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DOE OSTI2025

Enrichment of root-associated Streptomyces strains in response to drought is driven by diverse functional traits and does not predict beneficial effects on plant growth

The genus Streptomyces has consistently been found enriched in drought-stressed plant root microbiomes, yet the ecological basis and functional variation underlying this enrichment at the strain and isolate level remain unclear. Using two 16S rRNA sequencing methods with different levels of taxonomic resolution, we confirmed drought-associated enrichment (DE) of Streptomyces in field-grown sorghum roots and identified five closely related but distinct amplicon sequence variants (ASVs) belonging to the genus with variable drought enrichment patterns. From a culture collection of sorghum root endophytes, we selected 12 Streptomyces isolates representing these ASVs for phenotypic and genomic characterization. Whole-genome sequencing revealed substantial variation in gene content, even among closely related isolates, and exometabolomic profiling showed distinct metabolic responses to media supplemented with drought- versus well-watered root tissue. Traits linked to drought survival, including osmotic stress tolerance, siderophore production, and carbon utilization, varied widely among isolates and were not phylogenetically conserved. Using a broader panel of 48 Streptomyces, we demonstrate that DE scores, determined through mono-association experiments in gnotobiotic sorghum systems, showed high variability and lacked correlation with plant growth promotion. Pangenome-wide association identified orthogroups involved in osmolyte transport (e.g., proP) and membrane biosynthesis (e.g., fabG) as positively associated with DE, though most associations lacked phylogenetic signal. Collectively, these results demonstrate that Streptomyces DE is not a conserved genus-level trait but is instead strain-specific and functionally heterogeneous. Furthermore, DE in the root microbiome was shown not to predict beneficial effects on plant growth. This work underscores the need to resolve functional traits at the strain level and highlights the complexity of microbe-host-environment interactions under abiotic stress.

Fonseca-Garcia, Citlali↗

DOE OSTI2024

Multilevel analysis between Physcomitrium patens and Mortierellaceae endophytes explores potential long‐standing interaction among land plants and fungi

SUMMARY The model moss species Physcomitrium patens has long been used for studying divergence of land plants spanning from bryophytes to angiosperms. In addition to its phylogenetic relationships, the limited number of differential tissues, and comparable morphology to the earliest embryophytes provide a system to represent basic plant architecture. Based on plant–fungal interactions today, it is hypothesized these kingdoms have a long‐standing relationship, predating plant terrestrialization. Mortierellaceae have origins diverging from other land fungi paralleling bryophyte divergence, are related to arbuscular mycorrhizal fungi but are free‐living, observed to interact with plants, and can be found in moss microbiomes globally. Due to their parallel origins, we assess here how two Mortierellaceae species, Linnemannia elongata and Benniella erionia , interact with P. patens in coculture. We also assess how Mollicute ‐related or Burkholderia ‐related endobacterial symbionts (MRE or BRE) of these fungi impact plant response. Coculture interactions are investigated through high‐throughput phenomics, microscopy, RNA‐sequencing, differential expression profiling, gene ontology enrichment, and comparisons among 99 other P. patens transcriptomic studies. Here we present new high‐throughput approaches for measuring P. patens growth, identify novel expression of over 800 genes that are not expressed on traditional agar media, identify subtle interactions between P. patens and Mortierellaceae, and observe changes to plant–fungal interactions dependent on whether MRE or BRE are present. Our study provides insights into how plants and fungal partners may have interacted based on their communications observed today as well as identifying L. elongata and B. erionia as modern fungal endophytes with P. patens .

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

Fungal community composition predicts forest carbon storage at a continental scale

Forest soils harbor hyper-diverse microbial communities which fundamentally regulate carbon and nutrient cycling across the globe. Directly testing hypotheses on how microbiome diversity is linked to forest carbon storage has been difficult, due to a lack of paired data on microbiome diversity and in situ observations of forest carbon accumulation and storage. Here, we investigated the relationship between soil microbiomes and forest carbon across 238 forest inventory plots spanning 15 European countries. We show that the composition and diversity of fungal, but not bacterial, species is tightly coupled to both forest biotic conditions and a seven-fold variation in tree growth rates and biomass carbon stocks when controlling for the effects of dominant tree type, climate, and other environmental factors. This linkage is particularly strong for symbiotic endophytic and ectomycorrhizal fungi known to directly facilitate tree growth. Since tree growth rates in this system are closely and positively correlated with belowground soil carbon stocks, we conclude that fungal composition is a strong predictor of overall forest carbon storage across the European continent.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2020

Metatranscriptomic dynamics after Verticillium dahliae infection and root damage in Olea europaea

Background: The olive tree is of particular economic interest in the Mediterranean basin. Researchers have conducted several studies on one of the most devastating disorders affecting this tree, the Verticillium wilt, which causes substantial economic losses in numerous areas. We analyzed metatranscriptomic samples taken from a previous study conducted on leaves and roots of Olea europaea that were infected with Verticillium dahliae. In addition, we also analyzed mechanically damaged roots. The aim of our approach is to describe the dynamics of the root microbiome after severe perturbations. Results: Our results not only describe the dynamics of the microbial community associated with the disturbance, but also show the high complexity of these systems and explain how this can lead to a conflicting assignment of the various types of parasitism observed in a specific organism. Conclusions: Our findings indicate that this infection, although led by Verticillium, is driven not by a single species, but by a polymicrobial consortium that also includes natural endophytes of the olive tree. This community contains both biotrophic and necrotrophic organisms that alternate and live together during the infection. In addition, opportunistic organisms appear that take profit not from plant tissues, but from new emerging populations of microorganisms. Therefore, this system can be described as a complex biological system composed of different interacting communities. Notably, our work has important considerations when it comes to classifying the type of parasitism of a given species.

Verticillium dahliae↗