Plant-Guided Microbiome Selection Produces Transient Effects on Insect Performance and Rhizosphere Community Assembly

Microbial communities are essential for plant health, but using these relationships to enhance growth and pest protection is challenging. Leveraging the natural mechanisms plants employ to manage relationships with microbes is one promising means to selectively engineer whole microbial communities with beneficial properties. This approach, known as host-guided selection, has been successful in some model species targeting performance traits (e.g., biomass). However, few studies use crop plants or focus on defensive traits (e.g., pest resistance). Our goal was to naturally engineer tomato root-associated microbiomes that increase resistance to insect pests. First, we used an iterative soil microbial inoculation process to engineer insect-suppressive rhizosphere soil microbiomes that reduce damage from aphid feeding (Macrosiphum euphorbiae) or caterpillar defoliation (Manduca sexta, Spodoptera exigua). We then characterized the bacterial and fungal microbial communities of soils associated with differences in insect performance using metabarcoding approaches. Overall, soil microbiome selection produced transient differences in aphid performance, but caterpillar growth was unaffected. In four of nine generations, the aphid population growth rate was significantly lower on plants with rhizospheres selected for "low" insect performance, where abundance was reduced by up to 20%. Correspondingly minor shifts in fungal and bacterial relative abundance occurred in insect-suppressive communities. However, network analysis indicated that aphid feeding disrupted rhizosphere microbiome assembly, resulting in lower community complexity and connectivity and fewer structurally important taxa compared with uninfested controls. Overall, our results highlight critical factors for successful engineering of beneficial microbiomes, particularly insect feeding guild and microbial community stability.