Pinewood Nematodes Manipulate Locomotion of the Vector Beetle Through ATP1-Driven Energy Metabolism

The transmission of many pathogens depends on insect vectors, and these pathogens tend to manipulate vector behaviors after acquisition to enhance their spread. However, the underlying molecular mechanisms remain largely unknown. The pinewood nematode (PWN), the causative agent of pine wilt disease, primarily relies on Monochamus alternatus beetles for dispersal in Asia. The behavior of the beetle plays a crucial role in the spread of the pinewood nematode among host pine trees. Here, we investigated the behavioral and molecular effects of PWN loading on M. alternatus. Behavioral assay demonstrated that PWN loading significantly reduced beetle locomotion, with decreases in movement distance, speed, and activity duration. Comparative transcriptomic analysis of the muscle of beetles with and without PWN highlighted the disruptions in key energy metabolism pathways and pathways related to aging responses and neurodegenerative diseases. Gene co-expression network showed ATP synthase subunit alpha (ATP1), which was notably down-regulated by PWN loading, is central in energy metabolism and the aging process. The reduced ATP production in the muscles of beetles with PWN suggested ATP1 as a candidate gene required for locomotion control. RNA interference (RNAi) targeting ATP1 led to a decline in beetle locomotion, confirming its role as a key mediator of these locomotion changes. Overall, our findings revealed that the pinewood nematode manipulates vector behavior through energy metabolic genes such as ATP1 and provides potential cues for vector manipulation by the pathogen on aging and longevity.