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Spatafora, J. W.

Publications and source records attributed to Spatafora, J. W..

10 recordsLinked to original sources

Prediction of Lignocellulose Degradation Potential of Wood Decay Fungi using Comparative Genomic Analysis

The Agaricomycotina accounts for roughly a third of all described fungi. They are important due to their wide range of lifestyles and economic and environmental relevance. Certain agaricomycetes act as lignocellulose degraders, playing a significant role in forest ecosystems and bioremediation processes. These wood-decaying fungi have historically been classified as mostly white- or brown-rot based on their ability to degrade lignin, with white-rot fungi possessing a collection of lignocellulose-degrading enzymes, which are reduced or absent in brown-rot fungi. Here, we sequenced and annotated the genome of the agaricomycete Crepidotus cesatii CBS 511.95 and explored its genome and predicted enzymatic content in a comparative context. The 36.04 Mbp genome is in 235 scaffolds, with 3.34% repeat content and 12,891 predicted genes. We found that the PFAM distributions of identified orthogroups suggested that C. cesatii shows patterns more similar to white-rot fungi compared to brown-rot fungi. Additionally, C. cesatii contained multiple copies of CAZymes CBM1 and AA9 involved in hydrolysis of lignocellulose, similar to white-rot fungi. On the other hand, according to the Conserved Unique Peptide Patterns (CUPP) data for AA2 peroxidases, the key enzymes in lignin degradation, C. cesatii is more similar to brown-rot fungi. Based on our analyses we predict that C. cesatii is another representation of the continuum of wood decaying modes between white and brown rot fungi combining genetic features of both types of fungi.

genetics↗

Absolute abundance unveils Basidiobolus as a cross-domain bridge indirectly bolstering gut microbiome homeostasis

The host microbiome is integral to metabolism, immune function, and resilience against pathogens. However, reliance on relative abundance (RA) to estimate host-associated microbiomes introduces compositional biases, while limited tools for absolute abundance (AA) quantification hinder broader applications. To address these challenges, we developed DspikeIn (https://github.com/mghotbi/DspikeIn), an R package paired with a versatile wet-lab methodology for AA quantification. Using RA and AA to compare core microbiome distributions across herpetofauna orders and their natural histories revealed starkly distinct results, driven by aggregate effects, including inherited compositional biases in RA and additional multifactorial influences. Focusing on two closely related Desmognathus species demonstrated that AA quantification enhanced resolution in differential abundance analyses and minimized false discovery rates (FDR) when identifying enriched taxa in their gut microbiomes. Keystone taxa identified through network associations also differed between RA and AA data. For example, Lactococcus and Cetobacterium were core members in Anura and Caudata, while Basidiobolus and Mortierella were core to Chelonia and Squamata, facilitating host adaptation to diverse environments, insights undetectable with RA data. AA-based network analysis further revealed that removing the Basidiobolus subnetwork increased negative interactions, highlighting its role in promoting gut homeostasis through cross-domain connectivity. Despite low redundancy, the Basidiobolus node exhibited high betweenness, efficiency, and degree, serving as a critical bridge linking disconnected nodes or modules and indirectly supporting microbiome stability, consistent with Burts structural hole theory. DspikeIn represents a transformative tool for microbiome research, enabling the transition from RA to AA quantification and delivering more accurate, consistent, and comparable results across studies. Graphical abstract DspikeIn cheatsheet O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=156 SRC="FIGDIR/small/630554v1_ufig1.gif" ALT="Figure 1"> View larger version (65K): org.highwire.dtl.DTLVardef@150900forg.highwire.dtl.DTLVardef@21cd90org.highwire.dtl.DTLVardef@13ead1borg.highwire.dtl.DTLVardef@1d6fa84_HPS_FORMAT_FIGEXP M_FIG C_FIG

microbiology↗

Herptile gut microbiomes: a natural system to study multi-kingdom interactions between filamentous fungi and bacteria

