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LaButti, K.

Publications and source records attributed to LaButti, K..

18 recordsLinked to original sources

Fungal microbial enrichment method enables fungal metagenomics directly from human clinical samples

Fungi play important roles in health and disease, but current methods such as culture, PCR, and amplicon sequencing cannot provide genome-level characterization directly from clinical samples. Although metagenomic sequencing could overcome these limitations, it remains impractical in clinical samples where fungal DNA is present at low abundance relative to human DNA. Here, we extend a recently described microbial enrichment method (MEM)(1) to fungi (fungal Microbial Enrichment Method; fMEM) and test the method in bronchoalveolar lavage (BAL) samples to demonstrate direct-from-sample fungal metagenomic analysis and metagenome-assembled genome (MAG) recovery. In BAL samples, fMEM depleted human DNA by more than 1000-fold while preserving fungal DNA within 10-fold, enabling shotgun sequencing from samples with fungal biomass as low as 10 pg fungal DNA per 200 {micro}L BAL. fMEM enabled de novo recovery of fungal MAGs from three of four sequenced BAL samples, including two near-complete MAGs (>90% BUSCO completeness) and one 82.1% complete MAG, with low BUSCO-estimated contamination ([≤]1.5%). Fungal MAGs recovered by fMEM also resolved potentially clinically-relevant genes, not fully predictable from taxonomy alone and revealed genomic content absent from currently-available same-species reference genomes. fMEM is compatible with a whole-genome amplification (including long-read sequencing workflows). Long reads from fMEM-processed samples provided high coverage (>10X) over fungal assemblies. fMEMs compatibility with long-read sequencing enables recovery of genes that would be difficult to assemble with short reads alone. fMEM may enable new insights into the role of human-associated fungi, impacting public health, clinical management, and research into complex diseases with suspected fungal roles. ImportanceFungi influence human health, infectious disease, and the microbiome, but direct genome analysis from clinical samples has remained impractical because fungal DNA is often overwhelmed by human DNA. We developed a fungal microbial enrichment method (fMEM) that enables direct-from-sample fungal metagenomic sequencing and genome recovery from bronchoalveolar lavage samples without requiring culture for genome assembly. fMEM recovers genome-level features not predicted by taxonomy or current same-species reference genomes and is compatible with long-read sequencing workflows that can recover loci missed by short-read sequencing. fMEM opens new opportunities for culture-independent fungal genomics, clinical microbiology, comparative genomics, and mechanistic studies of human-associated fungi.

bioengineering↗

Comparative genomics reveals shared accessory regions between members of two Fusarium species complexes virulent on garden pea

The contribution of accessory or conditionally dispensable chromosomes to host-specific virulence was first demonstrated in members of the Fusarium solani species complex (FSSC) that are pathogens of garden pea, Pisum sativum L. The phenomenon has since been shown to exist in many fungal plant pathogens, including the closely related F. oxysporum species complex (FOSC). Genome analysis of members of the FSSC and FOSC pathogenic on pea revealed a diverse size range of the accessory genome of these fungi. Despite the [~]65 million years of diverging time, regions on a chromosome known to carry host-specific virulence factors for pea, including the cytochrome P450 pisatin demethylase (PDA) and other pea pathogenicity (PEP) genes, were present in all genomes of these pea pathogens. Genes directly involved in virulence on pea - PEP2, PDA, and PEP5- were the most frequently clustered together. Transcriptome analysis of fungal mycelia treated with the pea phytoalexin pisatin, identified 1,155 differentially expressed genes where many were involved in cellular stress responses. As wilt pathogens that invade host xylem, members of the FOSC encode more putative effectors, when compared to those in the FSSC, and several FOSC effectors were identified to confer race specificity. The conservation of part of the accessory genomes across two evolutionarily diverged species complexes suggests a common origin. Horizontal transfer of accessory chromosomes containing genetic loci involved in pathogenesis for garden pea offers a parsimonious explanation of the polyphyletic origin of host specificity.

