Ewany, J.; Hiltpold, I.; Defossez, E.; Glauser, G.; Arce, C. C. M.; Zhang, W.; Rasmann, S.; Turlings, T. C. J.; Machado, R. A. R.

Photorhabdus bacteria are potent insect-killing microbes associated with entomopathogenic nematodes and offer opportunities for environmentally benign pest control. They can be applied as foliar sprays or soil drenches without their nematode vector, resulting in massive amounts of Photorhabdus cells and their (toxic) metabolites introduced into the soil. However, their effects beyond the target organisms are unknown. To fill this knowledge gap, we investigated the soil legacy effects of Photorhabdus cells and their metabolites on soil microbial communities, plant performance and resistance to herbivores. To this end, we first conditioned soils with i) mechanically killed (MK) or Photorhabdus-infected insect larvae, ii) aqueous extracts of MK or Photorhabdus-infected insect larvae, iii) cell-free Photorhabdus supernatants, iv) autoclaved soil complemented with live soil previously conditioned with MK or Photorhabdus-infected insect larvae. We then grew maize plants in these soils and measured plant biomass, profiled soil microbial communities and plant metabolites, and evaluated plant resistance against two pest insects, Diabrotica balteata and Spodoptera frugiperda. We found that conditioned soils increased plant biomass by 10 to 26% relative to controls and significantly altered soil bacterial and nematode communities, and to a lesser extent, fungal communities. Reinoculating conditioned soil microbiota into autoclaved soils recreated the plant growth-promoting effects, indicating microbial-mediated mechanisms. Additionally, plants grown in soils conditioned with Photorhabdus-infected insect cadavers were often more resistant to herbivorous insect attack, in a strain-specific manner. On average, D. balteata and S. frugiperda larvae gained 10 to 20% and 10 to 59% less weight, respectively, when fed on plants grown in conditioned soils than on plants grown in control soils. The plant metabolic profiles of plant leaves and roots also varied with resistance levels. We conclude that Photorhabdus metabolites modulate soil microbial communities towards a structure that enhances plant growth and triggers systemic responses against herbivores.