Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus

Abstract

The majority of nitrogen in forest soils is found in organic matter–protein complexes. Ectomycorrhizal fungi (EMF) are thought to have a key role in decomposing and mobilizing nitrogen from such complexes. However, little is known about the mechanisms governing these processes, how they are regulated by the carbon in the host plant and the availability of more easily available forms of nitrogen sources. Here we used spectroscopic analyses and transcriptome profiling to examine how the presence or absence of glucose and/or ammonium regulates decomposition of litter material and nitrogen mobilization by the ectomycorrhizal fungus Paxillus involutus. We found that the assimilation of nitrogen and the decomposition of the litter material are triggered by the addition of glucose. Glucose addition also resulted in upregulation of the expression of genes encoding enzymes involved in oxidative degradation of polysaccharides and polyphenols, peptidases, nitrogen transporters and enzymes in pathways of the nitrogen and carbon metabolism. In contrast, the addition of ammonium to organic matter had relatively minor effects on the expression of transcripts and the decomposition of litter material, occurring only when glucose was present. On the basis of spectroscopic analyses, three major types of chemical modifications of the litter material were observed, each correlated with the expression of specific sets of genes encoding extracellular enzymes. Our data suggest that the expression of the decomposition and nitrogen assimilation processes of EMF can be tightly regulated by the host carbon supply and that the availability of inorganic nitrogen as such has limited effects on saprotrophic activities.

Endemism and functional convergence across the North American soil mycobiome

“…Specifically, peroxidase activity correlated positively with the ratio of ectomycorrhizal to saprotrophic diversity, whereas cellobiohydrolases showed the reverse trend, correlating positively with the ratio of saprotrophic to ectomycorrhizal diversity (Dataset S1). These observations are consistent with the classical notion of saprotrophs as principal degraders of readily available carbon, as well as recent hypotheses that ectomycorrhizal fungi target nutrients bound in complex soil organic matter (49,50). Because species-level composition of fungal communities does not correlate strongly with enzyme activity at the scale of this study, functional trait or phylogenetic approaches targeting key resource acquisition strategies may offer a better predictive framework for understanding fungal function across systems that have few species in common.…”

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

“…They are portrayed as mutualists trading host photoassimilates for nutrients and having limited capacity to decompose soil lignocellulose 1-3 , as a result of their reduced repertoire of PCWDEs 4-6 . However, recent studies are challenging this view [7][8][9][10] . An improved understanding of the ability of ECM fungi to decompose lignocellulose is needed to resolve mechanisms of nutrient cycling in forests.…”

“…Gene tree-species tree reconciliations of LPMOs and other decay-related CAZymes suggest that parallel losses of brown-rot saprotrophy have occurred in the three ECM lineages in Boletales (Boletineae, Suillineae and Sclerodermatineae; Supplementary Figs. 15-23), although the ability to oxidize organic matter remains in Paxillus involutus 9 .…”

Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes

“…The most abundant CAZyme family acting on the plant cell wall in the genome of L. bicolor is LPMO (7). P. involutus has a unique enzymatic system, similar to that of brown rot fungi, to decompose plant biomass (78,79). Transcriptomic studies of P. involutus have revealed that only one ␤-1,4-endoglucanase (GH9) and two LPMO genes are expressed during growth on plant litter or cellulose (79).…”