Species identity predicts decomposition capabilities of fungi better than phylogeny or functional type

Background/Question/Methods

Linking community composition to ecosystem function is a central goal of ecology. Microorganisms are responsible for decomposition of dead organic matter (i.e. litter) in ecosystems, yet we still do not understand the biological characteristics of different microbial species that determine their role in decay. We tested the hypothesis that functional type of soil fungi (i.e. primary source of carbon in soils) is a better predictor of decomposition capability than evolutionary history (i.e. phylogenetic relatedness) of fungal species. To test this hypothesis, we studied decomposition by 55 model species of soil fungi in isolation on sterilized leaf litter in laboratory microcosms. The species spanned the fungal phylogeny, including 44 genera, 38 families, and 6 orders of fungi, and included closely related pairs of ectomycorrhizal (ECM) and saprotrophic (SAP) fungi. These groups are hypothesized to vary in decomposition strategy owing to different primary source of carbon (live plant roots (ECM) vs. dead organic matter (SAP)). We measured activity of 10 different extracellular enzymes on 5 replicate microcosm samples colonized by each fungal species after 3 months of decay. For each enzyme, we tested the effect of functional type (ECM vs. SAP) and phylogenetic relatedness (net relatedness index) on activity.

Results/Conclusions

Decomposition capabilities of fungi differed among phylogenetic groups. However, the effect varied by enzyme. Cellobiose-, hemicellulose-, and protein-targeting enzymes all differed significantly among orders of fungi (P = 0.0003, P = 0.0499, P = 0.018, respectively). Cellulose-, starch-, chitin-, and phosphorus targeting enzymes did not differ significantly among phylogenetic groups. By contrast, activity of all extracellular enzymes varied by functional type. Across phylogenetic groups, cellulose-targeting (P = 0.0007), cellobiose-targeting (P = 0.0009), starch-targeting (P = 0.014), chitin-targeting (P < 0.0001), hemicellulose-targeting (P = 0.01), phosphorus-targeting (P < 0.0001), and protein-targeting (P < 0.0001) enzyme activity was significantly higher in litter colonized by saprotrophs compared to ectomycorrhizal species. However, within closely related pairs of fungi, species identity was a better predictor of decay capability than functional type. For example, protein-targeting enzymes were higher in litter colonized by Piloderma bicolor (ECM) than Anomoporia bombycina (SAP) (P<0.0001), but were higher in Amanita thiersii (SAP) than Amanita muscaria (ECM) (P<0.0001). Collectively, our results indicate that while functional type is a better predictor of decomposition niche than phylogenetic relatedness of fungi, species identity is the major determinant of decomposition capability. Differences among species at the genomic level may provide insight into the biological controls over decomposer activity.