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At least 19 records
All sourcesNASA NTRSDOE OSTI
DOE OSTI2020

Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota

Ascomycota, the largest and most well-studied phylum of fungi, contains three subphyla: Saccharomycotina (budding yeasts), Pezizomycotina (filamentous fungi), and Taphrinomycotina (fission yeasts). Despite its importance, we lack a comprehensive genome-scale phylogeny or understanding of the similarities and differences in the mode of genome evolution within this phylum. By examining 1107 genomes from Saccharomycotina (332), Pezizomycotina (761), and Taphrinomycotina (14) species, we inferred a robust genome-wide phylogeny that resolves several contentious relationships and estimated that the Ascomycota last common ancestor likely originated in the Ediacaran period. Comparisons of genomic properties revealed that Saccharomycotina and Pezizomycotina differ greatly in their genome properties and enabled inference of the direction of evolutionary change. The Saccharomycotina typically have smaller genomes, lower guanine-cytosine contents, lower numbers of genes, and higher rates of molecular sequence evolution compared with Pezizomycotina. These results provide a robust evolutionary framework for understanding the diversity and ecological lifestyles of the largest fungal phylum.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Luteibacter mycovicinus sp. nov., a yellow-pigmented gammaproteobacterium found as an endohyphal symbiont of endophytic Ascomycota

We isolated and described a yellow-pigmented strain of bacteria (strain 9143 T ), originally characterized as an endohyphal inhabitant of an endophytic fungus in the Ascomycota. Although the full-length sequence of its 16S rRNA gene displays 99 % similarity to Luteibacter pinisoli, genomic hybridization demonstrated <30 % genomic similarity between 9143 T and its closest named relatives, further supported by average nucleotide identity results. This and related endohyphal strains form a well-supported clade separate from L. pinisoli and other validly named species including the most closely related Luteibacter rhizovicinus. The name Luteibacter mycovicinus sp. nov. is proposed, with type strain 9143 T (isolate DBL433), for which a genome has been sequenced and is publicly available from the American Type Culture Collection (ATCC TSD-257 T ) and from the Leibniz Institute DSMZ (DSM 112764 T ). The type strain reliably forms yellow colonies across diverse media and growth conditions (lysogeny broth agar, King’s Medium B, potato dextrose agar, trypticase soy agar and Reasoner's 2A (R2A) agar). It forms colonies readily at 27 °C on agar with a pH of 6–8, and on salt (NaCl) concentrations up to 2 %. It lacks the ability to utilize sulphate as a sulphur source and thus only forms colonies on minimal media if supplemented with alternative sulphur sources. It is catalase-positive and oxidase-negative. Although it exhibits a single polar flagellum, motility was only clearly visible on R2A agar. Its host range and close relatives, which share the endohyphal lifestyle, are discussed.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Phylogenomic insights into the taxonomy, ecology, and mating systems of the lorchel family Discinaceae (Pezizales, Ascomycota)

Lorchels, also known as false morels (Gyromitra sensu lato), are iconic due to their brain-shaped mushrooms and production of gyromitrin, a deadly mycotoxin. Molecular phylogenetic studies have hitherto failed to resolve deep-branching relationships in the lorchel family, Discinaceae, hampering our ability to settle longstanding taxonomic debates and to reconstruct the evolution of toxin production. We generated 75 draft genomes from cultures and ascomata (some collected as early as 1960), conducted phylogenomic analyses using 1542 single-copy orthologs to infer the early evolutionary history of lorchels, and identified genomic signatures of trophic mode and mating-type loci to better understand lorchel ecology and reproductive biology. Our phylogenomic tree was supported by high gene tree concordance, facilitating taxonomic revisions in Discinaceae. We recognized 10 genera across two tribes: tribe Discineae (Discina, Maublancomyces, Neogyromitra, Piscidiscina, and Pseudodiscina) and tribe Gyromitreae (Gyromitra, Hydnotrya, Paragyromitra, Pseudorhizina, and Pseudoverpa); Piscidiscina was newly erected and 26 new combinations were formalized. Paradiscina melaleuca and Marcelleina donadinii formed their own family-level clade sister to Morchellaceae, which merits further taxonomic study. Genome size and CAZyme content were consistent with a mycorrhizal lifestyle for the truffle species (Hydnotrya spp.), whereas the other Discinaceae genera possessed genomic properties of a saprotrophic habit. Lorchels were found to be predominantly heterothallic-either MAT1-1 or MAT1-2-but a single occurrence of colocalized mating-type idiomorphs indicative of homothallism was observed in Gyromitra esculenta strain CBS101906 and requires additional confirmation and follow-up study. Lastly, we confirmed that gyromitrin has a phylogenetically discontinuous distribution, having been detected exclusively in two distantly related genera (Gyromitra and Piscidiscina) belonging to separate tribes. Our genomic dataset will facilitate further investigations into the gyromitrin biosynthesis genes and their evolutionary history. With additional sampling of Geomoriaceae and Helvellaceae-two closely related families with no publicly available genomes-these data will enable comprehensive studies on the independent evolution of truffles and ecological diversification in an economically important group of pezizalean fungi.

