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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. 

Abstract Ecological diversity in fungi is largely defined by metabolic traits, including the ability to produce secondary or “specialized” metabolites (SMs) that mediate interactions with other organisms. Fungal SM pathways are frequently encoded in biosynthetic gene clusters (BGCs), which facilitate the identification and characterization of metabolic pathways. Variation in BGC composition reflects the diversity of their SM products. Recent studies have documented surprising diversity of BGC repertoires among isolates of the same fungal species, yet little is known about how this population-level variation is inherited across macroevolutionary timescales. Here, we applied a novel linkage-based algorithm to reveal previously unexplored dimensions of diversity in BGC composition, distribution, and repertoire across 101 species of Dothideomycetes, which are considered the most phylogenetically diverse class of fungi and known to produce many SMs. We predicted both complementary and overlapping sets of clustered genes compared with existing methods and identified novel gene pairs that associate with known secondary metabolite genes. We found that variation among sets of BGCs in individual genomes is due to nonoverlapping BGC combinations and that several BGCs have biased ecological distributions, consistent with niche-specific selection. We observed that total BGC diversity scales linearly with increasing repertoire size, suggesting that secondary metabolites have little structural redundancy in individual fungi. We project that there is substantial unsampled BGC diversity across specific families of Dothideomycetes, which will provide a roadmap for future sampling efforts. Our approach and findings lend new insight into how BGC diversity is generated and maintained across an entire fungal taxonomic class. 

Scientific communication is facilitated by a data-driven, scientifically sound taxonomy that considers the end-user's needs and established successful practice. Previously (Geiser et al. 2013; Phytopathology 103:400-408. 2013), the Fusarium community voiced near unanimous support for a concept of Fusarium that represented a clade comprising all agriculturally and clinically important Fusarium species, including the F. solani Species Complex (FSSC). Subsequently, this concept was challenged by one research group (Lombard et al. 2015 Studies in Mycology 80: 189-245) who proposed dividing Fusarium into seven genera, including the FSSC as the genus Neocosmospora, with subsequent justification based on claims that the Geiser et al. (2013) concept of Fusarium is polyphyletic (Sandoval-Denis et al. 2018; Persoonia 41:109-129). Here we test this claim, and provide a phylogeny based on exonic nucleotide sequences of 19 orthologous protein-coding genes that strongly support the monophyly of Fusarium including the FSSC. We reassert the practical and scientific argument in support of a Fusarium that includes the FSSC and several other basal lineages, consistent with the longstanding use of this name among plant pathologists, medical mycologists, quarantine officials, regulatory agencies, students and researchers with a stake in its taxonomy. In recognition of this monophyly, 40 species recently described as Neocosmospora were recombined in Fusarium, and nine others were renamed Fusarium. Here the global Fusarium community voices strong support for the inclusion of the FSSC in Fusarium, as it remains the best scientific, nomenclatural and practical taxonomic option available.