Phylogenetic signature of fungal response to long-term chemical pollution

Abstract

Territories around industrial enterprises represent gradients of soil acidity and heavy metal excess. Exploration of soil fungal communities in pollution gradients serves the remediation interests and brings fundamental knowledge about biota response to environmental changes. In this work, using industrial pollution as a model of environmental filtering, we performed high-throughput sequencing of 180 soil samples collected along strong long-term pollution gradients in spruce-fir and birch-pine forests. Based on 1008 Agaricomycetes operational taxonomic units, we found that in unpolluted forests, communities were randomly assembled in deep phylogenetic branches and clustered at the terminal branches. Pollution caused a 32–43% reduction in Agaricomycetes richness, resulting in the phylogenetic diversity decrease and phylogenetic clustering. The Auriculariales, Thelephorales, Phallomycetidae, Typhuloid, Marasmioid, and Tricholomatoid clades were sensitive to pollution, while Agaricoid clade, Boletales, and Russulales were tolerant, evidencing a phylogenetic signal of tolerance to pollution. To compare the trophic guilds’ response to pollution, we performed phylogenetically-informed and uninformed modeling. Both approaches showed that biotrophs were more tolerant compared to saprotrophs at different taxonomic levels, illustrating that trophic mode determines fungal response to pollution or is associated with biochemical traits underlying tolerance to heavy metal excess and soil acidification. The shift in the proportions of fungal trophic guilds, which differ in the pathways and intensity of organic matter transformation, determines carbon and nitrogen dynamics in polluted lands and the rate of ecosystem restoration after the reduction of emissions.