Abstract
BackgroundThere is growing evidence that some devastating biotic invasions are facilitated by microbial symbionts. The red turpentine beetle (RTB), an innocuous secondary insect attacking weakened trees in North America, has formed an invasive complex with the fungus Leptographium procerum in China, and this invasive beetle-fungus symbiotic complex is capable of attacking and killing healthy pines. A previous study demonstrated that three Chinese-resident fungi, newly acquired by RTB in China, induce high levels of a phenolic defensive chemical, naringenin, in pines and this invasive beetle-fungus complex is suppressed by elevated levels of naringenin while the beetle uses its gallery as an external detoxification system in which particular yeast-like fungi and bacterial species biodegrade naringenin. However, the functional roles of key microbial players in the symbiosis, contained within the microbiome of the bark beetle gallery, have not been well elucidated.ResultsIn this report, the symbiotic naringenin-degrading microbiota were found to increase RTB survivorship in the presence of induced host defenses, and potential genes associated with degradation pathways were discovered. While fungi in the gallery microbiota had little involvement in naringenin degradation, bacterial community structure within the beetle gallery was highly correlated to naringenin degrading activity. Phylotypes of the Gram-negative bacterial genus Novosphingobium, which possessed genes involved in degradation pathways, were highly correlated to naringenin degradation activities and RTB associated with an isolated species of this genus acquired protection against naringenin and gained fitness.ConclusionsOur results demonstrated that symbiotic bacterial community of RTB galleries enhances the survivorship and overall fitness of invasive beetles by degrading the host phenolic naringenin, ultimately overcoming the tree defenses and facilitating the success of the invasive beetle-fungi complex. This dynamic interplay between the invasive insect pest and multipartite microbes suggests a putative mechanism in invasion ecology for mitigating biotic resistance to symbiotic invasion.
Highlights
There is growing evidence that some devastating biotic invasions are facilitated by microbial symbionts
The naringenin degradation function was highly correlated with bacterial community structure in the microbiota
This study might be among the first attempts of combining a variety of bioassay results with metagenomics and 454 pyrosequencing data to demonstrate the roles of key symbiotic microbes in facilitating species invasion
Summary
There is growing evidence that some devastating biotic invasions are facilitated by microbial symbionts. The functional roles of key microbial players in the symbiosis, contained within the microbiome of the bark beetle gallery, have not been well elucidated. Rhizospheres and roots of exotic plants and the living nests, bodies, and guts of exotic insects are well-known microhabitats colonized by various bacterial and fungal members [14,15,16,17,18]. These co-occurring microbes compose symbiotic microbiota that provide benefits for invasive species [19,20,21]. While much work has been done to understand the roles of the key symbiotic microbiota, there are still many knowledge gaps
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