Reptiles and amphibians (herptiles) represent some of the more endangered and threatened species on the planet and numerous conservation strategies are being implemented with the goal of ensuring species recovery. Little is known, however, about the wild gut microbiome of herptiles and how it relates to the health of wild populations. Here we report results from both a broad survey of hosts and a more intensive sampling of hosts and geography of fungi and bacteria associated with herptile gut microbiomes. We demonstrate that bacterial communities sampled from frogs, lizards and salamanders are structured by the host higher level taxonomy and that the fungus Basidiobolus is a common and natural component of these wild gut microbiomes. Intensive sampling of multiple hosts across the ecoregions of Tennessee revealed that geography and host:geography interactions are strong predictors of distinct Basidiobolus OTUs present within a given host. Co-occurrence analyses of Basidiobolus and bacterial community diversity supports a correlation and interaction between Basidiobolus and bacteria, suggesting that Basidiobolus may play a role in structuring the bacterial community. We further the hypothesis that this interaction is advanced by unique specialized metabolism originating from horizontal gene transfer from bacteria to Basidiobolus, and demonstrate that Basidiobolus is capable of producing a diversity of specialized metabolites including small cyclic peptides. IMPORTANCEThis work significantly advances our understanding of interactions in herptile microbiomes; the role that fungi play as a structural and functional member of herptile gut microbiomes; and the chemical functions that structure host:microbiome phenotypes. We also provide an important observational system of how the gut microbiome represents a unique environment that selects for novel metabolic functions through horizontal gene transfer between fungi and bacteria. Such studies are needed to better understand the complexity of gut microbiomes in nature and will inform conservation strategies for threatened species of herpetofauna.

ecology↗

Taxonomic vs genomic fungi: contrasting evolutionary loss of protistan genomic heritage and emergence of fungal novelties

Fungi are among the most ecologically important heterotrophs that have radiated into most niches on Earth and fulfil key ecological services. However, despite intense interest in their origins, major genomic trends characterising the evolutionary route from a unicellular opisthokont ancestor to derived multicellular fungi remain poorly known. Here, we reconstructed gene family evolution across 123 genomes of fungi and relatives and show that a dominant trend in early fungal evolution has been the gradual shedding of protist genes and highly episodic innovation via gene duplication. We find that the gene content of early-diverging fungi is protist-like in many respects, owing to the conservation of protist genes in early fungi. While gene loss has been constant and gradual during early fungal evolution, our reconstructions show that gene innovation showed two peaks. Gene groups with the largest contribution to genomic change included extracellular proteins, transcription factors, as well as ones linked to the coordination of nutrient uptake with growth, highlighting the transition to a sessile osmotrophic feeding strategy and subsequent lifestyle evolution as important elements of early fungal evolution. Taken together, this work provided a highly resolved genome-wide catalogue of gene family changes across fungal evolution. This suggests that the genome of pre-fungal ancestors may have been transformed into the archetypal fungal genome by a combination of gradual gene loss, turnover and two large duplication events rather than by abrupt changes, and consequently, that the taxonomically defined fungal kingdom does not represent a genomically uniform assemblage of extant species characterized by diagnostic synapomorphies.

evolutionary biology↗

Divergent evolution of early terrestrial fungi reveals the evolution of Mucormycosis pathogenicity factors

Fungi have evolved over millions of years and their species diversity is predicted to be the second largest on the earth. Fungi have cross-kingdom interactions with many organisms which have mutually shaped their evolutionary trajectories. Zygomycete fungi hold a pivotal position in the fungal tree of life and provide important perspectives on the early evolution of fungi from aquatic to terrestrial environments. Phylogenomic analyses have found that zygomycete fungi diversified into two separate clades, the Mucoromycota which are frequently associated with plants and Zoopagomycota that are commonly animal-associated fungi. Genetic elements that contributed to the fitness and divergence of these lineages may have been shaped by the varied interactions these fungi have had with plants, animals, bacteria and other microbes. To investigate this, we performed comparative genomic analyses of the two clades in the context of Kingdom Fungi, benefiting from our generation of a new collection of zygomycete genomes. We identified lineage-specific genomic content which may contribute to the disparate biology observed in these zygomycetes. Our findings include the discovery of undescribed diversity in CotH, a Mucormycosis pathogenicity factor, which was found in a broad set of zygomycetes. Reconciliation analysis identified multiple duplication events and an expansion of CotH copies throughout Mucoromycotina, Mortierellomycotina, Neocallimastigomycota, and Basidiobolus lineages. A kingdom-level phylogenomic analysis also identified new evolutionary relationships within the sub-phyla of Mucoromycota and Zoopagomycota.