genomics↗

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↗

Evidence for the acquisition of a proteorhodopsin-like rhodopsin by a chrysophyte-infecting giant virus

Chrysophytes are nanoflagellate protists widespread in aquatic ecosystems with diverse trophic roles as primary producers and bacterivores. Molecular evidence suggests that chrysophytes are commonly infected by giant viruses but isolates of such virus-host systems have not been reported. Here, we describe the first cultivated chrysophyte-infecting virus, Chrysophyceae Clade H virus SA1 (ChrysoHV), isolated along with its phago-mixotrophic host alga from surface waters in the tropical North Pacific Ocean. The ChrysoHV capsid (290 {+/-} 40 nm diameter) is associated with a loose, sac-like membrane that extends its effective diameter (720 {+/-} 120 nm) and presents a long (1,200 {+/-} 240 nm), thin (20 {+/-} 2), flexible tail, a morphology unlike any virion yet described. The assembled genome is 1.19 Mbp. Phylogenetic analysis places ChrysoHV as the third cultivated member of the Aliimimivirinae subfamily in the Mimiviridae family of giant viruses. The ChrysoHV genome encodes two heliorhodopsins and one proteorhodopsin. Proteorhodopsins are well known light-driven proton pumps in bacteria but have not been previously reported in a viral genome. The predicted viral proteorhodopsin structure suggests it may not have a functional retinal binding site implying a light-independent function. The genome also encodes two ribosomal proteins and nine genes with closest known homologs in marine cyanobacteria, most annotated as encoding for proteins involved in nutrient uptake. This unusual virus could serve as a model system for exploring viral rhodopsin functions and its genome suggests that phagotrophic protists may serve as an intracellular market for gene exchange between infecting viruses and ingested bacterial prey. ImportanceChrysophytes are abundant eukaryotic phytoplankton with trophic strategies ranging from photosynthesis to phagotrophy. They serve as models of mixotrophy among aquatic protists, but no chrysophyte-infecting viruses had been isolated, leaving a gap in experimental virus-host systems for a major class of protists. This study reports on the characterization of the first isolated chrysophyte-infecting virus, ChrysoHV. The virion morphology is unusual, having a loose membranous sac around a large capsid and a long filamentous tail. The genome contains genes for ribosomal proteins, a rarity in eukaryotic viruses, and multiple genes with homologs in common marine bacteria, one of which is a type of rhodopsin never before reported in a virus. We hypothesize that phago-mixotrophs, through infections and ingestion, may facilitate lateral gene exchange between eukaryote-infecting viruses and bacteria, entities that might not otherwise directly interact. The results expand the observed morphological diversity among viruses and the catalog of known virus genes.

microbiology↗

Genomic and Transcriptomic Characterization of Carbohydrate-Active Enzymes in the Anaerobic Fungus Neocallimastix cameroonii var. constans

Anaerobic gut fungi effectively degrade lignocellulose in the guts of large herbivores, but there remains a limited number of isolated, publicly available, and sequenced strains that impede our understanding of the role of anaerobic fungi within microbial communities. We isolated and characterized a new fungal isolate, Neocallimastix cameroonii var. constans, providing a transcriptomic and genomic understanding of its ability to degrade diverse carbohydrates. This anaerobic fungal strain was stably cultivated for multiple years in vitro among members of an initial enrichment microbial community derived from goat feces, and it demonstrated the ability to pair with other microbial members, namely archaeal methanogens to produce methane from lignocellulose. Genomic analysis revealed a higher number of predicted carbohydrate-active enzymes encoded in the N. cameroonii var. constans genome compared to most other sequenced anaerobic fungi. The carbohydrate-active enzyme profile for this isolate contained 660 glycoside hydrolases, 160 carbohydrate esterases, 194 glycosyltrasferases, and 85 polysaccharide lyases. Differential gene expression analysis showed the upregulation of thousands of genes (including predicted carbohydrate-active enzymes) when N. cameroonii var. constans was grown on lignocellulose (reed canary grass) compared to less complex substrates, such as cellulose (filter paper), cellobiose, and glucose. AlphaFold was used to predict functions of transcriptionally active yet poorly annotated genes, revealing feruloyl esterases that likely play an important role in lignocellulose degradation by anaerobic fungi. The combination of this strains genomic and transcriptomic characterization, omics-informed structural prediction, and robustness in microbial co-culture make it a well-suited platform to conduct future investigations into bioprocessing and enzyme discovery.

