Utilization of a nutritionally refractive food source by the European woodwasp, Sirex noctilio, and its microbial symbiont community

Pine xylem tissue is composed predominantly of cellulose and lignin and is generally low in nitrogen compared to all other plant tissues. These traits, coupled with terpene and resin defenses, prohibit most phytophagous insects from utilizing pine xylem as food. The European woodwasp, Sirex noctilio (Siricidae), is unique among sawflies in its ability to attack and kill healthy pine hosts. Sirex adults weaken hosts and open xylem resources to progeny by introducing a phytotoxic mucous and a pathogenic fungal symbiont, during ovipositon. The fungal symbiont (Amylosterium aerolatum) is essential for host colonization and is hypothesized to act as both a source of digestive enzymes and food for developing larvae, though nutritional aspects of Amylosterium have not been studied. We examined the relationship between Sirex larvae and all potential sources of nutrition using resource-specific sterol signals, feeding behavior, and genomic analysis of microbial communities associated with Sirex. Spatial analysis of larval feeding position in relation to a cellulose digestive enzyme (laccase) produced by Amylosterium showed larva feeding distinctly outside areas of fungal growth. GC-MS analysis indicated no fungal ergosterol, in tissues of developing larvae. These results suggest alternative sources of essential sterols and digestive enzymes. Community metagenomic analysis of the microbial community associated with Sirex larvae revealed a rich bacterial community with numerous catalytic pathways capable of serving as sources of essential enzymes and metabolites. Our results suggest that Sirex is not feeding directly on the fungus, but instead enlists a symbiotic bacterial community for digestion of a refractive food resource.