Climate change alters beneficial crop-microbe-invertebrate interactions

Increasing levels of CO2 and tropospheric ozone (O3) due to climate change are contributing to reduced plant health and unstable crop yield production1. The inoculation of plant roots with beneficial fungi or bacteria can increase plant health2. However, this is often studied under very controlled conditions and it is unknown how climate change or interactions with other species can alter the resulting benefits. Here we show that the rhizosphere bacterium Acidovorax radicis N35 can increase plant growth and reduce insect growth - with increased impact in a high-stress elevated O3 environment, but reduced impact under elevated CO2. In a fully-factorial climate chamber experiment we disentangled the impacts of climate factors (elevated CO2 and elevated O3) and biotic interactions (plant cultivar, sap-feeding insects and earthworms) on cereal growth and insect suppression mediated by A. radicis N35. Earthworms promoted plant aboveground growth, whereas A. radicis N35 promoted root growth, and overall plant growth was higher when both species were present. However, earthworms also promoted insect growth and therefore increased plant damage through herbivory. While A. radicis N35 inoculation was able to mitigate these negative effects to some extent under an ambient environment this was lost under climate change conditions. Our results show that knowledge-based solutions for sustainable agriculture should include biotic interactions and must be tested across variable climate change scenarios in order to build resilient cropping systems.