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Does cryptic microbiota mitigate pine resistance to an invasive beetle-fungus complex? Implications for invasion potential.

ABSTRACT: Microbial symbionts are known to assist exotic pests in their colonization of new host plants. However, there has been little evidence linking symbiotic invasion success to mechanisms for mitigation of native plant resistance. The red turpentine beetle (RTB) was introduced with a fungus, Leptographium procerum, to China from the United States and became a destructively invasive symbiotic complex in natural Pinus tabuliformis forests. Here, we report that three Chinese-resident fungi, newly acquired by RTB in China, induce high levels of a phenolic defensive chemical, naringenin, in pines. This invasive beetle-fungus complex is suppressed by elevated levels of naringenin. However, cryptic microbiotas in RTB galleries strongly degrade naringenin, and pinitol, the main soluble carbohydrate of P. tabuliformis, is retained in L. procerum-infected phloem and facilitate naringenin biodegradation by the microbiotas. These results demonstrate that cryptic microbiota mitigates native host plant phenolic resistance to an invasive symbiotic complex, suggesting a putative mechanism for reduced biotic resistance to symbiotic invasion.

SUBMITTER: Cheng C

PROVIDER: S-EPMC5020614 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Does cryptic microbiota mitigate pine resistance to an invasive beetle-fungus complex? Implications for invasion potential.

Cheng Chihang C Xu Letian L Xu Dandan D Lou Qiaozhe Q Lu Min M Sun Jianghua J

Scientific reports 20160913

Microbial symbionts are known to assist exotic pests in their colonization of new host plants. However, there has been little evidence linking symbiotic invasion success to mechanisms for mitigation of native plant resistance. The red turpentine beetle (RTB) was introduced with a fungus, Leptographium procerum, to China from the United States and became a destructively invasive symbiotic complex in natural Pinus tabuliformis forests. Here, we report that three Chinese-resident fungi, newly acqui ...[more]

PMID: 27621032

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Project description: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.

Dataset Information

Does cryptic microbiota mitigate pine resistance to an invasive beetle-fungus complex? Implications for invasion potential.

Publications

Does cryptic microbiota mitigate pine resistance to an invasive beetle-fungus complex? Implications for invasion potential.

Similar Datasets

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