Volatiles produced by bacteria alleviate antagonistic effects of one associated fungus on Dendroctonus valens larvae

Wang, Shanshan; Zhou, Fangyuan; Wang, Bo; Xu, Dandan; Cao, Qingjie; Lü, Min; Sun, Jianghua

doi:10.1007/s11427-017-9073-9

Cited by 10 publications

(4 citation statements)

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“…In pine phloem, carbon sources available for both fungal and bacterial symbionts are mainly D-pinitol followed by D-glucose [31]. Previous studies have shown that dominant bacteria associated with RTB and their released volatiles, including ammonia, inhibit the growth and main carbohydrates consumption of antagonistic fungi O. minus, which alleviate antagonistic effects of O. minus on RTB larvae [37,47,56]. On the contrary, in this study, the volatile ammonia from bacteria associated with RTB accelerates the consumption of the main carbohydrates by mutualistic fungi L. procerum.…”

Section: Discussionmentioning

confidence: 99%

An invasive beetle–fungus complex is maintained by fungal nutritional-compensation mediated by bacterial volatiles

et al. 2020

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Mutualisms between symbiotic microbes and animals have been well documented, and nutritional relationships provide the foundation for maintaining beneficial associations. The well-studied mutualism between bark beetles and their fungi has become a classic model system in the study of symbioses. Despite the nutritional competition between bark beetles and beneficial fungi in the same niche due to poor nutritional feeding substrates, bark beetles still maintain mutualistic associations with beneficial fungi over time. The mechanism behind this phenomenon, however, remains largely unknown. Here, we demonstrated the bark beetle Dendroctonus valens LeConte relies on the symbiotic bacterial volatile ammonia, as a nitrogen source, to regulate carbohydrate metabolism of its mutualistic fungus Leptographium procerum to alleviate nutritional competition, thereby maintaining the stability of the bark beetle–fungus mutualism. Ammonia significantly reduces competition of L. procerum for carbon resources for D. valens larval growth and increases fungal growth. Using stable isotope analysis, we show the fungus breakdown of phloem starch into d-glucose by switching on amylase genes only in the presence of ammonia. Deletion of amylase genes interferes with the conversion of starch to glucose. The acceleration of carbohydrate consumption and the conversion of starch into glucose benefit this invasive beetle–fungus complex. The nutrient consumption–compensation strategy mediated by tripartite beetle–fungus–bacterium aids the maintenance of this invasive mutualism under limited nutritional conditions, exacerbating its invasiveness with this competitive nutritional edge.

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Section: Discussionmentioning

confidence: 99%

An invasive beetle–fungus complex is maintained by fungal nutritional-compensation mediated by bacterial volatiles

et al. 2020

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“…Bark beetles (Coleoptera: Curculionidae: Scolytinae) are among the most economically important pests of conifers causing significant losses to pine forests worldwide ( Raffa and Berryman, 1987 ; Paine et al, 1997 ; Gitau et al, 2013 ; Wang et al, 2017 ; Zhou et al, 2017 ). Previous studies have focused on gut aerobic bacteria in major bark beetle species in order to explain the pests’ ecology ( Xu et al, 2016c ).…”

Section: Introductionmentioning

confidence: 99%

Effect of Oxygen on Verbenone Conversion From cis-Verbenol by Gut Facultative Anaerobes of Dendroctonus valens

et al. 2018

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Since its introduction from North America, Dendroctonus valens LeConte has become a destructive forest pest in China. Although gut aerobic bacteria have been investigated and some are implicated in beetle pheromone production, little is known about the abundance and significance of facultative anaerobic bacteria in beetle gut, especially with regards to effects of oxygen on their role in pheromone production. In this study, we isolated and identified gut bacteria of D. valens adults in an anaerobic environment, and further compared their ability to convert cis-verbenol into verbenone (a multi-functional pheromone of D. valens) under different O2 concentrations. Pantoea conspicua, Enterobacter xiangfangensis, Staphylococcus warneri were the most frequently isolated species among the total of 10 species identified from beetle gut in anaerobic conditions. Among all isolated species, nine were capable of cis-verbenol to verbenone conversion, and the conversion efficiency increased with increased oxygen concentration. This O2-mediated conversion of cis-verbenol to verbenone suggests that gut facultative anaerobes of D. valens might play an important role in the frass, where there is higher exposure to oxygen, hence the higher verbenone production. This claim is further supported by distinctly differential oxygen concentrations between gut and frass of D. valens females.

