Project description:To understand the evolution of genome regulation and cell differentiation, we investigated the transcriptional dynamics of the ichthyosporean Creolimax fragrantissima, a close relative of animals that undergoes coenocytic development. We report the transcriptional differences between the amoeboid stage and the multinucleate stage of this species, describing the various aspects of differential genome regualtion found in those samples.
Project description:Cooperation is associated with major transitions in evolution such as the emergence of multicellularity. It is central to the evolution of many complex traits in nature, including growth and virulence in pathogenic bacteria. Whether cells of multicellular parasites function cooperatively during infection remains however largely unknown. Here, we show that hyphal cells of the fungal pathogen Sclerotinia sclerotiorum reprogram towards division of labor to facilitate the colonization of host plants. Using global transcriptome sequencing, we reveal that gene expression patterns diverge markedly in cells at the center and apex of hyphae during A. thaliana colonization compared to in vitro growth. We reconstructed a genome-scale metabolic model for S. sclerotiorum and used flux balance analysis to demonstrate metabolic heterogeneity supporting division of labor between hyphal cells. Accordingly, continuity between the central and apical compartments of invasive hyphae was required for optimal growth in planta. Using a multi-cell model of fungal hyphae, we show that this cooperative functioning enhances fungal growth predominantly during host colonization. Our work identifies cooperation in fungal hyphae as a mechanism emerging at the multicellular level to support host colonization and virulence.
Project description:Bilaterian animals differ from other metazoans in their apparent bilateral symmetry and the development of a third germ layer. Both might have facilitated the evolution of the diverse and complex bilaterian body plans. The first cnidarian genome sequence revealed that despite their morphological simplicity, this sister group to all bilaterians shares an immense genomic complexity with vertebrates. This suggested that it might have been the complexity of gene regulation which increased during the evolution of bilaterians. We compared the gene regulatory landscape of cnidarians and bilaterians. To this end we generated the first genome-wide prediction of gene regulatory elements and profiled five epigenetic marks in a non-bilaterian animal, the cnidarian Nematostella vectensis. We found that the location of chromatin modifications relative to genes and distal enhancers is conserved among eumetazoans. Surprisingly, the genomic landscape of gene regulatory elements is highly similar between Nematostella and bilaterian model organisms. This suggests that complex regulation of developmental gene expression evolved in eumetazoans without a major increase in complexity in bilaterians. ChIP-seq of p300, RNA Pol2, and five histone modifications in Nematostella vectensis.
Project description:In this study, we profiled the transcriptional changes in a polyphagous spider mite, Tetranychus urticae, after adaptation to spatial and tempospatial stress. We show heritable down-regulation of genes encoding for core enzymes involved in the citric acid and gluconeogenesis/glycolyse pathways (glucose 6-phosphatase among others). Additionally, we observe heritable transcriptional changes in amino acid pathways (methionine, tyrosine and phenylalanine) and in laterally acquired genes from bacteria (cobalamin-independent methionine synthase). By similiar study results in other organisms, we argue that these heritable transcriptional changes (partially) underpin the changed life history traits observed in our experimental evolution set-up.
Project description:The “Amoeboid Predator-Fungal Animal Virulence Hypothesis” posits that interactions with environmental phagocytes shape the evolution of virulence traits in fungal pathogens. In this hypothesis, selection to avoid predation by amoeba inadvertently selects for traits that contribute to fungal escape from phagocytic immune cells. Here, we investigate this hypothesis in the human fungalpathogens Cryptococcus neoformans and Cryptococcus deneoformans. Applying quantitative trait locus (QTL) mapping and comparative genomics, we discovered a cross-species QTL region that is responsible for variation in resistance to amoeba predation. In C. neoformans, this same QTL was found to have pleiotropic effects on melanization, an established virulence factor. Through fine mapping and population genomic comparisons, we identified the gene encoding the transcription factor BZP4 that underlies this pleiotropic QTL and we show that decreased expression of this gene reduces melanization and increases susceptibility to amoeba predation. Despite the joint effects of BZP4 on amoeba resistance and melanin production, we find no relationship between BZP4 genotype and escape from macrophages or virulence in murine models of disease. Our findings provide new perspectives on how microbial ecology shapes the genetic architecture of fungal virulence, and suggests the need for more nuanced models for the evolution of pathogenesis that account for the complexities of both microbe-microbe and microbe-host interactions.
