Laure Fauchery

Grassland ecosystems contain approximately 40% of terrestrial organic carbon; however, the genomic mechanisms underlying fungal decomposer adaptation to these environments remain poorly understood. We sequenced 22 new genomes of Agaricales mushroom-forming fungi and compared them with 100 published genomes spanning diverse ecological niches to investigate the genomic innovations associated with substrate specialisation. Our analyses revealed distinct genomic signatures across ecological guilds, with ectomycorrhizal fungi showing a pronounced reduction in plant cell wall-degrading enzymes, whereas grassland saprotrophs exhibited convergent expansion of cellulose-degrading machinery, particularly the CBM1, CBM13, and AA9 families. Notably, several species displayed intermediate genomic profiles that challenge traditional ecological classifications, suggesting more complex evolutionary trajectories along the saprotrophy-symbiosis spectrum than previously recognised. We focused our detailed analysis on Agaricus sinodeliciosus, a wild mushroom endemic to the high-altitude Tibetan Plateau grasslands, which uniquely forms large fruiting bodies underground. Compared to its cultivated relative A. bisporus, A. sinodeliciosus showed substantial genome expansion through transposable element proliferation, a dramatic reduction in plant cell wall-degrading enzymes, and species-specific pathways, including expanded tyrosine metabolism for melanin synthesis and hypoxia-responsive HIF-1 signalling. Transcriptomic analysis revealed that underground fruiting involves the coordinated regulation of hydrophobins, environmental sensors responsive to pH and nutrient availability, and downregulation of cAMP signalling pathways, which typically suppress fruiting body formation. These findings illuminate the genomic basis of fungal niche adaptation and highlight how substrate chemistry and environmental extremes drive the evolutionary innovation of mushroom-forming fungi.

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.

Summary: Microbial communities interplay with their environment through their functional traits that can be a response or an effect on the environment. Here, we explore how a functional trait—the decomposition of organic matter, can be addressed based on genetic markers and how the expression of these markers reflect ecological strategies of two fungal litter decomposer Gymnopus androsaceus and Chalara longipes . We sequenced the genomes of these two fungi, as well as their transcriptomes at different steps of Pinus sylvestris needles decomposition in microcosms. Our results highlighted that if the gene content of the two species could indicate similar potential decomposition abilities, the expression levels of specific gene families belonging to the glycoside hydrolase category reflected contrasting ecological strategies. Actually, C . longipes , the weaker decomposer in this experiment, turned out to have a high content of genes involved in cell wall polysaccharides decomposition but low expression levels, reflecting a versatile ecology compare to the more competitive G . androsaceus with high expression levels of keystone functional genes. Thus, we established that sequential expression of genes coding for different components of the decomposer machinery indicated adaptation to chemical changes in the substrate as decomposition progressed.

The access and recycling of the base cations are essential processes for the long-lasting functioning of forest ecosystems. While the role of soil bacterial communities has been demonstrated in mineral weathering and tree nutrition, our understanding of the link between the availability of base cations and the functioning of these communities remains limited. To fill this gap, we developed a microcosm approach to investigate how an increase in key base cations (potassium or magnesium) impacted the taxonomic and functional structures of the bacterial communities. During a 2-month period after fertilization with available potassium or magnesium, soil properties, global functions (metabolic potentials and respiration) as well as mineral weathering bioassays and 16S rRNA amplicon pyrosequencing were monitored. Our analyses showed no or small variations in the taxonomic structure, total densities and global functions between the treatments. In contrast, a decrease in the frequency and effectiveness of mineral weathering bacteria was observed in the fertilized treatments. Notably, quantitative PCR targeting specific genera known for their mineral weathering ability (i.e., Burkholderia and Collimonas) confirmed this decrease. These new results suggest that K and Mg cation availability drives the distribution of the mineral weathering bacterial communities in forest soil.