Comparative genomics reveals a core gene toolbox for lifestyle transitions in Hypocreales fungi.
Ontology highlight
ABSTRACT:
SUBMITTER: Wu B
PROVIDER: S-EPMC8360070 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Modern genomics has shed light on many entomopathogenic fungi and expanded our knowledge widely; however, little is known about the genomic features of the insect-commensal fungi. Harpellales are obligate commensals living in the digestive tracts of disease-bearing insects (black flies, midges, and mosquitoes). In this study, we produced and annotated whole-genome sequences of nine Harpellales taxa and conducted the first comparative analyses to infer the genomic diversity within the members of the Harpellales. The genomes of the insect gut fungi feature low (26% to 37%) GC content and large genome size variations (25 to 102 Mb). Further comparisons with insect-pathogenic fungi (from both Ascomycota and Zoopagomycota), as well as with free-living relatives (as negative controls), helped to identify a gene toolbox that is essential to the fungus-insect symbiosis. The results not only narrow the genomic scope of fungus-insect interactions from several thousands to eight core players but also distinguish host invasion strategies employed by insect pathogens and commensals. The genomic content suggests that insect commensal fungi rely mostly on adhesion protein anchors that target digestive system, while entomopathogenic fungi have higher numbers of transmembrane helices, signal peptides, and pathogen-host interaction (PHI) genes across the whole genome and enrich genes as well as functional domains to inactivate the host inflammation system and suppress the host defense. Phylogenomic analyses have revealed that genome sizes of Harpellales fungi vary among lineages with an integer-multiple pattern, which implies that ancient genome duplications may have occurred within the gut of insects.IMPORTANCE Insect guts harbor various microbes that are important for host digestion, immune response, and disease dispersal in certain cases. Bacteria, which are among the primary endosymbionts, have been studied extensively. However, fungi, which are also frequently encountered, are poorly known with respect to their biology within the insect guts. To understand the genomic features and related biology, we produced the whole-genome sequences of nine gut commensal fungi from disease-bearing insects (black flies, midges, and mosquitoes). The results show that insect gut fungi tend to have low GC content across their genomes. By comparing these commensals with entomopathogenic and free-living fungi that have available genome sequences, we found a universal core gene toolbox that is unique and thus potentially important for the insect-fungus symbiosis. This comparative work also uncovered different host invasion strategies employed by insect pathogens and commensals, as well as a model system to study ancient fungal genome duplication within the gut of insects.
| S-EPMC5954228 | biostudies-literature
Project description:Dark septate endophytes (DSE) are a form-group of root endophytic fungi with elusive functions. Here, the genomes of two common DSE of semiarid areas, Cadophora sp. and Periconia macrospinosa were sequenced and analyzed with another 32 ascomycetes of different lifestyles. Cadophora sp. (Helotiales) and P. macrospinosa (Pleosporales) have genomes of 70.46 Mb and 54.99 Mb with 22,766 and 18,750 gene models, respectively. The majority of DSE-specific protein clusters lack functional annotation with no similarity to characterized proteins, implying that they have evolved unique genetic innovations. Both DSE possess an expanded number of carbohydrate active enzymes (CAZymes), including plant cell wall degrading enzymes (PCWDEs). Those were similar in three other DSE, and contributed a signal for the separation of root endophytes in principal component analyses of CAZymes, indicating shared genomic traits of DSE fungi. Number of secreted proteases and lipases, aquaporins, and genes linked to melanin synthesis were also relatively high in our fungi. In spite of certain similarities between our two DSE, we observed low levels of convergence in their gene family evolution. This suggests that, despite originating from the same habitat, these two fungi evolved along different evolutionary trajectories and display considerable functional differences within the endophytic lifestyle.