microbiology↗

Comparative genomics of the extremophile Cryomyces antarcticus and other psychrophilic Dothideomycetes

Cryomyces antarcticus is an endolithic fungus that inhabits rock outcrops in Antarctica. It survives extremes of cold, humidity and solar radiation in one of the least habitable environments on Earth. This fungus is unusual because it produces heavily melanized, meristematic growth and is thought to be haploid and asexual. Due to its growth in the most extreme environment, it has been suggested as an organism that could survive on Mars. However, the mechanisms it uses to achieve its extremophilic nature are not known. Over a billion years of fungal evolution has enabled representatives of this kingdom to populate almost all parts of planet Earth and to adapt to some of its most uninhabitable environments including extremes of temperature, salinity, pH, water, light, or other sources of radiation. Comparative genomics can provide clues to the processes underlying biological diversity, evolution, and adaptation. This effort has been greatly facilitated by the 1000 Fungal Genomes project and the JGI MycoCosm portal where sequenced genomes have been assembled into phylogenetic and ecological groups representing different projects, lifestyles, ecologies, and evolutionary histories. Comparative genomics within and between these groups provides insights into fungal adaptations, for example to extreme environmental conditions. Here, we analyze two Cryomyces genomes in the context of additional psychrophilic fungi, as well as non-psychrophilic fungi with diverse lifestyles selected from the MycoCosm database. This analysis identifies families of genes that are expanded and contracted in Cryomyces and other psychrophiles and may explain their extremophilic lifestyle. Higher GC contents of genes and of bases in the third positions of codons may help to stabilize DNA under extreme conditions. Numerous smaller contigs in C. antarcticus suggest the presence of an alternative haplotype that could indicate that the sequenced isolate is diploid or dikaryotic. These analyses provide a first step to unraveling the secrets of the extreme lifestyle of C. antarcticus.

genomics↗

High phenotypic and genotypic plasticity among strains of the mushroom-forming fungus Schizophyllum commune

Schizophyllum commune is a mushroom-forming fungus notable for its distinctive fruiting bodies with split gills. It is used as a model organism to study mushroom development, lignocellulose degradation and mating type loci. It is a hypervariable species with considerable genetic and phenotypic diversity between the strains. In this study, we systematically phenotyped 16 dikaryotic strains for aspects of mushroom development and 18 monokaryotic strains for lignocellulose degradation. There was considerable heterogeneity among the strains regarding these phenotypes. The majority of the strains developed mushrooms with varying morphologies, although some strains only grew vegetatively under the tested conditions. Growth on various carbon sources showed strain-specific profiles. The genomes of seven monokaryotic strains were sequenced and analyzed together with six previously published genome sequences. Moreover, the related species Schizophyllum fasciatum was sequenced. Although there was considerable genetic variation between the genome assemblies, the genes related to mushroom formation and lignocellulose degradation were well conserved. These sequenced genomes will provide a solid basis for functional genomics analyses of the strains of S. commune.

microbiology↗

Genomic innovation and horizontal gene transfer shaped plant colonization and biomass degradation strategies of a globally prevalent fungal pathogen

