CO2 drives the pine wood nematode off its insect vector

Abstract

Insects have developed special organs, spiracles and the trachea, for oxygen-carbon dioxide exchange to adapt to terrestrial life. The plant-parasitic nematode Bursaphelenchus xylophilus, also known as pine wood nematode (PWN), is vectored by pine sawyer beetles (Monochamus spp.) and causes destructive pine wilt disease, threatening the safety and stability of pine forest ecosystems. Unlike the free-living nematode model species Caenorhabditis elegans, PWN have two distinct life stages (dispersive and propagative), each requiring a unique host relationship ranging from symbiotic/commensal to parasitic. Its symbiotic vector beetle and the pine tree it ultimately infects represent dramatically different host environments within which it needs to successfully maneuver. In Asia, the symbiotic relationship between PWN and its host vector M. alternatus is very close (Figure S1A, see Supplemental Information). Previous studies have shown that third-stage juveniles (J_III) are attracted by specific terpenes produced by mature insect larvae and aggregate around pupal chambers in diseased trees [1] and fourth-stage juveniles (J_IV) are attracted to newly eclosed adults by ascarosides the beetles secrete [2]. These J_IV, sometimes up to 200,000 per beetle [3], then enter the tracheal system of the newly eclosed beetle, which is full of CO₂, for dispersal. Later, those nematodes depart from the spiracles to invade new healthy trees via the feeding wounds on pine branches made during beetles' feeding, thus starting a new cycle of infection, propagation and dispersal. The mechanism mediating the nematodes' departure remains unknown and remains an important unsolved focal point in the PWN life cycle. Our experimental evidence suggests acute CO₂ avoidance triggers this behavior.