Dirks, Alden C↗
DOE OSTI2023

A genome-informed higher rank classification of the biotechnologically important fungal subphylum Saccharomycotina

The subphylum Saccharomycotina is a lineage in the fungal phylum Ascomycota that exhibits levels of genomic diversity similar to those of plants and animals. The Saccharomycotina consist of more than 1 200 known species currently divided into 16 families, one order, and one class. Species in this subphylum are ecologically and metabolically diverse and include important opportunistic human pathogens, as well as species important in biotechnological applications. Many traits of biotechnological interest are found in closely related species and often restricted to single phylogenetic clades. However, the biotechnological potential of most yeast species remains unexplored. Although the subphylum Saccharomycotina has much higher rates of genome sequence evolution than its sister subphylum, Pezizomycotina, it contains only one class compared to the 16 classes in Pezizomycotina. The third subphylum of Ascomycota, the Taphrinomycotina, consists of six classes and has approximately 10 times fewer species than the Saccharomycotina. These data indicate that the current classification of all these yeasts into a single class and a single order is an underappreciation of their diversity. Our previous genome-scale phylogenetic analyses showed that the Saccharomycotina contains 12 major and robustly supported phylogenetic clades; seven of these are current families (Lipomycetaceae, Trigonopsidaceae, Alloascoideaceae, Pichiaceae, Phaffomycetaceae, Saccharomycodaceae, and Saccharomycetaceae), one comprises two current families (Dipodascaceae and Trichomonascaceae), one represents the genus Sporopachydermia, and three represent lineages that differ in their translation of the CUG codon (CUG-Ala, CUG-Ser1, and CUG-Ser2). Using these analyses in combination with relative evolutionary divergence and genome content analyses, we propose an updated classification for the Saccharomycotina, including seven classes and 12 orders that can be diagnosed by genome content. This updated classification is consistent with the high levels of genomic diversity within this subphylum and is necessary to make the higher rank classification of the Saccharomycotina more comparable to that of other fungi, as well as to communicate efficiently on lineages that are not yet formally named.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Microbial Type IA Topoisomerase C-Terminal Domain Sequence Motifs, Distribution and Combination

Type IA topoisomerases have highly conserved catalytic N-terminal domains for the cleaving and rejoining of a single DNA/RNA strand that have been extensively characterized. In contrast, the C-terminal region has been less covered. Two major types of small tandem C-terminal domains, Topo_C_ZnRpt (containing C4 zinc finger) and Topo_C_Rpt (without cysteines) were initially identified in Escherichia coli and Mycobacterium tuberculosis topoisomerase I, respectively. Their structures and interaction with DNA oligonucleotides have been revealed in structural studies. Here, we first present the diverse distribution and combinations of these two structural elements in various bacterial topoisomerase I (TopA). Previously, zinc fingers have not been seen in type IA topoisomerases from well-studied fungal species within the phylum Ascomycota. In our extended studies of C-terminal DNA-binding domains, the presence of zf-GRF and zf-CCHC types of zinc fingers in topoisomerase III (Top3) from fungi species in many phyla other than Ascomycota has drawn our attention. We secondly analyze the distribution and combination of these fungal zf-GRF- and zf-CCHC-containing domains. Their potential structures and DNA-binding mechanism are evaluated. The highly diverse arrangements and combinations of these DNA/RNA-binding domains in microbial type IA topoisomerase C-terminal regions have important implications for their interactions with nucleic acids and protein partners as part of their physiological functions.

