Positive Linkage in Bacterial Microbiota at the Plant-Insect Interface Benefits an Invasive Bark Beetle

Symbiotic microbes facilitate rapid adaptation of invasive insects on novel plants via multifaceted function provisions, but little was known on the importance of cross linkages in symbiotic microbiota to insect invasiveness. Novel host pine Pinus tabuliformis is inherently unsuitable for invasive red turpentine beetle (RTB) in China; however, Novosphingobium and Erwinia/Serratia in gallery microbiota (at the interface between RTB larvae and pine phloem) have been discovered to help beetles via biodegrading pine detrimental compounds naringenin and pinitol, respectively. Here, we further revealed significant positive linkage of the two functions, with higher activity level conferring more growth benefit to RTB larvae. Abundance of Erwinia/Serratia was remarkably increased in response to pinitol, while naringenin-biodegrading Novosphingobium was unable to utilize this main phloem carbohydrate directly. High-activity bacterial microbiota produced nutritive metabolites (sucrose and hexadecanoic acid) from pinitol consumption that facilitated growth of both Novosphingobium and beetle larvae. Functional proteins of several bacterial taxa were enriched in high-activity microbiota that appeared to form a metabolic network collectively to regulate the nutrient production. Our results indicate that positive interaction between Erwinia/Serratia and Novosphingobium is critical for RTB invasion success, while Bacilli bacteria might restrict this linkage, providing new insights into symbiotic microbial interactions for insect herbivores.