M. Müller, Maryse A. P. Huve, Michael Kunzler, Mitja N. P. Remus-Emsermann, R. Schlechter, Luis R. Paniagua Voirol
Phyllosphere bacteria can influence plant-insect interactions, with bacterial community richness associated with reduced P. brassicae larval performance and SynCom20 linked to stronger JA accumulation in leaves during feeding. Conversely, herbivory increased leaf bacterial loads, shifted leaf community composition, and filtered leaf-associated bacteria during passage into the larval gut. These findings establish this functionally gnotobiotic insect-plant system as a tractable model for dissecting reciprocal effects between resident phyllosphere bacteria and herbivory.
BACKGROUND: The leaf surface, or phyllosphere, hosts abundant and diverse bacterial communities that interact with both the host plant and herbivorous insects, yet their collective influence on plant-insect interactions remains poorly investigated. We established a functionally gnotobiotic insect-plant system combining axenically grown Arabidopsis thaliana, Pieris brassicae larvae, and defined synthetic phyllosphere communities (SynComs) of increasing richness: SynCom5, SynCom10 and SynCom20, containing 5, 10 and 20 bacterial strains, respectively. We investigated how phyllosphere bacteria influence herbivore performance, plant defence responses, and bacterial colonisation of both leaves and the insect gut. RESULTS: While larval weight tended to decrease with increasing bacterial community richness, only the most diverse SynCom (20 members) caused significant weight reductions without affecting survival. Plants harbouring the most diverse community showed enhanced jasmonic acid (JA) levels during feeding, whereas salicylic acid (SA) remained unchanged, suggesting the induction of herbivore-associated defence responses. Compared to plants experiencing no herbivory, feeding strongly reshaped bacterial colonisation on leaves, increasing total bacterial loads about fourfold and driving dominance of Pantoea eucalypti 299R as shown by 16S rRNA gene amplicon sequencing. Larvae acquired a distinct subset of bacteria, primarily recruited from the genera Methylobacterium, Microbacterium, Williamsia, and Curtobacterium. CONCLUSIONS: Phyllosphere bacteria can influence plant-insect interactions, with bacterial community richness associated with reduced P. brassicae larval performance and SynCom20 linked to stronger JA accumulation in leaves during feeding. Conversely, herbivory increased leaf bacterial loads, shifted leaf community composition, and filtered leaf-associated bacteria during passage into the larval gut. These findings establish this functionally gnotobiotic insect-plant system as a tractable model for dissecting reciprocal effects between resident phyllosphere bacteria and herbivory.