59 BASIC BIOLOGICAL SCIENCES↗
NASA NTRS2004

A molecular timescale of eukaryote evolution and the rise of complex multicellular life

BACKGROUND: The pattern and timing of the rise in complex multicellular life during Earth's history has not been established. Great disparity persists between the pattern suggested by the fossil record and that estimated by molecular clocks, especially for plants, animals, fungi, and the deepest branches of the eukaryote tree. Here, we used all available protein sequence data and molecular clock methods to place constraints on the increase in complexity through time. RESULTS: Our phylogenetic analyses revealed that (i) animals are more closely related to fungi than to plants, (ii) red algae are closer to plants than to animals or fungi, (iii) choanoflagellates are closer to animals than to fungi or plants, (iv) diplomonads, euglenozoans, and alveolates each are basal to plants+animals+fungi, and (v) diplomonads are basal to other eukaryotes (including alveolates and euglenozoans). Divergence times were estimated from global and local clock methods using 20-188 proteins per node, with data treated separately (multigene) and concatenated (supergene). Different time estimation methods yielded similar results (within 5%): vertebrate-arthropod (964 million years ago, Ma), Cnidaria-Bilateria (1,298 Ma), Porifera-Eumetozoa (1,351 Ma), Pyrenomycetes-Plectomycetes (551 Ma), Candida-Saccharomyces (723 Ma), Hemiascomycetes-filamentous Ascomycota (982 Ma), Basidiomycota-Ascomycota (968 Ma), Mucorales-Basidiomycota (947 Ma), Fungi-Animalia (1,513 Ma), mosses-vascular plants (707 Ma), Chlorophyta-Tracheophyta (968 Ma), Rhodophyta-Chlorophyta+Embryophyta (1,428 Ma), Plantae-Animalia (1,609 Ma), Alveolata-plants+animals+fungi (1,973 Ma), Euglenozoa-plants+animals+fungi (1,961 Ma), and Giardia-plants+animals+fungi (2,309 Ma). By extrapolation, mitochondria arose approximately 2300-1800 Ma and plastids arose 1600-1500 Ma. Estimates of the maximum number of cell types of common ancestors, combined with divergence times, showed an increase from two cell types at 2500 Ma to approximately 10 types at 1500 Ma and 50 cell types at approximately 1000 Ma. CONCLUSIONS: The results suggest that oxygen levels in the environment, and the ability of eukaryotes to extract energy from oxygen, as well as produce oxygen, were key factors in the rise of complex multicellular life. Mitochondria and organisms with more than 2-3 cell types appeared soon after the initial increase in oxygen levels at 2300 Ma. The addition of plastids at 1500 Ma, allowing eukaryotes to produce oxygen, preceded the major rise in complexity.

Evolution, Molecular↗
DOE OSTI2023

Phylogenomics and diversification of Sordariomycetes

The Sordariomycetes is a specious, morphologically diverse, and widely distributed class of the phylum Ascomycota that forms a well-supported clade diverged from Leotiomycetes. Aside from their ecological significance as plant and human pathogens, saprobes, endophytes, and fungicolous taxa, species of Sordariomycetes produces a wide range of chemically novel and diverse metabolites used in important fields. Recent phylogenetic analyses derived from a small number of genes have considerably increased our understanding of the family, order, and subclass relationships within Sordariomycetes, but several important groups have not been resolved well. In addition, there are various paraphyletic or polyphyletic groups. Moreover, the criteria used to establish higher ranks remain highly variable across different studies. Therefore, the taxonomy of Sordariomycetes is in constant flux, remains poorly understood, and is subject to much controversy. Here, for the first time, we have assembled a phylogenetic dataset containing 638 genomes representing the 156 genera, 50 families, and 17 orders and 5 subclasses of Sordariomycetes. This data set is based on 1124 genes and results in a well-resolved phylogenomic tree. We further constructed an evolutionary timeline of Sordariomycetes diversification based on the genomic data sets. Our divergence time estimate results are inconsistent with previous studies, suggesting estimates of node ages are less precise and varied. Based on these results, we discuss the higher ranks of Sordariomycetes and empirically propose an unprecedented taxonomic framework for the class.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Variation in hyphal production rather than turnover regulates standing fungal biomass in temperate hardwood forests

