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Wilkins, M. J.

Publications and source records attributed to Wilkins, M. J..

10 recordsLinked to original sources

Burn intensity regulates post-fire effects on soil N2O emissions: A grassland soil pyrocosm study

Post-fire soil emissions of nitric oxide (NO) and nitrous oxide (N2O) are important ecosystem nitrogen (N) loss pathways, but their flux dynamics vary widely across studies, making generalizations challenging. Natural variation in burn intensity--or heat energy released during combustionm--may help resolve this variability by mediating the soil physicochemical and biological drivers of these emissions. Here, we used an experimental "pyrocosm" system to evaluate how varying burn intensity influences post-fire NO and N2O emissions using soil from a Southern California grassland across 18 weeks. Over several months, we measured soil NO and N2O fluxes alongside soil pH, extractable nitrate (NO3-) and ammonium (NH4+), net NH4+ production, net nitrification, soil carbon (C) pools, microbial biomass C, and the potential activities of five extracellular hydrolytic enzymes under Control, Low- (100.1 {+/-} 20.0 oC peak soil temperature at 5 cm depth), and High-intensity (243.8 {+/-} 7.4 oC peak soil temperature at 5 cm depth) burns. Soil NO emissions were not significantly affected by burn intensity. In contrast, N2O emissions tripled under low burn intensity relative to unburned controls, but did not differ from controls at high burn intensity. This stimulation of N2O emission under low burn intensity was driven by increased denitrification, as supported by elevated soil pH and labile C availability, and an 88% reduction in net nitrification that signaled active NO3- consumption. Under high burn intensity, however, severe loss of microbial biomass, soil C, and NO3- constrained denitrification, with rising hydrolytic enzyme activities over time suggesting C limitation. Together, these findings demonstrate that post-fire N2O emissions reflect a fire intensity-dependent balance between microbial mortality and resource limitation, helping to explain divergent N emissions across ecosystems.

ecology↗

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↗

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↗

A uniform stress response of stream microbiomes in the hyporheic zone across North America

BackgroundStream hyporheic zones represent a unique ecosystem at the interface of stream water and surrounding sediments, characterized by high heterogeneity and accelerated biogeochemical activity. These zones are increasingly impacted by anthropogenic stressors and environmental changes at a global scale, directly altering their microbiomes. Despite their importance, the current body of literature lacks a systematic understanding of active nitrogen and sulfur cycling across stream sediment and surface water microbiomes, particularly across geographic locations and in response to environmental stressors. ResultsBased on previously published and unpublished datasets, 363 stream metagenomes were combined to build a comprehensive MAG and gene database from stream sediments and surface water including a full-factorial mesocosm experiment which had been deployed to unravel microbial stress response. Metatranscriptomic data from 23 hyporheic sediment samples collected across North America revealed that microbial activity in sediments was distinct from the activity in surface water, contrasting similarly encoded metabolic potential across the two compartments. The expressed energy metabolism of the hyporheic zone was characterized by increased cycling of sulfur and nitrogen compounds, governed by Nitrospirota and Desulfobacterota lineages. While core metabolic functions like energy conservation were conserved across sediments, temperature and stream order change resulted in differential expression of stress response genes previously observed in mesocosm studies. ConclusionsThe hyporheic zone is a microbial hotspot in stream ecosystems, surpassing the activity of overlaying riverine surface waters. Metabolic activity in the form of sulfur and nitrogen cycling in hyporheic sediments is governed by multiple taxa interacting through metabolic handoffs. Despite the spatial heterogeneity of streams, the hyporheic sediment microbiome encodes and expresses conserved stress responses to anthropogenic stressors, e.g., temperature, in streams of separate continents. The high number of uncharacterized differentially expressed genes as a response to tested stressors is a call-to-action to deepen the study of stream systems.

microbiology↗

Metabolic interactions underpinning high methane fluxes across terrestrial freshwater wetlands

