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1. LaeA-Regulated Fungal Traits Mediate Bacterial Community Assembly

   https://doi.org/10.1128/mbio.00769-23  

   Tannous, Joanna; Cosetta, Casey M.; Drott, Milton T.; Rush, Tomás A.; Abraham, Paul E.; Giannone, Richard J.; Keller, Nancy P.; Wolfe, Benjamin E. (June 2023, mBio)

   Taylor, John W. (Ed.)

   ABSTRACT Potent antimicrobial metabolites are produced by filamentous fungi in pure culture, but their ecological functions in nature are often unknown. Using an antibacterial Penicillium isolate and a cheese rind microbial community, we demonstrate that a fungal specialized metabolite can regulate the diversity of bacterial communities. Inactivation of the global regulator, LaeA, resulted in the loss of antibacterial activity in the Penicillium isolate. Cheese rind bacterial communities assembled with the laeA deletion strain had significantly higher bacterial abundances than the wild-type strain. RNA-sequencing and metabolite profiling demonstrated a striking reduction in the expression and production of the natural product pseurotin in the laeA deletion strain. Inactivation of a core gene in the pseurotin biosynthetic cluster restored bacterial community composition, confirming the role of pseurotins in mediating bacterial community assembly. Our discovery demonstrates how global regulators of fungal transcription can control the assembly of bacterial communities and highlights an ecological role for a widespread class of fungal specialized metabolites. IMPORTANCE Cheese rinds are economically important microbial communities where fungi can impact food quality and aesthetics. The specific mechanisms by which fungi can regulate bacterial community assembly in cheeses, other fermented foods, and microbiomes in general are largely unknown. Our study highlights how specialized metabolites secreted by a Penicillium species can mediate cheese rind development via differential inhibition of bacterial community members. Because LaeA regulates specialized metabolites and other ecologically relevant traits in a wide range of filamentous fungi, this global regulator may have similar impacts in other fungus-dominated microbiomes. 

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2. Pathogen-microbiome interactions and the virulence of an entomopathogenic fungus

   https://doi.org/10.1128/aem.02293-23  

   Kolp, Matthew R; de_Anda_Acosta, Yazmin; Brewer, William; Nichols, Holly L; Goldstein, Elliott B; Tallapragada, Keertana; Parker, Benjamin J (June 2024, Applied and Environmental Microbiology)

   Tortosa, Pablo (Ed.)

   ABSTRACT Bacteria shape interactions between hosts and fungal pathogens. In some cases, bacteria associated with fungi are essential for pathogen virulence. In other systems, host-associated microbiomes confer resistance against fungal pathogens. We studied an aphid-specific entomopathogenic fungus calledPandora neoaphidisin the context of both host and pathogen microbiomes. Aphids host several species of heritable bacteria, some of which confer resistance againstPandora. We first found that spores that emerged from aphids that harbored protective bacteria were less virulent against subsequent hosts and did not grow on plate media. We then used 16S amplicon sequencing to study the bacterial microbiome of fungal mycelia and spores during plate culturing and host infection. We found that the bacterial community is remarkably stable in culture despite dramatic changes in pathogen virulence. Last, we used an experimentally transformed symbiont of aphids to show thatPandoracan acquire host-associated bacteria during infection. Our results uncover new roles for bacteria in the dynamics of aphid-pathogen interactions and illustrate the importance of the broader microbiological context in studies of fungal pathogenesis. IMPORTANCEEntomopathogenic fungi play important roles in the population dynamics of many insect species. Understanding the factors shaping entomopathogen virulence is critical for agricultural management and for the use of fungi in pest biocontrol. We show that heritable bacteria in aphids, which confer protection to their hosts against fungal entomopathogens, influence virulence against subsequent hosts. Aphids reproduce asexually and are typically surrounded by genetically identical offspring, and thus these effects likely shape the dynamics of fungal disease in aphid populations. Furthermore, fungal entomopathogens are known to rapidly lose virulence in lab culture, complicating their laboratory use. We show that this phenomenon is not driven by changes in the associated bacterial microbiome. These results contribute to our broader understanding of the aphid model system and shed light on the biology of the Entomophthorales—an important but understudied group of fungi. 