| S-EPMC5910433 | biostudies-literature
Project description:While there has been significant progress characterizing the 'symbiotic toolkit' of ectomycorrhizal (ECM) fungi, how host specificity may be encoded into ECM fungal genomes remains poorly understood. We conducted a comparative genomic analysis of ECM fungal host specialists and generalists, focusing on the specialist genus Suillus. Global analyses of genome dynamics across 46 species were assessed, along with targeted analyses of three classes of molecules previously identified as important determinants of host specificity: small secreted proteins (SSPs), secondary metabolites (SMs) and G-protein coupled receptors (GPCRs). Relative to other ECM fungi, including other host specialists, Suillus had highly dynamic genomes including numerous rapidly evolving gene families and many domain expansions and contractions. Targeted analyses supported a role for SMs but not SSPs or GPCRs in Suillus host specificity. Phylogenomic-based ancestral state reconstruction identified Larix as the ancestral host of Suillus, with multiple independent switches between white and red pine hosts. These results suggest that like other defining characteristics of the ECM lifestyle, host specificity is a dynamic process at the genome level. In the case of Suillus, both SMs and pathways involved in the deactivation of reactive oxygen species appear to be strongly associated with enhanced host specificity.
| S-EPMC7969408 | biostudies-literature
Project description:Synchytrium endobioticum is an obligate biotrophic soilborne Chytridiomycota (chytrid) species that causes potato wart disease, and represents the most basal lineage among the fungal plant pathogens. We have chosen a functional genomics approach exploiting knowledge acquired from other fungal taxa and compared this to several saprobic and pathogenic chytrid species. Observations linked to obligate biotrophy, genome plasticity and pathogenicity are reported. Essential purine pathway genes were found uniquely absent in S. endobioticum, suggesting that it relies on scavenging guanine from its host for survival. The small gene-dense and intron-rich chytrid genomes were not protected for genome duplications by repeat-induced point mutation. Both pathogenic chytrids Batrachochytrium dendrobatidis and S. endobioticum contained the largest amounts of repeats, and we identified S. endobioticum specific candidate effectors that are associated with repeat-rich regions. These candidate effectors share a highly conserved motif, and show isolate specific duplications. A reduced set of cell wall degrading enzymes, and LysM protein expansions were found in S. endobioticum, which may prevent triggering plant defense responses. Our study underlines the high diversity in chytrids compared to the well-studied Ascomycota and Basidiomycota, reflects characteristic biological differences between the phyla, and shows commonalities in genomic features among pathogenic fungi.
| S-EPMC6572847 | biostudies-literature
Project description:Emerging fungal pathogens are a threat to forest and agroecosystems, as well as animal and human health. How pathogens evolve from nonpathogenic ancestors is still poorly understood, making the prediction of future outbreaks challenging. Most pathogens have evolved lifestyle adaptations, which were enabled by specific changes in the gene content of the species. Hence, understanding transitions in the functions encoded by genomes gives valuable insight into the evolution of pathogenicity. Here, we studied lifestyle evolution in the genus Cryphonectria, including the prominent invasive pathogen Cryphonectria parasitica, the causal agent of chestnut blight on Castanea species. We assembled and compared the genomes of pathogenic and putatively nonpathogenic Cryphonectria species, as well as sister group pathogens in the family Cryphonectriaceae (Diaporthales, Ascomycetes), to investigate the evolution of genome size and gene content. We found a striking loss of genes associated with carbohydrate metabolism (CAZymes) in C. parasitica compared to other Cryphonectriaceae. Despite substantial CAZyme gene loss, experimental data suggest that C. parasitica has retained wood colonization abilities shared with other Cryphonectria species. Putative effectors substantially varied in number, cysteine content, and protein length among species. In contrast, secondary metabolite gene clusters show a high degree of conservation within the genus. Overall, our results underpin the recent lifestyle transition of C. parasitica toward a more pathogenic lifestyle. Our findings suggest that a CAZyme loss may have promoted pathogenicity of C. parasitica on Castanea species. Analyzing gene complements underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.IMPORTANCE Forest and agroecosystems, as well as animal and human health, are threatened by emerging pathogens. Following decimation of chestnuts in the United States, the fungal pathogen Cryphonectria parasitica colonized Europe. After establishment, the pathogen population gave rise to a highly successful lineage that spread rapidly across the continent. Core to our understanding of what makes a successful pathogen is the genetic repertoire enabling the colonization and exploitation of host species. Here, we have assembled >100 genomes across two related genera to identify key genomic determinants leading to the emergence of chestnut blight. We found subtle yet highly specific changes in the transition from saprotrophy to latent pathogenicity mostly determined by enzymes involved in carbohydrate metabolism. Large-scale genomic analyses of genes underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.
