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The emerald ash borer (EAB), Agrilus planipennis, is a destructive invasive insect of North American ash (Fraxinus). While microorganisms associated with the beetle may contribute to tree decline and death, the microbial community succession during an EAB attack is unknown. We repeatedly sampled the bottom two meters of green ash (Fraxinus pennsylvanica) and black ash (Fraxinus nigra) in seven stands across an infestation gradient over four years. Amplicon libraries were sequenced from control phloem tissue of trees showing no symptoms of infestation, uninfested phloem of trees with EAB, infested phloem (galleries), frass, and larvae to determine if there are shifts in the fungal and bacterial communities as trees succumb to EAB attack. We found that the control phloem communities significantly differed from the beetle-infested phloem in both tree species. Furthermore, as EAB progressed in its attack from the top limbs to the tree’s base, the microbial communities in uninfested phloem outside the galleries shifted away from communities in phloem of control trees. In infested phloem, more than 80% of the detected taxa were absent from control trees (i.e., most taxa were non-latent). However, the relative abundance of latent taxa in infested phloem was higher than the relative abundance of the non-latent taxa, especially for potential canker-causing fungi, which increased 21-fold and 32-fold in black ash and green ash trees, respectively. These findings provide valuable insight into how a woodboring beetle shapes the microbial environment within trees over time, influencing the overall microbial diversity, such as canker-causing and wood decay taxa. 

Fungi and bacteria associated with bark beetles can facilitate successful tree colonization, and, in some cases, these fungi act as pathogens of trees. The red turpentine beetle (RTB, Dendroctonus valens) is a bark beetle native to North America that colonizes stressed pines, rarely killing healthy trees. The fungal communities associated with RTB adults, larval galleries, and control tree phloem from red pine (Pinus resinosa) and white pine (P. strobus) forests in the Great Lakes region of the United States were characterized using both culture-independent and culture-dependent methods. Similarly, the bacterial communities associated with RTB adults in the same region were characterized using a culture-independent method. There were significant differences between the adult beetle fungal communities and the tree-based fungal communities. Culture-independent sequencing of RTB adults showed high abundances of the fungal order Filobasidiales (red pine: 28.71% relative abundance, white pine: 6.91% relative abundance), as well as the bacterial orders Enterobacterales (red pine: 53.72%, white pine: 22.15%) and Pseudomonadales (red pine: 15.86%, white pine: 12.91%). In contrast, we isolated high amounts of fungi in the orders Pleosporales (red pine: 21.79%, white pine: 15.90%) and Eurotiales (red pine: 15.38%, white pine: 16.51%) from the adult beetles by culturing. Culture-independent sequencing of beetle galleries yielded high abundances of fungi in the orders Helotiales (red pine: 22.23%, white pine: 23.21%), whereas culture-based isolation from the same galleries yielded high amounts of Eurotiales (red pine: 17.91%, white pine: 17.91%), Hypocreales (red pine: 16.42%, white pine: 16.42%), and Ophiostomatales (red pine: 23.39%, white pine: 23.39%). This contrasts with the culture-independent method, where, likely due to limitations in the sequencing method, the Ophiostomatales accounted for only around 2% of the fungi from RTB galleries in both pine species. We observed a high species-level diversity of Ophiostomatales associated with RTB, isolating 14 species from the Great Lakes region. Leptographium terebrantis, a species that has been described in association with RTB throughout the United States, was the most common species (e.g., >35% of the Ophiostomatales relative abundance in red pine environments and >14% of the Ophiostomatales relative abundance in the white pine environment). This study enhances our understanding of RTB-associated fungi and bacteria in the beetle’s native range at both the community and species levels. 

ABSTRACT Plants have coevolved with herbivorous insects for millions of years, resulting in variation in resistance both within and between species. Using a manipulative experiment combined with untargeted metabolomics, microbiome sequencing and transcriptomics approaches, we investigated the roles of plant metabolites and the microbiome in defence mechanisms in native resistant Manchurian ash (Fraxinus mandshurica) trees and non‐native susceptible velvet ash (Fraxinus velutina) trees against the highly invasive emerald ash borer (EAB,Agrilus planipennis). Comparative transcriptomics and metabolomics analyses show that the phenylpropanoid pathway, which is enriched in differentially expressed genes and differentially abundant metabolites, may serve as a potential regulator of resistance. Additionally, the microbiome is distinctly shifted in two ash species. Indicator taxa analysis reveals that the distinct genera are dominant in the galleries of two ash species, for example,Pseudomonasin velvet, andHafnia‐Obesumbacteriumin Manchurian. The strong correlation between indicator taxa and metabolites suggests that the chemical compounds might impact the microbial community in phloem directly or indirectly, or vice versa. This study significantly enhances our understanding of the variation in resistance between ash species and its contribution to the invasion success of EAB, providing valuable insights for the development of pest management strategies.