For 15 years, the team has used combinations of various approaches (laboratory experiments, field work, modeling, population genetics and genomics) for contributing to our understanding of the fungal diversity and of how organisms evolve and adapt to their environment. The question of adaptation is fundamental to understand the living world, and it also has applied importance within the context of current global changes (climate change but also movements of organisms worldwide and habitat disturbance) and increasing food demand. In addition, microbial diversity and its evolution are still poorly known, while fungi have paramount ecological and economic importance. Indeed, fungi ensure many services in ecosystems (like recycling the organic matter or establishing essential symbioses with plants), they can be the dangerous pathogens in natural populations and crops, and they were domesticated for a variety of uses, such as food fermentation and antibiotic production.
For some years, the team has developed genomic studies, to obtain new perspectives on the mechanisms of adaptation. Fungi are good eukaryotic models for these questions, given their small genomes, their accessible haploid phase, their experimental tractability and the functional data available. We could obtain a complete assembly of the genome of the fungus Microbotryum lychnidis–dioicae, thanks to the recent improvements of the Pacific Biosciences technology, which produces very long reads. This assembly was the first eukaryotic genome published with chromosome-length assemblies using new sequencing technologies. The analysis of the M. lychnidis–dioicae genome revealed features linked to its obligatory biotroph lifestyle, with in particular a repertoire of putative effectors in the form of small secreted proteins and of expansions of gene families, such as lipases which could contribute degrading cuticular waxes of the host plant.
We also have sequenced the genomes of fifty individuals to study the prevalence and genomic bases of adaptation in M. lychnidis-dioicae. A recent episode of adaptation leaves particular signatures: for example when a beneficial allele is selected for, the frequency of this allele in the population increases quickly, as that of the linked alleles, creating a local decrease in diversity. This is called a selective sweep. Our population genomic study revealed selective sweeps in ca. fifty regions of the genome in M. lychnidis-dioicae (17% of the genome was affected by recent selective sweeps). In the genomic regions of selective sweeps, the most represented functional categories were related to interactions with the host. This represented one of the first studies of selective sweeps at the level of a completely assembled eukaryotic genome, and the results showed that an unexpected proportion of the genome was involved in recent adaptation events and identified key functions. Overall, these results are important for our understanding of the evolution of new species of emerging pathogenic fungi, and their adaptation onto new hosts.
We also have sequenced several genomes of the fungus M. lychnidis-dioicae parasitizing plants in areas more or less contaminated around Chernobyl and studied the frequency of the disease, the capacity of spores to germinate and grow. We did not find any footprints of deleterious changes in the genomes or decrease in viability which would be correlated with the radiation levels in the field, likely because the red pigments of the fungus protect it from radiations. In fact, many fungi with pigments are very resistant and can grow close to the damaged reactor. On the other hand, the frequency of the disease decreased with the rate of radiation in the field, likely because the abundance of the pollinators decreased, while pollinators transport the spores of the fungus, and pollinators are sensitive to radiations.
We will also use approaches of comparative genomics to understand the mechanisms underlying adaptation and the formation of new species using as models the Microbotryum pathogenic fungi, causing the anther-smut disease sterilizing plants of the Caryophyllaceae family. Indeed, there exists more than 100 species in this genus causing anther-smut disease, the various species being phylogenetically close but specialized on different host plants. There was thus an adaptive radiation, with specialization events on very different and well identified ecological niches, which makes it an excellent model to study the underlying genomic mechanisms of adaptation. We already obtained genome assemblies of exceptional quality for 20 pathogenic species of Microbotryum specialized on different plants. This constitutes a unique material, making it possible to study poorly known processes, like the role of the gene gains and losses, chromosomal rearrangements, and localization in particular genomic regions. Indeed, new sequencing technologies did not allow until one or two years ago to obtain information on the genomic structure, whereas it is essential to understand whether certain genomic areas, such as regions rich in transposable elements, telomeres, or chromosomal inversions, play a significant role in the processes of adaptation, by generating variability or by protecting beneficial association of alleles from recombination. This constitutes a new frontier of research regarding the genomics of adaptation.