Project description:The Aspergillus fumigatus sterol regulatory element binding protein (SREBP) SrbA belongs to the basic Helix-Loop-Helix (bHLH) family of transcription factors and is crucial for antifungal drug resistance and virulence. The latter phenotype is especially striking, as loss of SrbA results in complete loss of virulence in murine models of invasive pulmonary aspergillosis (IPA). How fungal SREBPs mediate fungal virulence is unknown, though it has been suggested that lack of growth in hypoxic conditions accounts for the attenuated virulence. To further understand the role of SrbA in fungal infection site pathobiology, chromatin immunoprecipitation followed by massively parallel DNA sequencing (ChIP-seq) was used to identify genes under direct SrbA transcriptional regulation in hypoxia. These results confirmed the direct regulation of ergosterol biosynthesis and iron uptake by SrbA in hypoxia and revealed new roles for SrbA in nitrate assimilation and heme biosynthesis. Moreover, functional characterization of an SrbA target gene with sequence similarity to SrbA identified a new transcriptional regulator of the fungal hypoxia response and virulence, SrbB. SrbB co-regulates genes involved in heme biosynthesis and demethylation of C4 sterols with SrbA in hypoxic conditions. However, SrbB also has regulatory functions independent of SrbA including regulation of carbohydrate metabolism. Loss of SrbB markedly attenuates A. fumigatus virulence, and loss of both SREBPs further reduces in vivo fungal growth. These data suggest that both A. fumigatus SREBPs are critical for hypoxia adaptation and virulence and reveals new insights into SREBPM-bM-^@M-^Ys complex role in infection site adaptation and fungal virulence. 4 hour and 12 hour ChIP experiments were completed. Input control samples for each set were collected.
Project description:Members of the fungal genus Armillaria are necrotrophic pathogens with efficient plant biomass-degrading strategies. Armillaria species are some of the largest terrestrial organisms on Earth that cause tremendous losses in diverse ecosystems. Despite their global importance, how 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, acquired at least 1,025 genes via 124 horizontal gene transfer (HGT) events, primarily from Ascomycota donors. Functional and expression data suggest that HGT might have affected plant biomass-degrading and virulence abilities of Armillaria, two pivotal traits in their lifestyle. HGT provides an explanation for their soft-rot like biomass degrading strategy, which is which is markedly different from the primarily white rot decay mechanism of related species. Combined multi-species expression data revealed extensive regulation of horizontally acquired and wood-decay related genes, putative virulence factors as well as novel conserved pathogenicity-induced small secreted proteins (PiSSPs), two of which were experimentally verified to induce necrosis in live plants. Overall, this study details how evolution knitted together horizontally and vertically inherited genes in complex adaptive traits, such as plant biomass degradation and pathogenicity in one of the most influential fungal pathogens of temperate forest ecosystems.
Project description:Members of the fungal genus Armillaria are necrotrophic pathogens with efficient plant biomass-degrading strategies. Armillaria species are some of the largest terrestrial organisms on Earth that cause tremendous losses in diverse ecosystems. Despite their global importance, how 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 acquired at least 1025 genes via 124 horizontal gene transfer (HGT) events, primarily from Ascomycota donors. Functional and expression data suggest that HGT might have affected plant biomass-degrading and virulence abilities of Armillaria, two pivotal traits in their lifestyle. HGT provides an explanation for their soft-rot like biomass degrading strategy too, which is markedly different from the primarily white rot decay mechanism of related species. Combined multi-species expression data revealed putative virulence factors, extensive regulation of horizontally acquired and wood-decay related genes as well as novel noserved 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 pathogenicityin one of the most influential fungal pathogens of temperate forest ecosystems.
Project description:Members of the fungal genus Armillaria are necrotrophic pathogens with efficient plant biomass-degrading strategies. Armillaria species are some of the largest terrestrial organisms on Earth that cause tremendous losses in diverse ecosystems. Despite their global importance, how 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 acquired at least 1025 genes via 124 horizontal gene transfer (HGT) events, primarily from Ascomycota donors. Functional and expression data suggest that HGT might have affected plant biomass-degrading and virulence abilities of Armillaria, two pivotal traits in their lifestyle. HGT provides an explanation for their soft-rot like biomass degrading strategy too, which is markedly different from the primarily white rot decay mechanism of related species. Combined multi-species expression data revealed putative virulence factors, extensive regulation of horizontally acquired and wood-decay related genes as well as novel noserved 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 pathogenicityin one of the most influential fungal pathogens of temperate forest ecosystems.
Project description:Members of the fungal genus Armillaria are necrotrophic pathogens with efficient plant biomass-degrading strategies. Armillaria species are some of the largest terrestrial organisms on Earth that cause tremendous losses in diverse ecosystems. Despite their global importance, how 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 acquired at least 1025 genes via 124 horizontal gene transfer (HGT) events, primarily from Ascomycota donors. Functional and expression data suggest that HGT might have affected plant biomass-degrading and virulence abilities of Armillaria, two pivotal traits in their lifestyle. HGT provides an explanation for their soft-rot like biomass degrading strategy too, which is markedly different from the primarily white rot decay mechanism of related species. Combined multi-species expression data revealed putative virulence factors, extensive regulation of horizontally acquired and wood-decay related genes as well as novel noserved 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 pathogenicityin one of the most influential fungal pathogens of temperate forest ecosystems.