evolutionary biology↗

Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales

O_LIIn this study, we aim to identify genomic traits of the transitions to the ectomycorrhizal ecology within the Boletales, one of the most diverse lineages of symbiotrophic fungi. C_LIO_LIWe sequenced the genomes and compared the gene repertoires of symbiotrophic Boletales species to their saprotrophic brown-rot relatives. We also reconstructed gene duplication/loss histories along a time-calibrated phylogeny. C_LIO_LIWe showed that the rate of gene duplication is constant along the backbone of Boletales phylogeny with large loss events in lineages leading to several families. The rate of gene family expansion sharply increased in the late Miocene and mostly took place in Boletaceae. C_LIO_LIMost of the ectomycorrhizal Boletales are characterized by a large genome size due to transposable element (TE) expansions and a reduction in the diversity of plant cell wall degrading enzymes (PCWDEs) compared to their brown-rot relatives. However, several species in the Boletaceae, Paxillaceae and Boletinellaceae have kept a substantial set of endoglucanases and LPMOs acting on cellulose/hemicellulose and fungal polysaccharides suggesting that they may partly decompose organic matter by a combined activity of oxidative and hydrolytic enzymes. C_LIO_LIThe present study provides novel insights on our understanding of the mechanisms that influence the evolutionary diversification of boletes and symbiosis evolution. C_LI

genomics↗

Genome-scale phylogenetic analyses confirm Olpidium as the closest living zoosporic fungus to the non-flagellated, terrestrial fungi

The zoosporic obligate endoparasites, Olpidium, hold a pivotal position to the reconstruction of the flagellum loss in fungi, one of the key morphological transitions associated with the colonization of land by the early fungi. We generated genome and transcriptome data from non-axenic zoospores of Olpidium bornovanus and used a metagenome approach to extract phylogenetically informative fungal markers. Our phylogenetic reconstruction strongly supported Olpidium as the closest zoosporic relative of the non-flagellated terrestrial fungi. Super-alignment analyses resolved Olpidium as sister to the non-flagellated terrestrial fungi, whereas a super-tree approach recovered different placements of Olpidium, but without strong support. Further investigations detected little conflicting signal among the sampled markers but revealed a potential polytomy in early fungal evolution associated with the branching order among Olpidium, Zoopagomycota and Mucoromycota. The branches defining the evolutionary relationships of these lineages were characterized by short branch lengths and low phylogenetic content and received equivocal support for alternative phylogenetic hypotheses from individual markers. These nodes were marked by important morphological innovations, including the transition to hyphal growth and the loss of flagellum, which enabled early fungi to explore new niches and resulted in rapid and temporally concurrent Precambrian diversifications of the ancestors of several phyla of fungi.

evolutionary biology↗

A genome-scale phylogeny of Fungi; insights into early evolution, radiations, and the relationship between taxonomy and phylogeny