Current estimates of wetland contributions to the global methane budget carry high uncertainty, particularly in accurately predicting emissions from high methane-emitting wetlands. Microorganisms mediate methane cycling, yet knowledge of their conservation across wetlands remains scarce. To address this, we integrated 1,118 16S rRNA amplicon datasets (116 new), 305 metagenomes (20 new) that yielded 4,745 medium and high-quality metagenome assembled genomes (MAGs; 617 new), 133 metatranscriptomes, and annual methane flux data across 9 wetlands to create the Multi-Omics for Understanding Climate Change (MUCC) v2.0.0 database. This new resource was leveraged to link microbiome compositional profiles to encoded functions and emissions, with specific focus on methane-cycling populations and the microbial carbon decomposition networks that fuel them. We identified eight methane-cycling genera that were conserved across wetlands, and deciphered wetland specific metabolic interactions across marshes, revealing low methanogen-methanotroph connectivity in high-emitting wetlands. Methanoregula emerged as a hub methanogen across networks and was a strong predictor of methane flux, demonstrating the potential broad relevance of methylotrophic methanogenesis in these ecosystems. Collectively, our findings illuminate trends between microbial decomposition networks and methane flux and provide an extensive publicly available database to advance future wetland research.

microbiology↗

A functional microbiome catalog crowdsourced from North American rivers

Predicting elemental cycles and maintaining water quality under increasing anthropogenic influence requires understanding the spatial drivers of river microbiomes. However, the unifying microbial processes governing river biogeochemistry are hindered by a lack of genome-resolved functional insights and sampling across multiple rivers. Here we employed a community science effort to accelerate the sampling, sequencing, and genome-resolved analyses of river microbiomes to create the Genome Resolved Open Watersheds database (GROWdb). This resource profiled the identity, distribution, function, and expression of thousands of microbial genomes across rivers covering 90% of United States watersheds. Specifically, GROWdb encompasses 1,469 microbial species from 27 phyla, including novel lineages from 10 families and 128 genera, and defines the core river microbiome for the first time at genome level. GROWdb analyses coupled to extensive geospatial information revealed local and regional drivers of microbial community structuring, while also presenting a myriad of foundational hypotheses about ecosystem function. Building upon the previously conceived River Continuum Concept1, we layer on microbial functional trait expression, which suggests the structure and function of river microbiomes is predictable. We make GROWdb available through various collaborative cyberinfrastructures2, 3 so that it can be widely accessed across disciplines for watershed predictive modeling and microbiome-based management practices.

microbiology↗

Long-term CRISPR array dynamics and stable host-virus co-existence in subsurface fractured shales

Viruses are the most ubiquitous biological entities on earth. Even so, elucidating the impact of viruses on microbial communities and associated ecosystem processes often requires identification of strong host-virus linkages - an undeniable challenge in many ecosystems. Subsurface fractured shales present a unique opportunity to first make these strong linkages and subsequently reveal complex long-term host-virus dynamics and trends in CRISPR array size and frequency. Here, we sampled two replicated sets of fractured shale wells for nearly 800 days (Denver-Julesburg Basin, Colorado, USA). We identified a relatively diverse microbial community with widely encoded CRISPR viral defense systems, which facilitated 2,110 CRISPR-based viral linkages across 90 host MAGs representing 25 phyla. Leveraging these linkages with timeseries data across differing well ages, we observed how patterns of host-virus co-existence develop and converge in this closed ecosystem through time. We observed a transition to smaller CRISPR arrays in older, more established wells, potentially reflecting a natural progression where CRISPR arrays harbor fewer, yet more effective spacers that target viral genes with fewer mutations. Together, our findings shed light on the complexities of host-virus temporal dynamics as well as possible drivers of spacer loss and acquisition within CRISPR arrays of diverse microbial populations through time.

microbiology↗

Implications of sample treatment on characterization of the riverine environmental metabolome

