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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. Plant‐driven changes in soil microbial communities influence seed germination through negative feedbacks

   https://doi.org/10.1002/ece3.5476  

   Miller, Elizabeth C. ; Perron, Gabriel G. ; Collins, Cathy D. ( July 2019 , Ecology and Evolution)

   Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination.

   We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs.

   We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host‐specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host‐specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs.

   Synthesis. Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host‐specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe‐mediated interactions between plants at different life stages that next‐generation sequencing can begin to unravel.

    

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3. 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.)

   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.

   Terpenes 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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4. The Impact of Tree Species on Microbial Community Structure and Soil Function on Forest Plantations in the Central Hardwoods Region (CHR)

   https://doi.org/10.3390/f14050859  

   Gardner, Terrence G. ; Frene, Juan P. ; Lawson, Shaneka S. ; Lue Sue, Niall D. ; Handy, Jeffery ; Crawford, Ralph H. ( May 2023 , Forests)

   Interactions between above- and below-ground monoculture forest plantation components are critical to tree growth and development. Within the Central Hardwoods Region (CHR), synergistic relationships between tree species and soil microbial community structure and function have received limited research attention. Soil microbes are integral to forest ecosystems as their activities intrinsically promote soil organic matter decomposition, nutrient cycling, and ecosystem functioning. Here, we examined soils from two perfectly aligned stands of black walnut (BW, Juglans nigra L.) and Northern red oak (RO, Quercus rubra L.) trees. Measurements of selected soil chemical properties, microbial community structure using ester-linked fatty acid methyl ester (EL-FAME), and soil enzyme activities (EAs) were used. Analysis of modifications within microbial communities showed a significant positive response to BW based upon soil EAs and microbial indicators, compared to RO. Seasonal comparisons predictably revealed higher microbial activities during summer. Fungi dominated the soil microbial community structure with a fungal/bacterial ratio of 2:1. Gram-positive rather than Gram-negative bacteria or actinomycetes dominated the bacterial community. The activity of the soil enzymes ß-glucosidase and arylsulfatase increased, but ß-glucosaminidase and acid phosphatase decreased. Additionally, acid phosphatase and arbuscular mycorrhizal fungi revealed strong correlations. The differences observed in biological properties, specifically microbial communities and EAs, highlight the varied responses to BW and RO soil biology and subsequent soil ecosystem functions. These results indicate that variations in microbial abundance and soil functions occur throughout the course of an entire year.

    

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5. Burkholderia from Fungus Gardens of Fungus-Growing Ants Produces Antifungals That Inhibit the Specialized Parasite Escovopsis

   https://doi.org/10.1128/AEM.00178-21  

   Francoeur, Charlotte B. ; May, Daniel S. ; Thairu, Margaret W. ; Hoang, Don Q. ; Panthofer, Olivia ; Bugni, Tim S. ; Pupo, Mônica T. ; Clardy, Jon ; Pinto-Tomás, Adrián A. ; Currie, Cameron R. ( June 2021 , Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Within animal-associated microbiomes, the functional roles of specific microbial taxa are often uncharacterized. Here, we use the fungus-growing ant system, a model for microbial symbiosis, to determine the potential defensive roles of key bacterial taxa present in the ants’ fungus gardens. Fungus gardens serve as an external digestive system for the ants, with mutualistic fungi in the genus Leucoagaricus converting the plant substrate into energy for the ants. The fungus garden is host to specialized parasitic fungi in the genus Escovopsis . Here, we examine the potential role of Burkholderia spp. that occur within ant fungus gardens in inhibiting Escovopsis. We isolated members of the bacterial genera Burkholderia and Paraburkholderia from 50% of the 52 colonies sampled, indicating that members of the family Burkholderiaceae are common inhabitants in the fungus gardens of a diverse range of fungus-growing ant genera. Using antimicrobial inhibition bioassays, we found that 28 out of 32 isolates inhibited at least one Escovopsis strain with a zone of inhibition greater than 1 cm. Genomic assessment of fungus garden-associated Burkholderiaceae indicated that isolates with strong inhibition all belonged to the genus Burkholderia and contained biosynthetic gene clusters that encoded the production of two antifungals: burkholdine1213 and pyrrolnitrin. Organic extracts of cultured isolates confirmed that these compounds are responsible for antifungal activities that inhibit Escovopsis but, at equivalent concentrations, not Leucoagaricus spp. Overall, these new findings, combined with previous evidence, suggest that members of the fungus garden microbiome play an important role in maintaining the health and function of fungus-growing ant colonies. IMPORTANCE Many organisms partner with microbes to defend themselves against parasites and pathogens. Fungus-growing ants must protect Leucoagaricus spp., the fungal mutualist that provides sustenance for the ants, from a specialized fungal parasite, Escovopsis . The ants take multiple approaches, including weeding their fungus gardens to remove Escovopsis spores, as well as harboring Pseudonocardia spp., bacteria that produce antifungals that inhibit Escovopsis. In addition, a genus of bacteria commonly found in fungus gardens, Burkholderia , is known to produce secondary metabolites that inhibit Escovopsis spp. In this study, we isolated Burkholderia spp. from fungus-growing ants, assessed the isolates’ ability to inhibit Escovopsis spp., and identified two compounds responsible for inhibition. Our findings suggest that Burkholderia spp. are often found in fungus gardens, adding another possible mechanism within the fungus-growing ant system to suppress the growth of the specialized parasite Escovopsis . 

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