| S-EPMC7565894 | biostudies-literature
Project description:Various strains of the mycoparasitic fungal species Clonostachys rosea are used commercially as biological control agents for the control of fungal plant diseases in agricultural crop production. Further improvements of the use and efficacy of C. rosea in biocontrol require a mechanistic understanding of the factors that determines the outcome of the interaction between C. rosea and plant pathogenic fungi. Here, we determined the genome sequences of 11 Clonostachys strains, representing five species in Clonostachys subgenus Bionectria, and performed a comparative genomic analysis with the aim to identify gene families evolving under selection for gene gains or losses. Several gene families predicted to encode proteins involved in biosynthesis of secondary metabolites, including polyketide synthases, nonribosomal peptide syntethases and cytochrome P450s, evolved under selection for gene gains (p ≤ .05) in the Bionectria subgenus lineage. This was accompanied with gene copy number increases (p ≤ .05) in ATP-binding cassette (ABC) transporters and major facilitator superfamily (MFS) transporters predicted to contribute to drug efflux. Most Clonostachys species were also characterized by high numbers of auxiliary activity (AA) family 9 lytic polysaccharide monooxygenases, AA3 glucose-methanol-choline oxidoreductases and additional carbohydrate-active enzyme gene families with putative activity (or binding) towards xylan and rhamnose/pectin substrates. Particular features of the C. rosea genome included expansions (p ≤ .05) of the ABC-B4 multidrug resistance transporters, the ABC-C5 multidrug resistance-related transporters and the 2.A.1.3 drug:H + antiporter-2 MFS drug resistance transporters. The ABC-G1 pleiotropic drug resistance transporter gene abcG6 in C. rosea was induced (p ≤ .009) by exposure to the antifungal Fusarium mycotoxin zearalenone (1121-fold) and various fungicides. Deletion of abcG6 resulted in mutants with reduced (p < .001) growth rates on media containing the fungicides boscalid, fenhexamid and iprodione. Our results emphasize the role of biosynthesis of, and protection against, secondary metabolites in Clonostachys subgenus Bionectria.
| S-EPMC7896725 | biostudies-literature
Project description:BackgroundPectobacterium spp. are necrotrophic bacterial plant pathogens of the family Pectobacteriaceae, responsible for a wide spectrum of diseases of important crops and ornamental plants including soft rot, blackleg, and stem wilt. P. carotovorum is a genetically heterogeneous species consisting of three valid subspecies, P. carotovorum subsp. brasiliense (Pcb), P. carotovorum subsp. carotovorum (Pcc), and P. carotovorum subsp. odoriferum (Pco).ResultsThirty-two P. carotovorum strains had their whole genomes sequenced, including the first complete genome of Pco and another circular genome of Pcb, as well as the high-coverage genome sequences for 30 additional strains covering Pcc, Pcb, and Pco. In combination with 52 other publicly available genome sequences, the comparative genomics study of P. carotovorum and other four closely related species P. polaris, P. parmentieri, P. atrosepticum, and Candidatus P. maceratum was conducted focusing on CRISPR-Cas defense systems and pathogenicity determinants. Our analysis identified two CRISPR-Cas types (I-F and I-E) in Pectobacterium, as well as another I-C type in Dickeya that is not found in Pectobacterium. The core pathogenicity factors (e.g., plant cell wall-degrading enzymes) were highly conserved, whereas some factors (e.g., flagellin, siderophores, polysaccharides, protein secretion systems, and regulatory factors) were varied among these species and/or subspecies. Notably, a novel type of T6SS as well as the sorbitol metabolizing srl operon was identified to be specific to Pco in Pectobacterium.ConclusionsThis study not only advances the available knowledge about the genetic differentiation of individual subspecies of P. carotovorum, but also delineates the general genetic features of P. carotovorum by comparison with its four closely related species, thereby substantially enriching the extent of information now available for functional genomic investigations about Pectobacterium.
