Comparative Genomics Analyses of Lifestyle Transitions at the Origin of an Invasive Fungal Pathogen in the GenusCryphonectria

Abstract

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.

Chromosomal rearrangements with stable repertoires of genes and transposable elements in an invasive forest-pathogenic fungus

“…More noteworthy, we did not detect any significant changes in the SM and CSEP gene repertoires between the two genomes. This small variation in gain and loss of genes confirmed the results obtained in Stauber et al (2020), who compared the genomes of 90 C. parasitica isolates sampled in both the native and invasive areas, using Illumina sequencing technology. Similar results were also obtained in Microbotryum sp., the causal agents of anther-smut diseases, for which the low number of gene gains and losses observed between a ten of pairs of isolates have been considered neutral or lowly deleterious (Hartmann et al 2018).…”

Emergence and diversification of a highly invasive chestnut pathogen lineage across southeastern Europe

“…Necrotrophic pathogens like C. parasitica often rely less on effector-based gene-for-gene interactions and tend to deploy toxins or cell-wall degrading enzymes ( Friesen et al, 2008 ; Torres et al, 2020 ). Interestingly, C. parasitica has recently experienced a loss of genes associated with carbohydrate metabolism and cell-wall degradation, which may have reduced exposure to the host immunity system and increased virulence ( Stauber et al, 2020 ). The lack of genes with confirmed pathogenicity functions largely prevents thorough investigations on factors facilitating virulence evolution (e.g., epigenetic silencing or sequence rearrangements).…”

Endophytic Fungi and Ecological Fitness of Chestnuts

“…Indeed, recent observations seem to support the conjecture that mycoviruses can directly interact with the genome of fungi and convert necrotrophic pathogens into unharmful or even beneficial endophytes [ 77 , 78 ]. Moreover, additional data have pointed out that the pathogenic transition in C. parasitica was probably driven by the loss of genes involved in carbohydrate metabolism [ 79 ].…”