Plant-guided microbiome selection produces transient effects on insect performance and rhizosphere community assembly

Microbial communities are essential for plant health and protection. Recently, it has been suggested that the natural mechanisms plants employ to manage relationships with microbes can be used to selectively engineer whole microbial communities with beneficial or protective properties that enhance key plant traits. This approach, known as host-guided selection, has yet to be developed for crop plants in agricultural settings. Our goal was to naturally engineer tomato root-associated microbiomes that increase resistance to common insect pests. First, we tested several approaches for engineering insect-suppressive rhizosphere soil microbiomes that reduce damage from aphid feeding (Macrosiphum euphorbiae) or caterpillar defoliation (Manduca sexta, Spodoptera exigua) using an iterative soil microbial inoculation process. Second, using metabarcoding approaches we characterized the bacterial and fungal communities of selected soils associated with differences in aphid performance on tomato. Overall, host-guided soil microbiome selection for higher or lower insect performance was successful for aphids but not caterpillars, although effects were transient over time. There were minor shifts in relative abundance of fungal and bacteria taxa observed in insect-suppressive communities, but substantial changes in community composition occurred over time. Network analysis indicated aphid feeding was disruptive to rhizosphere microbiome assembly, resulting in lower community complexity, connectivity and keystone taxa compared to un-infested controls. Overall, our results suggest several factors are critical for successful host-guided engineering of beneficial microbiomes, particularly microbial community stability and microbe-microbe interactions, external environmental influences, and the extent to which the crop trait of interest is microbially mediated.