Members of the fungal genus Armillaria are necrotrophic pathogens with efficient plant biomass-degrading strategies. The genus includes some of the largest terrestrial organisms on Earth, spreading underground and causing tremendous losses in diverse ecosystems. Despite their global importance, the mechanism by which Armillaria evolved pathogenicity in a clade of dominantly non-pathogenic wood-degraders (Agaricales) remains elusive. Here, using new genomic data, we show that Armillaria species, in addition to widespread gene duplications and de novo gene origins, appear to have at least 775 genes that were acquired via 101 horizontal gene transfer (HGT) events, primarily from Ascomycota. Functional and expression data suggest that HGT might have affected plant biomass-degrading and virulence abilities of Armillaria, two pivotal traits in their lifestyle. We further assayed gene expression during root and cambium colonization, and report putative virulence factors, extensive regulation of horizontally acquired and wood-decay related genes as well as novel pathogenicity-induced small secreted proteins (PiSSPs). Two PiSSPs induced necrosis in live plants, suggesting they are potential virulence effectors conserved across Armillaria. Overall, this study details how evolution knitted together horizontally and vertically inherited genes in complex adaptive traits, such as plant biomass degradation and pathogenicity, paving the way for development of infection models for one of the most influential pathogens of temperate forest ecosystems.

genomics↗

Genome evolution and transcriptome plasticity associated with adaptation to monocot and eudicot plants in Colletotrichum fungi

Colletotrichum fungi infect a wide diversity of monocot and eudicot hosts, causing plant diseases on almost all economically important crops worldwide. In addition to its economic impact, Colletotrichum is a suitable model for the study of gene family evolution on a fine scale to uncover events in the genome that are associated with the evolution of biological characters important for host interactions. Here we present the genome sequences of 30 Colletotrichum species, 18 of them newly sequenced, covering the taxonomic diversity within the genus. A time-calibrated tree revealed that the Colletotrichum ancestor diverged in the late Cretaceous around 70 million years ago (mya) in parallel with the diversification of flowering plants. We provide evidence of independent host jumps from eudicots to monocots during the evolution of this pathogen, coinciding with a progressive shrinking of the degradative arsenal and expansions in lineage specific genes. Comparative transcriptomics of four reference species with different evolutionary histories and adapted to different hosts revealed similarity in gene content but differences in the modulation of their transcription profiles. Only a few orthologs show similar expression profiles on different plant cell walls. Combining genome sequences and expression profiles we identified a set of core genes, such as specific transcription factors, involved in plant cell wall degradation in Colletotrichum.Together, these results indicate that the ancestral Colletotrichum were associated with eudicot plants and certain branches progressively adapted to different monocot hosts, reshaping part of the degradative and transcriptional arsenal.

microbiology↗

SPRAY-INDUCED GENE SILENCING IDENTIFIES PATHOGEN PROCESSES CONTRIBUTING TO POWDERY MILDEW PROLIFERATION

Spray-induced gene silencing (SIGS) is an emerging tool for crop pest protection. It utilizes exogenously applied double stranded RNA to specifically reduce pest target gene expression using endogenous RNA interference machinery. Powdery mildews, widespread obligate biotrophic fungi infect agricultural crops including wheat, barley, cucurbits, grapevine, and ornamentals such as roses. In this study, SIGS methods were developed and optimized for powdery mildews using the known azole-fungicide target CYP51 and the Golovinomyces orontii-Arabidopsis thaliana pathosystem. Additional screening resulted in the identification of conserved gene targets and processes important to powdery mildew proliferation: apoptosis-antagonizing transcription factor in essential cellular metabolism and stress response; lipase a, lipase 1, and acetyl-CoA oxidase in lipid catabolism; 9-cis-epoxycarotenoid dioxygenase, xanthoxin dehydrogenase, and a putative abscisic acid G-protein coupled receptor predicted to function in manipulation of the plant hormone abscisic acid; and the secreted effector EC2. Powdery mildew is the dominant disease impacting grapes and extensive powdery mildew resistance to applied fungicides has been reported. Therefore, we developed SIGS for the Erysiphe necator-Vitis vinifera system and tested six successful targets identified using the G. orontii-A. thaliana system. For all targets tested, a similar reduction in powdery mildew disease was observed between systems. This indicates screening of broadly conserved targets in the G. orontii-A. thaliana pathosystem identifies targets and processes for the successful control of other powdery mildews. The flexibility, specificity, reduced environmental and health risks, and rapid transition from the bench to the field make SIGS an exciting prospect for commercial powdery mildew control.