Abstract Soil fungi link above‐ and belowground carbon (C) fluxes through their interactions with plants and contribute to C and nutrient dynamics through the production, turnover, and activity of fungal hyphae. Despite their importance to ecosystem processes, estimates of hyphal production and turnover rates are relatively uncommon, especially in temperate hardwood forests. We sequentially harvested hyphal ingrowth bags to quantify the rates of Dikarya (Ascomycota and Basidiomycota) hyphal production and turnover in three hardwood forests in the Midwestern United States, where plots differed in their abundance of arbuscular (AM)‐ vs. ectomycorrhizal (ECM)‐associated trees. Hyphal production rates increased linearly with the percentage of ECM trees and annual production rates were 66% higher in ECM‐ than AM‐dominated plots. Hyphal turnover rates did not differ across the mycorrhizal gradient (plots varying in their abundance of AM vs. ECM trees), suggesting that the greater fungal biomass in ECM‐dominated plots relates to greater fungal production rather than slower fungal turnover. Differences in hyphal production across the gradient aligned with distinctly different fungal communities and activities. As ECM trees increased in dominance, fungi inside ingrowth bags produced more extracellular enzymes involved in degrading nitrogen (N)‐bearing relative to C‐bearing compounds, suggesting greater fungal (and possibly plant) N demand in ECM‐dominated soils. Collectively, our results demonstrate that shifts in temperate tree species composition that result in changes in the dominant type of mycorrhizal association may have strong impacts on Dikarya hyphal production, fungal community composition and extracellular enzyme activity, with important consequences for soil C and N cycling.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Habitat specialization and edge effects of soil microbial communities in a fragmented landscape

Abstract Soil microorganisms play outsized roles in nutrient cycling, plant health, and climate regulation. Despite their importance, we have a limited understanding of how soil microbes are affected by habitat fragmentation, including their responses to conditions at fragment edges, or “edge effects.” To understand the responses of soil communities to edge effects, we analyzed the distributions of soil bacteria, archaea, and fungi in an experimentally fragmented system of open patches embedded within a forest matrix. In addition, we identified taxa that consistently differed among patch, edge, or matrix habitats (“specialists”) and taxa that showed no habitat preference (“nonspecialists”). We hypothesized that microbial community turnover would be most pronounced at the edge between habitats. We also hypothesized that specialist fungi would be more likely to be mycorrhizal than nonspecialist fungi because mycorrhizae should be affected more by different plant hosts among habitats, whereas specialist prokaryotes would have smaller genomes (indicating reduced metabolic versatility) and be less likely to be able to sporulate than nonspecialist prokaryotes. Across all replicate sites, the matrix and patch soils harbored distinct microbial communities. However, sites where the contrasts in vegetation and pH between the patch and matrix were most pronounced exhibited larger differences between patch and matrix communities and tended to have edge communities that differed from those in the patch and forest. There were similar numbers of patch and matrix specialists, but very few edge specialist taxa. Acidobacteria and ectomycorrhizae were more likely to be forest specialists, while Chloroflexi, Ascomycota, and Glomeromycota (i.e., arbuscular mycorrhizae) were more likely to be patch specialists. Contrary to our hypotheses, nonspecialist bacteria were not more likely than specialist bacteria to have larger genomes or to be spore‐formers. We found partial support for our mycorrhizal hypothesis: arbuscular mycorrhizae, but not ectomycorrhizae, were more likely to be specialists. Overall, our results indicate that soil microbial communities are sensitive to edges, but not all taxa are equally affected, with arbuscular mycorrhizae in particular showing a strong response to habitat edges. In the context of increasing habitat fragmentation worldwide, our results can help inform efforts to maintain the structure and functioning of the soil microbiome.

