Biology subjects

Enright, D. J.

Publications and source records attributed to Enright, D. J..

4 recordsLinked to original sources

bioRxiv2025

Strain-Level Adaptation of Pyrophilous Bacteria through Gene Fragmentation and Horizontal Gene Transfer

Wildfires reshape soil carbon (C) and nitrogen (N) dynamics by generating pyrogenic organic matter (PyOM) and selecting for pyrophilous "fire-loving" bacteria, yet the genomic mechanisms underpinning their post-fire adaptations are largely unknown. We combined comparative genomics of 16 pyrophilous bacteria spanning three phyla with bioassays and transcriptome profiling following PyOM exposure to test whether post-fire conditions promote genomic innovation within bacterial populations. Pyrophilous bacterial isolates exhibited genomic novelty through gene fragmentation, horizontal gene transfer (HGT), and plasmid-mediated operon expansion, enriching aromatic C degradation and N acquisition genes relative to non-pyrophilous sister taxa. Plasmid-encoded PyOM metabolism genes showed evidence of HGT across pyrophilous bacterial orders and cross-kingdom with pyrophilous fungi. Bioassays revealed overflow organic acid production associated with variation in tricarboxylic acid cycle genes, potentially moderating elevated post-fire soil pH and facilitating microbial succession. Our findings reveal how fire selects for bacterial genomic innovation and illuminate microbial evolution in extreme environments.

microbiology↗

bioRxiv2025

Gene Duplication, Horizontal Gene Transfer, and Trait Trade-offs Drive Evolution of Post-Fire Resource Acquisition in Pyrophilous Fungi

Wildfires significantly alter soil carbon (C) and nitrogen (N), reducing microbial richness and biomass, while selecting for "fire-loving" pyrophilous microbes that drive post-fire nutrient cycling. However, the genomic strategies and functional trade-offs (balancing gains in one trait with costs in another) underlying the traits that enable pyrophilous microbes to survive and thrive post-fire are virtually unknown. We hypothesized that pyrophilous fungi employ specialized genomic adaptations for C and N cycling, with evolutionary trade-offs between traits governing aromatic C degradation, N acquisition pathways, and rapid growth. To test these hypotheses, we performed complementary comparative genomics, transcriptomics after pyrogenic organic matter amendment, and growth rate bioassays for 18 pyrophilous fungi from five Ascomycota (Eurotiales, Pleosporales, Sordariales, Coniochaetales, and Pezizales) and three Basidiomycota (Agaricales, Holtermaniales, and Geminibasidiales) orders isolated from burned soils. We found a dramatic trait trade-off between fast growth and number of genes responsible for aromatic C degradation, implying burned environments select for metabolically costly genes despite their evolutionary cost. We used the comparative genomics framework to evaluate genomic signatures of evolution and found that either gene duplication and somatic mutation, or recombination via sexual reproduction, were the primary drivers of fungal genomic variation in aromatic C degradation and N acquisition genes. Finally, we identified cross-kingdom bacterial to fungal horizontal gene transfer as a secondary strategy producing novel aromatic C degradation genes. Overall, we found that trait trade-offs and genome evolutionary strategies are key drivers that may predict the persistence and contribution of pyrophilous fungi to global C and N cycling. Significance statementWildfires affect large tracts of the terrestrial biosphere, and while much is understood about plant adaptations to fire, here we uncovered for the first time genomic adaptations in fungi that can be modeled to predict impacts on global C and N cycling. We tested theorized trait trade-offs, and showed with genomics and bioassays how evolutionary trade-offs, like prioritizing aromatic C degradation at the expense of rapid growth, enable pyrophilous fungi to thrive post-fire. Further, we advance fungal genomics, and reveal the importance of mechanisms like gene duplication, sexual reproduction, and cross-kingdom horizontal gene transfer for enabling adaptation and evolutionary diversification in fungi. Finally, we identify fungi that may be useful inoculants to enhance recovery of polluted or burned soils.

genomics↗

bioRxiv2024

Evaluating Best Practices for Isolating Pyrophilous Bacteria and Fungi from Burned Soil