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“…Moreover, both bacterial genera can degrade complex polymers such as cellulose, starch, xylan, and lignin to help beetle nutrient acquisition (21, 65, 84). These bacteria genera can also recycle uric acid from beetle faeces, helping the beetles meet the crucial nitrogen requirement (23, 85) and producing antifungal compounds to suppress pathogenic fungal growth, aiding the beetle survival (86). Other core members such as Dyella, Pseudoxanthomonas, Sphingomonas, Saccharomonospora, Acidisoma have the enzymatic competency to help the beetle metabolize complex carbohydrates found in the conifer cell wall (21, 69, 87–90).…”

Section: Discussionmentioning

confidence: 99%

Comparative metagenomic study unveils bacterial communities and their putative involvement in ecological success of two pine-feedingIpsbeetle holobionts

Khara,

Chakraborty,

Modlinger

et al. 2024

Preprint

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Climate change has recently boosted the severity and frequency of the pine bark beetle attacks. The bacterial community associated with these beetles acts as “hidden players”, enhancing their ability to infest and thrive on defence-rich pine trees. There is limited understanding of the environmental acquisition of these hidden players and their life stage-specific association with different pine-feeding bark beetles. There is inadequate knowledge on novel bacterial introduction to pine trees after the beetle infestation. Hence, we conducted the first comparative bacterial metabarcoding study comprehensively revealing the bacterial communities in the pine trees before and after beetle feeding and in different life stages of two dominant pine-feeding bark beetles, namelyIps sexdentatusandIps acuminatus. We also evaluated the bacterial association between wild and lab-bred beetles to measure the deviation due to inhabiting a controlled environment. Significant differences in bacterial amplicon sequence variance (ASVs) abundance existed among different life stages within and between the pine beetles. Such observations endorsed that the bark beetle life stage shaped bacterial assemblage. Furthermore, lab-bred and wild-collected adult beetles had distinct bacterial assemblages, implying that the breeding environment induced crucial changes. Alteration of pine wood bacteriome after beetle feeding is an intriguing observation in the present study, which demands further investigation. We validated the relative abundances of selected bacterial taxa estimated by metagenomic sequencing with quantitative PCR. Functional predictions revealed that these bacterial genera might execute conserved functions, aiding the ecological success of these beetles. Nevertheless, these findings shed new insights into bacterial associations and their putative metabolic roles in pine beetles under the influence of various drivers such as environment, host, and life stages and provide the foundation for future downstream functional investigations.ImportanceThe current understanding of bark beetle as holobiont is restricted. Most studies lack information on microbial community assembly in bark beetle microhabitats. No data comprehensively reveals the influence of lab breeding on pine beetle microbial associations. It is unknown if there is any adaptive convergence in beetle microbial assemblage due to feeding on the same host. Such information is essential to developing a bark beetle management strategy to restore forests from beetle-mediated damage. Our study shows that lab-breeding considerably influences beetle bacterial community assembly. We documented that beetle feeding alters bacteriome at the microhabitat level, and the beetle life stage shapes the bacterial associations. Nevertheless, our study revisited the bark beetle symbiosis under the influence of different drivers and revealed intriguing insight into bacterial community assembly, facilitating future functional studies.

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Volatiles produced by bacteria alleviate antagonistic effects of one associated fungus on Dendroctonus valens larvae

Cited by 10 publications

References 10 publications

An invasive beetle–fungus complex is maintained by fungal nutritional-compensation mediated by bacterial volatiles

An invasive beetle–fungus complex is maintained by fungal nutritional-compensation mediated by bacterial volatiles

Effect of Oxygen on Verbenone Conversion From cis-Verbenol by Gut Facultative Anaerobes of Dendroctonus valens

Comparative metagenomic study unveils bacterial communities and their putative involvement in ecological success of two pine-feedingIpsbeetle holobionts

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