Winfrey, Claire C. [Department of Ecology and Evol↗
DOE OSTI2020

Keratinophilic fungi: Specialized fungal communities in a desert ecosystem identified using cultured-based and Illumina sequencing approaches

Soil fungi in desert ecosystems are adapted to harsh environmental conditions such as high soil surface temperatures and limited organic matter and water. Given limited carbon inputs from plant material, heterotrophic fungi likely use unconventional sources of carbon in these systems. A baiting method was used to culture keratinophilic fungi from biocrust and rhizosphere soils in an arid grassland in Utah, USA. Fungi were baited using llama and sheep wool, horsehair, and snakeskin on two media, and pure cultures were identified using ITS and LSU rRNA sequences. One hundred-eighteen fungal colonies were grown, representing a total of 32 Operational Taxonomic Units (OTUs) at 97 % similarity. Cultures were dominated by the phylum Ascomycota (88 %) followed by Mucoromycota (8.6 %) and Basidiomycota (3.4 %). The orders Pleosporales, Eurotiales, Hypocreales, and Sordariales were commonly isolated, with the dominant taxa Alternaria (27 %), Aspergillus (22 %), Fusarium (11 %), and Chaetomium (8%). Thirty percent of the fungi isolated have the capacity to degrade keratin in vitro using a keratin azure assay, with Penicillium showing the highest degradation followed by Geomyces, Alternaria, and Fusarium. Although keratin degraders can be infectious, dermatophytes associated with skin infections were not isolated in culture or detected in Illumina sequencing. Illumina sequencing was used to determine general patterns in seasonal variation and habitat preference of keratinophiles. Alternaria was the most abundant genus with >70 % of the sequences. The combination of Illumina data with culture-dependent approaches facilitated the characterization of a specialized community and confirmed the low abundance of dermatophytes in this arid site.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Necromass responses to warming: A faster microbial turnover in favor of soil carbon stabilisation

Microbial byproducts and residues (hereafter ‘necromass’) potentially play the most critical role in soil organic carbon (SOC) sequestration. However, little is known about the influence of climate warming on necromass accumulation in the agroecosystem and the underlying mechanisms associated with microbial life strategies. Here, in order to address these knowledge gaps, we used amino sugars as biomarkers of microbial necromass, and investigated their variation through an 8-year trial in an agroecosystem with two warming levels (+1.6 and + 3.2 °C) compared to ambient temperature. The results showed that the lower warming level had no impact on total microbial necromass carbon. Conversely, warming the soil 3.2 °C above ambient increased total microbial necromass by 17 % and its contribution to SOC by 21.3 %, mainly by increasing fungal necromass (+19.8 %), whereas +3.2 °C warming had no impact on bacterial necromass. At the phylum level, compared with the ambient control, +3.2 °C warming induced an increase in the abundance of Proteobacteria and a decrease in both Acidobacteria and Actinobacteria, whereas in the fungal community, Ascomycota increased and Mortierellomycota decreased. This indicates that r-strategists outcompete K-strategists in warmer climates, which led to increased microbial necromass production and accumulation, as supported by the positive correlation between r-strategists and microbial necromass. Stronger microbial competition for resources also resulted in a higher biomass turnover rate, greater cell death, and greater production of microbial necromass. This was supported by the lower bacterial and fungal network complexity and trophic links under warming conditions. In addition, the necromass generated from accelerated microbial turnover further offsets warming-induced deceases in microbial biomass. Consequently, bulk SOC did not change, despite microbial necromass having a much greater response to warming than the soil C pool. Therefore, future climate warming may influence the composition and persistence of SOC during microbial degradation.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2020

Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria

The fungal genus Armillaria contains necrotrophic pathogens and some of the largest terrestrial organisms that cause tremendous losses in diverse ecosystems, yet how they evolved pathogenicity in a clade of dominantly non-pathogenic wood degraders remains elusive. Here we show that Armillaria species, in addition to gene duplications and de novo gene origins, acquired at least 1,025 genes via 124 horizontal gene transfer events, primarily from Ascomycota. Horizontal gene transfer might have affected plant biomass degrading and virulence abilities of Armillaria, and provides an explanation for their unusual, soft rot-like wood decay strategy. Furthermore, combined multi-species expression data revealed extensive regulation of horizontally acquired and wood-decay related genes, putative virulence factors and two novel conserved pathogenicity-induced small secreted proteins, which induced necrosis in planta. Overall, this study details how evolution knitted together horizontally and vertically inherited genes in complex adaptive traits of plant biomass degradation and pathogenicity in important fungal pathogens.

