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.

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Fungal mycelium is increasingly recognized as a central component of soil biogeochemical cycling, yet our current understanding of the ecological controls on fungal necromass decomposition is limited to single sites and vegetation types. By deploying common fungal necromass substrates in a temperate oak savanna and hardwood forest in the midwestern USA, we assessed the generality of the rate at which high‐ and low‐quality fungal necromass decomposes; further, we investigated how the decomposer ‘necrobiome’ varies both across and within sites under vegetation types dominated by either arbuscular or ectomycorrhizal plants. The effects of necromass quality on decay rate were robust to site and vegetation type differences, with high‐quality fungal necromass decomposing, on average, 2.5 times faster during the initial stages of decay. Across vegetation types, bacterial and fungal communities present on decaying necromass differed from bulk soil microbial communities and were influenced by necromass quality. Moulds, yeasts and copiotrophic bacteria consistently dominated the necrobiome of high‐quality fungal substrates. Synthesis. We show that regardless of differences in decay environments, high‐quality fungal substrates decompose faster and support different types of decomposer micro‐organisms when compared with low‐quality fungal tissues. These findings help to refine our theoretical understanding of the dominant factors affecting fast cycling components of soil organic matter and the microbial communities associated with rapid decay.

Characterization of microbial communities in stressful conditions at a field level is rather scarce, especially when considering fungal communities from aboveground habitats. We aimed at characterizing fungal communities from different poplar habitats at a Hg-contaminated phytomanagement site by using Illumina-based sequencing, network analysis approach, and direct isolation of Hg-resistant fungal strains. The highest diversity estimated by the Shannon index was found for soil communities, which was negatively affected by soil Hg concentration. Among the significant correlations between soil operational taxonomic units (OTUs) in the co-occurrence network, 80% were negatively correlated revealing dominance of a pattern of mutual exclusion. The fungal communities associated with Populus roots mostly consisted of OTUs from the symbiotic guild, such as members of the Thelephoraceae, thus explaining the lowest diversity found for root communities. Additionally, root communities showed the highest network connectivity index, while rarely detected OTUs from the Glomeromycetes may have a central role in the root network. Unexpectedly high richness and diversity were found for aboveground habitats, compared to the root habitat. The aboveground habitats were dominated by yeasts from the Lalaria, Davidiella, and Bensingtonia genera, not detected in belowground habitats. Leaf and stem habitats were characterized by few dominant OTUs such as those from the Dothideomycete class producing mutual exclusion with other OTUs. Aureobasidium pullulans, one of the dominating OTUs, was further isolated from the leaf habitat, in addition to Nakazawaea populi species, which were found to be Hg resistant. Altogether, these findings will provide an improved point of reference for microbial research on inoculation-based programs of tailings dumps.

Industrial waste dumps are rarely colonized by vegetation after they have been abandoned, indicating biological infertility. Revegetation of industrial tailings dumps is thus necessary to prevent wind erosion, metal leaching and has been shown to restore soil functions and ecosystem services. However, little is known about the microbial colonization and community structure of vegetated tailings following the application of restoration technologies. In this study, we investigated the rhizosphere and phyllosphere bacterial communities of a poplar tree plantation within a phytomanagement-based restoration program of a Hg-contaminated site. We used Illumina-based sequencing combined with culture-dependent approaches to describe plant-associated bacterial communities and to isolate growth-promoting bacteria (PGPB) and Hg-resistant bacteria. The genus Streptomyces was highly specific to the root community, accounting for 24.4% of the relative abundance but only representing 0.8% of the soil community, whereas OTUs from the Chloroflexi phylum were essentially detected in the soil community. Aboveground habitats were dominated by bacteria from the Deinococcus-Thermus phylum, which were not detected in belowground habitats. Leaf and stem habitats were characterized by several dominant OTUs, such as those from the phylum Firmicutes in the stems or from the genera Methylobacterium, Kineococcus, Sphingomonas and Hymenobacter in the leaves. Belowground habitats hosted more cultivable Hg-resistant bacteria than aboveground habitats and more Hg-resistant bacteria were found on the episphere than in endospheric habitats. Hg-resistant isolates exhibiting plant growth-promoting (PGP) traits, when used as inoculants of Capsicum annuum, were shown to increase its root dry biomass but not Hg concentration. The N-fixing and Hg-resistant species Pseudomonas graminis, observed in the poplar phyllosphere, may be a key microorganism for the restoration of industrial tailings dumps.

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Understanding the post-senescent fate of fungal mycelium is critical to accurately quantifying forest carbon and nutrient cycling, but how this organic matter source decomposes in wood remains poorly studied. In this study, we compared the decomposition of dead fungal biomass (a.k.a. necromass) of two species, Mortierella elongata and Meliniomyces bicolor, in paired wood and soil plots in a boreal forest in northern Minnesota, USA. Mass loss was quantified at four time points over an 8-week incubation and the richness and composition of the fungal communities colonizing fungal necromass were characterized using high-throughput sequencing. We found that the structure of fungal decomposer communities in wood and soil differed, but, in both habitats, there was relatively rapid decay (∼30% remaining after 56 days). Mass loss was significantly faster in soil and for high-quality (i.e. high nitrogen and low melanin) fungal necromass. In both habitats, there was a clear trajectory of early colonization by opportunistic fungal taxa followed by colonization of fungi with greater enzymatic capacities to degrade more recalcitrant compounds, including white-rot and ectomycorrhizal fungi. Collectively, our results indicate that patterns emerging regarding substrate quality effects on fungal necromass decomposition in soil and leaf litter can be largely extended to fungal necromass decomposition in wood.

Chitin is one of the most abundant nitrogen-containing polymers in forest soil. Ability of ectomycorrhizal (EM) fungi to utilize chitin may play a key role in the EM symbiosis nutrition and soil carbon cycle. In forest, EM fungi exhibit high diversity, which could be based on function partitioning and trait complementarity. Although it has long been recognized that closely related species share functional characteristics, the phylogenetic conservatism of functional traits within microorganisms remains unclear. Because extracellular N-acetylglucosaminidase activity has been proposed as functional trait of chitin degradation, we screened this activity on 35 EM fungi species with or without chitin in the growth medium to (i) describe the functional diversity of EM fungi and (ii) identify potential links between this functional trait and EM fungal phylogeny. We observed large variations of the extracellular N-acetylglucosaminidase activities among the fungal strains. Furthermore, our results revealed two regulation patterns of extracellular N-acetylglucosaminidase activities. Indeed, these chitinolytic activities were stimulated or repressed in the presence of chitin, in comparison to the control treatment. These profiles of extracellular N-acetylglucosaminidase stimulation/repression might be conserved at a high phylogenetic level in the Basidiomycota phylum, as illustrated by the opposite patterns of regulation between Boletales and Agaricales. Finally, the downregulation of this activity by chitin, for some EM fungal groups, might suggest another chitin degradation pathway.