three long-term agricultural management systems: no input wheat/fallow, conventional maize/tomato, and organic maize/tomato. We tracked bacterial and archaeal communities by 16S rRNA sequencing prior to mixing and then at 4 days and 32 days post-mixing. We investigated whether phylogenetic relatedness of the invaders (compost microbes) to the resident (soil) community predicted invader success, as well as whether the management systems differed in their invasibility. At both time points, invader persistence was associated with a closer phylogenetic relationship to a member of the resident community, with OTUs most closely related to a member of the resident community 1.65 times more likely to persist than OTUs most distantly related to a member of the resident community on average. Conversely, invaders that achieved greater relative abundances were less related to the resident community, with OTUs most closely related to the resident community as a whole achieving 1.96 times lower relative abundance than OTUs most distantly related to the resident community as a whole on average. Increases in relative abundance of the same bacterial groups (e.g., Actinobacteria, Gammaproteobacteria, Alphaproteobacteria) among residents and invaders post-mixing suggest that similar resident and invader responses to the post-mixing environment may have driven the relative abundance relatedness result. Invaders that were more abundant in the compost also had higher probability of persistence and greater relative abundance post-mixing, with OTUs most abundant in the compost being 16.2 times more likely to persist and having 4.4 times greater relative abundance in the post-mixing community than OTUs least abundant in the compost on average. The organic management system - which had a history of compost addition - was less susceptible to invasion than the other two management systems, with OTUs 1.39 times less likely to persist in the organic system than in the other two systems on average. Our results suggest that both environmental filtering and the potential success of residents and invaders in the novel mixed environment should be considered when predicting outcomes of microbial coalescence events. Agricultural soil management history may also mediate invasion outcomes.

Automated summary

Compost application can benefit agricultural soil, but the persistence and roles of compost microbes in soil remain limited. Studies show that the success of microbial invaders is related to their phylogenetic relationship with the resident community, and similar responses of residents and invaders in the post-mixing environment may drive relative abundance results. Additionally, the management history of agricultural soil can influence invasion outcomes.