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3. Fungi shape genome evolution of bacteria even in the absence of major growth phenotypes

   https://doi.org/10.1093/ismejo/wraf081  

   Putnam, Emily E; May, Robert; Freeman, Nina; Arrigan, Dillon; Boylan, Andrew; Childs, Laura H; Wolfe, Benjamin E (May 2025, The ISME Journal)

   Abstract Studies of microbial interactions often emphasize interactions with large, easily measurable growth differences and short-term ecological outcomes spanning just a few generations. However, more subtle interactions, such as those without obvious phenotypes, may play a significant role in shaping both the short-term ecological dynamics and the long-term evolutionary trajectories of microbial species. We used the cheese rind model microbiome to examine how two fungal species, Penicillium camemberti and Geotrichum candidum, impact global gene expression and genome evolution of the bacterium Pseudomonas carnis LP. Even though fungi had limited impacts on the growth of P. carnis LP, approximately 4–40% of its genome was differentially expressed, depending on the specific fungal partner. When we evolved this Pseudomonas strain alone or in co-culture with each of the fungi, we observed frequent mutations in global regulators of nitrogen regulation, secondary metabolite production, and motility, depending on the fungus. Strikingly, many strains with mutations in the nitrogen regulatory gene ntrB emerged when evolved alone or with G. candidum, but not with P. camemberti. Metabolomic and fitness experiments demonstrate that release of free amino acids by P. camemberti removes the fitness advantages conferred by ntrB mutations. Collectively, these results demonstrate that even in the absence of major short-term growth effects, fungi can have substantial impacts on the transcriptome and genomic evolution of bacterial species. 

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4. Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities

   https://doi.org/10.1128/spectrum.01332-23  

   Chou, Ming-Yi; Andersen, Trine B.; Mechan Llontop, Marco E.; Beculheimer, Nick; Sow, Alassane; Moreno, Nick; Shade, Ashley; Hamberger, Bjoern; Bonito, Gregory; Calatrava, Victoria (October 2023, Microbiology Spectrum)

   Hom, Erik F. (Ed.)

   ABSTRACT Terpenes are among the oldest and largest class of plant-specialized bioproducts that are known to affect plant development, adaptation, and biological interactions. While their biosynthesis, evolution, and function in aboveground interactions with insects and individual microbial species are well studied, how different terpenes impact plant microbiomes belowground is much less understood. Here we designed an experiment to assess how belowground exogenous applications of monoterpenes (1,8-cineole and linalool) and a sesquiterpene (nerolidol) delivered through an artificial root system impacted its belowground bacterial and fungal microbiome. We found that the terpene applications had significant and variable impacts on bacterial and fungal communities, depending on terpene class and concentration; however, these impacts were localized to the artificial root system and the fungal rhizosphere. We complemented this experiment with pure culture bioassays on responsive bacteria and fungi isolated from the sorghum rhizobiome. Overall, higher concentrations (200 µM) of nerolidol were inhibitory toFerrovibriumand tested Firmicutes. While fungal isolates ofPenicilliumandPericoniawere also more inhibited by higher concentrations (200 µM) of nerolidol,Clonostachyswas enhanced at this higher level and together withHumicolawas inhibited by the lower concentration tested (100 µM). On the other hand, 1,8-cineole had an inhibitory effect onOrbiliaat both tested concentrations but had a promotive effect at 100 µM onPenicilliumandPericonia. Similarly, linalool at 100 µM had significant growth promotion inMortierella, but an inhibitory effect forOrbilia. Together, these results highlight the variable direct effects of terpenes on single microbial isolates and demonstrate the complexity of microbe-terpene interactions in the rhizobiome. ImportanceTerpenes represent one of the largest and oldest classes of plant-specialized metabolism, but their role in the belowground microbiome is poorly understood. Here, we used a “rhizobox” mesocosm experimental set-up to supply different concentrations and classes of terpenes into the soil compartment with growing sorghum for 1 month to assess how these terpenes affect sorghum bacterial and fungal rhizobiome communities. Changes in bacterial and fungal communities between treatments belowground were characterized, followed by bioassays screening on bacterial and fungal isolates from the sorghum rhizosphere against terpenes to validate direct microbial responses. We found that microbial growth stimulatory and inhibitory effects were localized, terpene specific, dose dependent, and transient in time. This work paves the way for engineering terpene metabolisms in plant microbiomes for improved sustainable agriculture and bioenergy crop production. 

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5. From networks to mechanisms: A cross-scale analysis of bacterial - fungal interactions in fungal necromass

   Beatty, Briana (December 2024, University of Minnesota Graduate School)

   Microbial community dynamics are dependent on interactions between the community members, yet studies of interactions across domains and with multiple experimental approaches are lacking. In this study, we explored interactions between bacteria and fungi associated with decaying fungal necromass using both field-based co-occurrence networks and laboratory-based pairwise interactions. The majority of field-derived bacterial-fungal correlations were negative, suggesting a potentially competitive environment within necromass compared to other systems. Laboratory experiments consisted of bacteria most often reducing fungal growth, while the fungal effect on bacterial growth was more varied and dependent on bacterial taxa. However, these interactions were not consistently predicted by field correlations, highlighting a disconnect between field-based and direct experimental approaches. Our findings suggest that using co-occurrence networks alone to predict BFI outcomes could be misleading, emphasizing the need for more comprehensive, multi-method studies to capture the dynamic and context-dependent nature of microbial interactions. 

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