A live microbial culture is invaluable to assess traits and functions, yet culturing immediately from fresh soil is logistically challenging and media selection is not trivial. Deeper ecological understanding of pyrophilous microbes and their traits is hampered by a lack of culture-based work causing researchers to rely heavily on community sequence analysis. To improve our understanding of isolating pyrophilous bacteria and fungi after wildfires from burned soil, we tested which: 1) soil storage method and 2) media retained highest genera richness and highest culturable viability as measured by CFUs retained. We tested four soil storage methods (dried, refrigerated at 4{degrees}C, stored at -80{degrees}C with or without glycerol) using a well-homogenized soil sample, plated microbes on rich media, and compared to fresh soil obtained 6 months after a severe California shrubland wildfire. From the fresh soils, we tested 3 media types: rich (Lysogeny Broth (LB) for bacteria; Malt Yeast Agar (MYA) for fungi), oligotrophic (Reasoners 2 Agar (R2A)) and media made from pyrogenic organic matter (PyOM). For bacteria, storing soil frozen at -80{degrees}C without glycerol yielded the highest genera richness and with glycerol preserved the most species. For fungi, storing soil at -80{degrees}C without glycerol preserved the most species but preserved equivalent richness of genera as fresh and 4{degrees}C soil. R2A yielded the highest bacterial and fungal genus richness but some species of interest were only captured with PyOM. Using a combination of these storage and media methods along with a few additional techniques (mushroom cultivation, smoke cultivation, etc.) from 2018-2022, we cultured >500 isolates (286 bacteria; 258 fungi) after 7 California wildfires for testing pyrophilous microbial traits. ImportanceFires are increasing in frequency and severity across the globe, making the understanding of the traits of the pyrophilous microbes that survive and thrive post-fire and influence post-fire ecosystem regeneration critical and pressing. Yet, our ability to characterize the traits of pyrophilous microbes through genomics, transcriptomics, and phenotypic assays is hampered by lack of organisms in culture. Here, we debut a new medium created from pyrogenic organic matter that helps to cultivate fastidious pyrophilous microbes, and also describe a large-scale culture collection of pyrophilous bacteria and fungi (>500 isolates) that can be used for future collaborative research. We comprehensively test how soil storage and media type affect the cultivation of both bacteria and fungi, and for the first time, we test the best method to store soil to retain fungal diversity. Our work can be applied to improve culture collections of fastidious microbes from a variety of environments.

microbiology↗

bioRxiv2021

Mega-fire in Redwood Tanoak Forest Reduces Bacterial and Fungal Richness and Selects for Pyrophilous Taxa and Traits that are Phylogenetically Conserved

Mega-fires of unprecedented size, intensity, and socio-economic impacts have surged globally due to climate change, fire suppression, and development. Soil microbiomes are critical for post-fire plant regeneration and nutrient cycling, yet how mega-fires impact the soil microbiome remains unclear. We had a serendipitous opportunity to obtain pre- and post-fire soils from the same sampling locations because the 2016 Soberanes Fire, a mega-fire burning >500 Km2, burned with high severity throughout several of our established redwood-tanoak plots. This makes our study the first to examine microbial fire response in redwood-tanoak forests. We re-sampled soils immediately post-fire from two burned plots and one unburned plot to elucidate the effect of mega-fire on soil microbiomes. We used Illumina MiSeq sequencing of 16S and ITS1 to determine that both bacterial and fungal richness were reduced by 38-70% in burned plots, with richness unchanged in the unburned plot. Fire altered composition by 27% for bacteria and 24% for fungi, whereas the unburned plots experienced no change in fungal and negligible change in bacterial composition. We observed several pyrophilous taxa previously observed in Pinaceae forests, indicating that these microbes are likely general fire-responders across forest types. Further, the pyrophilous taxa that positively responded to fire were phylogenetically conserved, suggesting shared evolutionary traits. For bacteria, fire selected for increased Firmicutes and Actinobacteria. For fungi, fire selected for the Ascomycota classes Pezizomycetes and Eurotiomycetes and for a Basidiomycota class of heat-resistant Geminibasidiomycete yeasts. We hypothesize that microbes share analogous fire response to plants and propose a trait-based conceptual model of microbial response to fire that builds from Grimes Competitor-Stress tolerator-Ruderal framework (C-S-R) and its recent applications to microbes. Using this framework and established literature on several microbial species, we hypothesize some generalizable principals to predict which microbial taxa will respond to fire.

ecology↗