Phylogenomic studies based on genome-scale amounts of data have greatly improved understanding of the tree of life. Despite their diversity, ecological significance, and biomedical and industrial importance, large-scale phylogenomic studies of Fungi are lacking. Furthermore, several evolutionary relationships among major fungal lineages remain controversial, especially those at the base of the fungal phylogeny. To begin filling these gaps and assess progress toward a genome-scale phylogeny of the entire fungal kingdom, we compiled a phylogenomic data matrix of 290 genes from the genomes of 1,644 fungal species that includes representatives from most major fungal lineages; we also compiled 11 additional data matrices by subsampling genes or taxa based on filtering criteria previously shown to improve phylogenomic inference. Analyses of these 12 data matrices using concatenation- and coalescent-based approaches yielded a robust phylogeny of the kingdom in which [~]85% of internal branches were congruent across data matrices and approaches used. We found support for several relationships that have been historically contentious (e.g., for the placement of Wallemiomycotina (Basidiomycota), as sister to Agaricomycotina), as well as evidence for polytomies likely stemming from episodes of ancient diversification (e.g., at the base of Basidiomycota). By examining the relative evolutionary divergence of taxonomic groups of equivalent rank, we found that fungal taxonomy is broadly aligned with genome sequence divergence, but also identified lineages, such as the subphylum Saccharomycotina, where current taxonomic circumscription does not fully account for their high levels of evolutionary divergence. Our results provide a robust phylogenomic framework to explore the tempo and mode of fungal evolution and directions for future fungal phylogenetic and taxonomic studies.

evolutionary biology↗

Phylogenomic analyses of non-Dikarya fungi supports horizontal gene transfer driving diversification of secondary metabolism in the amphibian gastrointestinal symbiont, Basidiobolus

Research into secondary metabolism (SM) production by fungi has resulted in the discovery of diverse, biologically active compounds with significant medicinal applications. However, the fungi rich in SM production are taxonomically restricted to Dikarya, two phyla of Kingdom Fungi, Ascomycota and Basidiomycota. Here, we explore the potential for SM production in Mucoromycota and Zoopagomycota, two phyla of nonflagellated fungi that are not members of Dikarya, by predicting and identifying core genes and gene clusters involved in SM. The majority of non-Dikarya have few genes and gene clusters involved in SM production except for the amphibian gut symbionts in the genus Basidiobolus. Basidiobolus genomes exhibit an enrichment of SM genes involved in siderophore, surfactin-like, and terpene cyclase production, all these with evidence of constitutive gene expression. Gene expression and chemical assays confirm that Basidiobolus has significant siderophore activity. The expansion of SMs in Basidiobolus are partially due to horizontal gene transfer from bacteria, likely as a consequence of its ecology as an amphibian gut endosymbiont.

genomics↗

The architecture of metabolism maximizes biosynthetic diversity in the largest class of fungi

AbstractO_ST_ABSBackgroundC_ST_ABSEcological diversity in fungi is largely defined by metabolic traits, including the ability to produce secondary or "specialized" metabolites (SMs) that mediate interactions with other organisms. Fungal SM pathways are frequently encoded in biosynthetic gene clusters (BGCs), which facilitate the identification and characterization of metabolic pathways. Variation in BGC composition reflects the diversity of their SM products. Recent studies have documented surprising diversity of BGC repertoires among isolates of the same fungal species, yet little is known about how this population-level variation is inherited across macroevolutionary timescales. ResultsHere, we applied a novel linkage-based algorithm to reveal previously unexplored dimensions of diversity in BGC composition, distribution, and repertoire across 101 species of Dothideomycetes, which are considered to be the most phylogenetically diverse class of fungi and are known to produce many SMs. We predicted both complementary and overlapping sets of clustered genes compared with existing methods and identified novel gene pairs that associate with known secondary metabolite genes. We found that variation in BGC repertoires is due to non-overlapping BGC combinations and that several BGCs have biased ecological distributions, consistent with niche-specific selection. We observed that total BGC diversity scales linearly with increasing repertoire size, suggesting that secondary metabolites have little structural redundancy in individual fungi. ConclusionsWe project that there is substantial unsampled BGC diversity across specific families of Dothideomycetes, which will provide a roadmap for future sampling efforts. Our approach and findings lend new insight into how BGC diversity is generated and maintained across an entire fungal taxonomic class.

genomics↗