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Bacterial microbiota protect an invasive bark beetle from a pine defensive compound.

ABSTRACT: BACKGROUND:There 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. RESULTS:In 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. CONCLUSIONS:Our 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.

SUBMITTER: Cheng C

PROVIDER: S-EPMC6064089 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Bacterial microbiota protect an invasive bark beetle from a pine defensive compound.

Cheng Chihang C Wickham Jacob D JD Chen Li L Xu Dandan D Lu Min M Sun Jianghua J

Microbiome 20180727 1

<h4>Background</h4>There 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 ...[more]

PMID: 30053907

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Project description:Bark beetle outbreaks have intensified in many forests around the globe in recent years. Yet, the legacy of these disturbances for future forest development remains unclear. Bark beetle disturbances are expected to increase further because of climate change. Consequently, feedbacks within the disturbance regime are of growing interest, for example, whether bark beetle outbreaks are amplifying future bark beetle activity (through the initiation of an even-aged cohort of trees) or dampening it (through increased structural and compositional diversity).We studied bark beetle-vegetation-climate interactions in the Bavarian Forest National Park (Germany), an area characterised by unprecedented bark beetle activity in the recent past. We simulated the effect of future bark beetle outbreaks on forest structure and composition and analysed how disturbance-mediated forest dynamics influence future bark beetle activity under different scenarios of climate change. We used process-based simulation modelling in combination with machine learning to disentangle the long-term interactions between vegetation, climate and bark beetles at the landscape scale.Disturbances by the European spruce bark beetle were strongly amplified by climate change, increasing between 59% and 221% compared to reference climate. Bark beetle outbreaks reduced the dominance of Norway spruce (Picea abies (L.) Karst.) on the landscape, increasing compositional diversity. Disturbances decreased structural diversity within stands (α diversity) and increased structural diversity between stands (β diversity). Overall, disturbance-mediated changes in forest structure and composition dampened future disturbance activity (a reduction of up to -67%), but were not able to fully compensate for the amplifying effect of climate change. Synthesis. Our findings indicate that the recent disturbance episode at the Bavarian Forest National Park was caused by a convergence of highly susceptible forest structures with climatic conditions favourable for bark beetle outbreaks. While future climate is increasingly conducive to massive outbreaks, the emerging landscape structure is less and less likely to support them. This study improves our understanding of the long-term legacies of ongoing bark beetle disturbances in Central Europe. It indicates that increased diversity provides an important dampening feedback, and suggests that preventing disturbances or homogenizing post-disturbance forests could elevate the future susceptibility to large-scale bark beetle outbreaks.

Dataset Information

Bacterial microbiota protect an invasive bark beetle from a pine defensive compound.

Publications

Bacterial microbiota protect an invasive bark beetle from a pine defensive compound.

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