High-resolution mass spectrometry techniques are widely used in the environmental sciences to characterize natural organic matter and, when utilizing these instruments, researchers must make multiple decisions regarding sample pre-treatment and the instrument ionization mode. To identify how these choices alter organic matter characterization and resulting conclusions, we analyzed a collection of 17 riverine samples from East River, CO (USA) under four PPL-based Solid Phase Extraction (SPE) treatment and electrospray ionization polarity (e.g., positive and negative) combinations: SPE (+), SPE (-), non-SPE (-), and non-SPE (+). The greatest number of formula assignments were achieved with SPE-treated samples due to the removal of compounds that could interfere with ionization. Furthermore, the SPE (-) treatment captured the most formulas across the widest chemical compound diversity. In addition to a reduced number of assigned formulas, the non-SPE datasets resulted in altered thermodynamic interpretations that could cascade into incomplete assumptions about the availability of organic matter pools for microbial heterotrophic respiration. Thus, we infer that the SPE (-) treatment is the best single method for characterizing environmental organic matter pools unless the focus is on lipid-like compounds, in which case we recommend a combination of SPE (-) and SPE (+) to adequately characterize these molecules. SynopsisWe provide data-driven sample treatment and ionization mode recommendations to researchers who aim to use high-resolution mass spectrometry to characterize environmental organic matter. Abstract Art O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

ecology↗

Playing with FiRE: A genome resolved view of the soil microbiome responses to high severity forest wildfire

Warming climate has increased the frequency and size of high severity wildfires in the western United States, with deleterious impacts on forest ecosystem resilience. Although forest soil microbiomes provide a myriad of ecosystem functions, little is known regarding the impact of high severity fire on microbially-mediated processes. Here, we characterized functional shifts in the soil microbiome (bacterial, fungal, and viral) across wildfire burn severity gradients one year post-fire in coniferous forests (Colorado and Wyoming, USA). We generated the Fire Responding Ecogenomic database (FiRE-db), consisting of 637 metagenome-assembled bacterial genomes, 2490 viral populations, and 2 fungal genomes complemented by 12 metatranscriptomes from soils affected by low and high-severity, and complementary marker gene sequencing and metabolomics data. Actinobacteria dominated the fraction of enriched and active taxa across burned soils. Taxa within surficial soils impacted by high severity wildfire exhibited traits including heat resistance, sporulation and fast growth that enhanced post-fire survival. Carbon cycling within this system was predicted to be influenced by microbial processing of pyrogenic compounds and turnover of dominant bacterial community members by abundant viruses. These genome-resolved analyses across trophic levels reveal the complexity of post-fire soil microbiome activity and offer opportunities for restoration strategies that specifically target these communities.

microbiology↗

Borgs are giant extrachromosomal elements with the potential to augment methane oxidation

Anaerobic methane oxidation exerts a key control on greenhouse gas emissions 1, yet factors that modulate the activity of microorganisms performing this function remain little explored. In studying groundwater, sediments, and wetland soil where methane production and oxidation occur, we discovered extraordinarily large, diverse DNA sequences that primarily encode hypothetical proteins. Four curated, complete genomes are linear, up to ~1 Mbp in length and share genome organization, including replicore structure, long inverted terminal repeats, and genome-wide unique perfect tandem direct repeats that are intergenic or generate amino acid repeats. We infer that these are a new type of archaeal extrachromosomal element with a distinct evolutionary origin. Gene sequence similarity, phylogeny, and local divergence of sequence composition indicate that many of their genes were assimilated from methane-oxidizing Methanoperedens archaea. We refer to these elements as "Borgs". We identified at least 19 different Borg types coexisting with Methanoperedens in four distinct ecosystems. Borg genes expand redox and respiratory capacity (e.g., clusters of multiheme cytochromes), ability to respond to changing environmental conditions, and likely augment Methanoperedens capacity for methane oxidation (e.g., methyl coenzyme M reductase). By this process, Borgs could play a previously unrecognized role in controlling greenhouse gas emissions.

microbiology↗