microbiology↗

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↗

The soybean rust pathogen Phakopsora pachyrhizi displays transposable element proliferation that correlates with broad host-range adaptation on legumes

Asian soybean rust, caused by Phakopsora pachyrhizi, is one of the worlds most economically damaging agricultural diseases. Despite P. pachyrhizis impact, the exceptional size and complexity of its genome prevented generation of an accurate genome assembly. We simultaneously sequenced three P. pachyrhizi genomes uncovering a genome up to 1.25 Gb comprising two haplotypes with a transposable element (TE) content of ~93%. The proliferation of TEs within the genome occurred in several bursts and correlates with the radiation and speciation of the legumes. We present data of clear de-repression of TEs that mirrors expression of virulence-related candidate effectors. We can see a unique expansion in amino acid metabolism for this fungus. Our data shows that TEs play a dominant role in P. pachyrhizis genome and have a key impact on various processes such as host range adaptation, stress responses and genetic plasticity of the genome.

microbiology↗

Enemy or ally: a genomic approach to elucidate the lifestyle of Phyllosticta citrichinaensis

Members of the fungal genus Phyllosticta can colonize a variety of plant hosts, including several Citrus species such as Citrus sinensis (orange), Citrus limon (lemon), and Citrus maxima (pomelo). Some Phyllosticta species have the capacity to cause disease, such as Citrus Black Spot, while others have only been observed as endophytes. Thus far, genomic differences underlying lifestyle adaptations of Phyllosticta species have not yet been studied. Furthermore, the lifestyle of Phyllosticta citrichinaensis is ambiguous, as it has been described as a weak pathogen but Kochs postulates may not have been established and the presence of this species was never reported to cause any crop or economic losses. Here, we examined the genomic differences between pathogenic and endophytic Phyllosticta spp. colonizing Citrus and specifically aimed to elucidate the lifestyle of Phyllosticta citrichinaensis. We found several genomic differences between species of different lifestyles, including groups of genes that were only present in pathogens or endophytes. We also observed that species, based on their carbohydrate active enzymes, group independent of their phylogenetic association, and this clustering correlated with trophy prediction. Phyllosticta citrichinaensis shows an intermediate lifestyle, sharing genomic and phenotypic attributes of both pathogens and endophytes. We thus present the first genomic comparison of multiple citrus-colonizing pathogens and endophytes of the genus Phyllosticta, and therefore provide the basis for further comparative studies into the lifestyle adaptations within this genus.

bioinformatics↗

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↗

Secondary metabolism drives ecological breadth in the Xylariaceae

Global, large-scale surveys of phylogenetically diverse plant and lichen hosts have revealed an extremely high richness of endophytes in the Xylariales, one of the largest clades of filamentous fungi and a significant source of novel secondary metabolites (SMs). Endophytes may produce host protective antimicrobial or insecticidal SMs, as well as compounds that facilitate symbiotic establishment through suppression or degradation of host immune response, but the ecological roles of most SMs are unknown. Here we characterized metabolic gene clusters in 96 genomes of endophytes and closely related saprotrophs and pathogens in two clades of Xylariales (Xylariaceae s.l. and Hypoxylaceae). Hundreds of genes appear horizontally transferred to xylarialean fungi from distantly related fungi and bacteria, including numerous genes in secondary metabolite gene clusters (SMGCs). Although all xylarialean genomes contain hyperabundant SMGCs, we show that increased gene duplications, horizontal gene transfers (HGTs), and SMGC content in Xylariaceae s.l. taxa are linked to greater phylogenetic host breadth, larger biogeographic distributions, and increased capacity for lignocellulose decomposition compared to Hypoxylaceae taxa. Overall, our results suggest that xylarialean endophytes capable of dual ecological modes (symbiotic and saprotrophic) experience greater selection to diversify SMGCs to both increase competitiveness within microbial communities and facilitate diverse symbiotic interactions.