60 APPLIED LIFE SCIENCES↗
DOE OSTI2021

The interplay of labile organic carbon, enzyme activities and microbial communities of two forest soils across seasons

Soil labile organic carbon (LOC) responds rapidly to environmental changes and plays an important role in carbon cycle. In this study, the seasonal fluctuations in LOC, the activities of carbon-cycle related enzymes, and the bacterial and fungal communities were analyzed for soils collected from two forests, namely Betula albosinensis (Ba) and Picea asperata Mast. (Pa), in the Qinling Mountains of China. Results revealed that the seasonal average contents of microbial biomass carbon (MBC), easily oxidized organic carbon (EOC), and dissolved organic carbon (DOC) of Pa forest soil were 13.5%, 30.0% and 15.7% less than those in Ba soil. The seasonal average enzyme activities of β-1,4-glucosidase (βG), and β-1,4-xylosidase (βX) of Ba forest soils were 30.0% and 32.3% higher than those of Pa soil while the enzyme activity of cellobiohydrolase (CBH) was 19.7% lower. Furthermore, the relative abundance of Acidobacteria was significantly higher in summer than in winter, whereas the relative abundance of Bacteroidetes was higher in winter. Regarding the fungal communities, the relative abundance of Basidiomycota was lowest in winter, whereas Ascomycota predominated in the same season. In addition, the soil LOC was significantly positively correlated with the CBH, βG and βX activities. Changes in LOC were significantly correlated with Acidobacteria, Bacteroidetes and Basidiomycota. We conclude that the seasonal fluctuations in forest soil LOC fractions relied on carbon cycle-associated enzymatic activities and microorganisms, which in turn were affected by climatic conditions.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2023

Large-scale genomic analyses with machine learning uncover predictive patterns associated with fungal phytopathogenic lifestyles and traits

Abstract Invasive plant pathogenic fungi have a global impact, with devastating economic and environmental effects on crops and forests. Biosurveillance, a critical component of threat mitigation, requires risk prediction based on fungal lifestyles and traits. Recent studies have revealed distinct genomic patterns associated with specific groups of plant pathogenic fungi. We sought to establish whether these phytopathogenic genomic patterns hold across diverse taxonomic and ecological groups from the Ascomycota and Basidiomycota, and furthermore, if those patterns can be used in a predictive capacity for biosurveillance. Using a supervised machine learning approach that integrates phylogenetic and genomic data, we analyzed 387 fungal genomes to test a proof-of-concept for the use of genomic signatures in predicting fungal phytopathogenic lifestyles and traits during biosurveillance activities. Our machine learning feature sets were derived from genome annotation data of carbohydrate-active enzymes (CAZymes), peptidases, secondary metabolite clusters (SMCs), transporters, and transcription factors. We found that machine learning could successfully predict fungal lifestyles and traits across taxonomic groups, with the best predictive performance coming from feature sets comprising CAZyme, peptidase, and SMC data. While phylogeny was an important component in most predictions, the inclusion of genomic data improved prediction performance for every lifestyle and trait tested. Plant pathogenicity was one of the best-predicted traits, showing the promise of predictive genomics for biosurveillance applications. Furthermore, our machine learning approach revealed expansions in the number of genes from specific CAZyme and peptidase families in the genomes of plant pathogens compared to non-phytopathogenic genomes (saprotrophs, endo- and ectomycorrhizal fungi). Such genomic feature profiles give insight into the evolution of fungal phytopathogenicity and could be useful to predict the risks of unknown fungi in future biosurveillance activities.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Genomic and morphological characterization of Knufia obscura isolated from the Mars 2020 spacecraft assembly facility

