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

ABSTRACT: 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.

SUBMITTER: Liu F

PROVIDER: S-EPMC7784882 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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

Liu Fanghua F Wickham Jacob D JD Cao Qingjie Q Lu Min M Sun Jianghua J

The ISME journal 20200819 11

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 benefi ...[more]

PMID: 32814865

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Project description:Microorganisms are diverse in their genome sequences and subsequently in their encoded metabolic pathways, which enabled them to adapt to numerous environmental conditions. They produce thousands of small molecules, many of which are volatiles in nature and play important roles in signaling in intra- and inter-species to kingdom and domain interactions, survival, or virulence. Many of these compounds have been studied, characterized, and organized in the mVOC 2.0 database. However, such dataset has not been investigated comprehensively in terms of its phylogeny to determine key volatile markers for certain taxa. It was hypothesized that some of the volatiles described in the mVOC 2.0 database could function as a phylogenetic signal since their production is conserved among certain taxa within the microbial evolutionary tree. Our meta-analysis revealed that some volatiles were produced by a large number of bacteria but not in fungal genera such as dimethyl disulfide, acetic acid, 2-nonanone, dimethyl trisulfide, 2-undecanone, isovaleric acid, 2-tridecanone, propanoic acid, and indole (common bacterial compounds). In contrast, 1-octen-3-ol, 3-octanone, and 2-pentylfuran (common fungal compounds) were produced primarily by fungal genera. Such chemical information was further confirmed by investigating genomic data of publicly available databases revealing that bacteria or fungi harbor gene families involved in these volatiles' biosynthesis. Our phylogenetic signal testing identified 61 volatiles with a significant phylogenetic signal as demonstrated by phylogenetic D statistic P-value < 0.05. Thirty-three volatiles were phylogenetically conserved in the bacterial domain (e.g., cyclocitral) compared to 17 volatiles phylogenetically conserved in the fungal kingdom (e.g., aristolochene), whereas 11 volatiles were phylogenetically conserved in genera from both bacteria and fungi (e.g., geosmin). These volatiles belong to different chemical classes such as heterocyclic compounds, long-chain fatty acids, sesquiterpenoids, and aromatics. The performed approaches serve as a starting point to investigate less explored volatiles with potential roles in signaling, antimicrobial therapy, or diagnostics.

Dataset Information

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

Publications

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

Similar Datasets

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