genomics↗

Genetic determinants of endophytism in the Arabidopsis root mycobiome

Roots of Arabidopsis thaliana do not engage in symbiotic associations with mycorrhizal fungi but host taxonomically diverse fungal communities that influence health and disease states. We sequenced the genomes of 41 fungal isolates representative of the A. thaliana root mycobiota for comparative analysis with 79 other plant-associated fungi. We report that root mycobiota members evolved from ancestors with diverse lifestyles and retained large repertoires of plant cell wall-degrading enzymes (PCWDEs) and effector-like small secreted proteins. We identified a set of 84 gene families predicting best endophytism, including families encoding PCWDEs acting on xylan (GH10) and cellulose (AA9). These genes also belong to a core transcriptional response induced by phylogenetically-distant mycobiota members in A. thaliana roots. Recolonization experiments with individual fungi indicated that strains with detrimental effects in mono-association with the host not only colonize roots more aggressively than those with beneficial activities but also dominate in natural root samples. We identified and validated the pectin degrading enzyme family PL1_7 as a key component linking aggressiveness of endophytic colonization to plant health.

microbiology↗

Evolutionary priming and transition to the ectomycorrhizal habit in an iconic lineage of mushroom-forming fungi: is preadaptation a requirement?

The ectomycorrhizal symbiosis is an essential guild of many forested ecosystems and has a dynamic evolutionary history across kingdom Fungi, having independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic features of the transition to the ectomycorrhizal habit within the Russulaceae, one of the most diverse lineages of ectomycorrhizal fungi. We present comparative analyses of the pangenome and gene repertoires of 21 species across the order Russulales, including a closely related saprotrophic member of Russulaceae. The ectomycorrhizal Russulaceae is inferred to have originated around the Cretaceous-Paleogene extinction event (73.6-60.1 million years ago (MY)). The genomes of the ectomycorrhizal Russulaceae are characterized by a loss of genes for plant cell-wall degrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of genes coding for certain secreted proteins with TE "nests". The saprotrophic sister group of the ectomycorrhizal Russulaceae, Gloeopeniophorella convolvens, possesses some of these aspects (e.g., loss of some PCWDE and protease orthologs, TE expansion, reduction in secondary metabolism clusters), resulting from an accelerated rate of gene evolution in the shared ancestor of Russulaceae that predates the evolution of the ectomycorrhizal habit. Genomes of Russulaceae possess a high degree of synteny, including a conserved set of terpene secondary metabolite gene clusters. We hypothesize that the evolution of the ectomycorrhizal habit requires premodification of the genome for plant root association followed by an accelerated rate of gene evolution within the secretome for host-defense circumvention and symbiosis establishment.

evolutionary biology↗

The genome of Auriculariopsis ampla sheds light on fruiting body development and wood-decay of bark-inhabiting fungi

The Agaricomycetes are fruiting body forming fungi that produce some of the most efficient enzyme systems to degrade woody plant materials. Despite decades-long interest in the ecological and functional diversity of wood-decay types and in fruiting body development, the evolution of the genetic repertoires of both traits are incompletely known. Here, we sequenced and analyzed the genome of Auriculariopsis ampla, a close relative of the model species Schizophyllum commune. Comparative analyses of wood-decay genes in these and other 29 Agaricomycetes species revealed that the gene family composition of A. ampla and S. commune are transitional between that of white rot species and less efficient wood-degraders (brown rot, ectomycorrhizal). Rich repertoires of suberinase and tannase genes were found in both species, with tannases generally restricted to species that preferentially colonize bark-covered wood. Analyses of fruiting body transcriptomes in both A. ampla and S. commune highlighted a high rate of divergence of developmental gene expression. Several genes with conserved developmental expression were found, nevertheless, including 9 new transcription factors as well as small secreted proteins, some of which may serve as fruiting body-specific effector molecules. Taken together, the genome sequence and developmental transcriptome of Auriculariopsis ampla has highlighted novel aspects of wood-decay diversity and of fruiting body development in mushroom-forming fungi.

evolutionary biology↗