Members of the family Trichomeriaceae, belonging to the Chaetothyriales order and the Ascomycota phylum, are known for their capability to inhabit hostile environments characterized by extreme temperatures, oligotrophic conditions, drought, or presence of toxic compounds. The genus Knufia encompasses many polyextremophilic species. In this report, the genomic and morphological features of the strain FJI-L2-BK-P2 presented, which was isolated from the Mars 2020 mission spacecraft assembly facility located at the Jet Propulsion Laboratory in Pasadena, California. The identification is based on sequence alignment for marker genes, multi-locus sequence analysis, and whole genome sequence phylogeny. The morphological features were studied using a diverse range of microscopic techniques (bright field, phase contrast, differential interference contrast and scanning electron microscopy). The phylogenetic marker genes of the strain FJI-L2-BK-P2 exhibited highest similarities with type strain of Knufia obscura (CBS 148926 T ) that was isolated from the gas tank of a car in Italy. To validate the species identity, whole genomes of both strains (FJI-L2-BK-P2 and CBS 148926 T ) were sequenced, annotated, and strain FJI-L2-BK-P2 was confirmed as K. obscura. The morphological analysis and description of the genomic characteristics of K. obscura FJI-L2-BK-P2 may contribute to refining the taxonomy of Knufia species. Key morphological features are reported in this K. obscura strain, resembling microsclerotia and chlamydospore-like propagules. These features known to be characteristic features in black fungi which could potentially facilitate their adaptation to harsh environments.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Phylogenetic and ecological drivers of the avian lung mycobiome and its potentially pathogenic component

Vertebrate lungs contain diverse microbial communities, but little is known about the drivers of community composition or consequences for health. Microbiome assembly by processes such as dispersal, coevolution, and host-switching can be probed with comparative surveys; however, few studies exist for lung microbiomes, particularly for the fungal component, the mycobiome. Distinguishing among fungal taxa that are generalist or specialist symbionts, potential pathogens, or incidentally inhaled spores is urgent because of potential for emerging diseases. Here, we characterize the avian lung mycobiome and test the relative influences of environment, phylogeny, and functional traits. We used metabarcoding and culturing from 195 lung samples representing 32 bird species across 20 families. We identified 526 fungal taxa as estimated by distinct sequence types (zOTUs) including many opportunistic pathogens. These were predominantly from the phylum Ascomycota (79%) followed by Basidiomycota (16%) and Mucoromycota (5%). Yeast and yeast-like taxa (Malassezia, Filobasidium, Saccharomyces, Meyerozyma, and Aureobasidium) and filamentous fungi (Cladosporium, Alternaria, Neurospora, Fusarium, and Aspergillus) were abundant. Lung mycobiomes were strongly shaped by environmental exposure, and further modulated by host identity, traits, and phylogenetic affinities. Our results implicate migratory bird species as potential vectors for long-distance dispersal of opportunistically pathogenic fungi.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Genomics discovery of giant fungal viruses from subsurface oceanic crustal fluids

Abstract The oceanic igneous crust is a vast reservoir for microbial life, dominated by diverse and active bacteria, archaea, and fungi. Archaeal and bacterial viruses were previously detected in oceanic crustal fluids at the Juan de Fuca Ridge (JdFR). Here we report the discovery of two eukaryotic Nucleocytoviricota genomes from the same crustal fluids by sorting and sequencing single virions. Both genomes have a tRNATyr gene with an intron (20 bps) at the canonical position between nucleotide 37 and 38, a common feature in eukaryotic and archaeal tRNA genes with short introns (<100 bps), and fungal genes acquired through horizontal gene transfer (HGT) events. The dominance of Ascomycota fungi as the main eukaryotes in crustal fluids and the evidence for HGT point to these fungi as the putative hosts, making these the first putative fungi-Nucleocytoviricota specific association. Our study suggests active host-viral dynamics for the only eukaryotic group found in the subsurface oceanic crust and raises important questions about the impact of viral infection on the productivity and biogeochemical cycling in this ecosystem.

Bhattacharjee, Ananda S.↗