| S-EPMC6286560 | biostudies-literature
Project description:Sooty blotch and flyspeck (SBFS) fungi are a distinctive group of plant pathogens which, although phylogenetically diverse, occupy an exclusively surface-dwelling niche. They cause economic losses by superficially blemishing the fruit of several tree crops, principally apple, in moist temperate regions worldwide. In this study, we performed genome-wide comparative analyses separately within three pairs of species of ascomycete pathogens; each pair contained an SBFS species as well as a closely related but plant-penetrating parasite (PPP) species. Our results showed that all three of the SBFS pathogens had significantly smaller genome sizes, gene numbers and repeat ratios than their counterpart PPPs. The pathogenicity-related genes encoding MFS transporters, secreted proteins (mainly effectors and peptidases), plant cell wall degrading enzymes, and secondary metabolism enzymes were also drastically reduced in the SBFS fungi compared with their PPP relatives. We hypothesize that the above differences in genome composition are due largely to different levels of acquisition, loss, expansion, and contraction of gene families and emergence of orphan genes. Furthermore, results suggested that horizontal gene transfer may have played a role, although limited, in the divergent evolutionary paths of SBFS pathogens and PPPs; repeat-induced point mutation could have inhibited the propagation of transposable elements and expansion of gene families in the SBFS group, given that this mechanism is stronger in the SBFS fungi than in their PPP relatives. These results substantially broaden understanding of evolutionary mechanisms of adaptation of fungi to the epicuticular niche of plants.
| S-EPMC5737583 | biostudies-literature
Project description:Ascosphaera (Eurotiomycetes: Onygenales) is a diverse genus of fungi that is exclusively found in association with bee nests and comprises both saprophytic and entomopathogenic species. To date, most genomic analyses have been focused on the honeybee pathogen A. apis, and we lack a genomic understanding of how pathogenesis evolved more broadly in the genus. To address this gap we sequenced the genomes of the leaf-cutting bee pathogen A. aggregata as well as three commensal species: A. pollenicola, A. atra and A. acerosa. De novo annotation and comparison of the assembled genomes was carried out, including the previously published genome of A. apis. To identify candidate virulence genes in the pathogenic species, we performed secondary metabolite-oriented analyses and clustering of biosynthetic gene clusters (BGCs). Additionally, we captured single copy orthologs to infer their phylogeny and created codon-aware alignments to determine orthologs under selective pressure in our pathogenic species. Our results show several shared BGCs between A. apis, A. aggregata and A. pollenicola, with antifungal resistance related genes present in the bee pathogens and commensals. Genes involved in metabolism and protein processing exhibit signatures of enrichment and positive selection under a fitted branch-site model. Additional known virulence genes in A. pollenicola, A. acerosa and A. atra are identified, supporting previous hypotheses that these commensals may be opportunistic pathogens. Finally, we discuss the importance of such genes in other fungal pathogens, suggesting a common route to evolution of pathogenicity in Ascosphaera.
| S-EPMC10793876 | biostudies-literature
Project description:Vibrio cholerae, the causative agent of cholera, is a bacterium autochthonous to the aquatic environment, and a serious public health threat. V. cholerae serogroup O1 is responsible for the previous two cholera pandemics, in which classical and El Tor biotypes were dominant in the sixth and the current seventh pandemics, respectively. Cholera researchers continually face newly emerging and reemerging pathogenic clones carrying diverse combinations of phenotypic and genotypic properties, which significantly hampered control of the disease. To elucidate evolutionary mechanisms governing genetic diversity of pandemic V. cholerae, we compared the genome sequences of 23 V. cholerae strains isolated from a variety of sources over the past 98 years. The genome-based phylogeny revealed 12 distinct V. cholerae lineages, of which one comprises both O1 classical and El Tor biotypes. All seventh pandemic clones share nearly identical gene content. Using analogy to influenza virology, we define the transition from sixth to seventh pandemic strains as a "shift" between pathogenic clones belonging to the same O1 serogroup, but from significantly different phyletic lineages. In contrast, transition among clones during the present pandemic period is characterized as a "drift" between clones, differentiated mainly by varying composition of laterally transferred genomic islands, resulting in emergence of variants, exemplified by V. cholerae O139 and V. cholerae O1 El Tor hybrid clones. Based on the comparative genomics it is concluded that V. cholerae undergoes extensive genetic recombination via lateral gene transfer, and, therefore, genome assortment, not serogroup, should be used to define pathogenic V. cholerae clones.
| S-EPMC2741270 | biostudies-literature