Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors

Abstract

Summary Ectomycorrhizal fungi are thought to have a key role in mobilizing organic nitrogen that is trapped in soil organic matter (SOM). However, the extent to which ectomycorrhizal fungi decompose SOM and the mechanism by which they do so remain unclear, considering that they have lost many genes encoding lignocellulose‐degrading enzymes that are present in their saprotrophic ancestors.Spectroscopic analyses and transcriptome profiling were used to examine the mechanisms by which five species of ectomycorrhizal fungi, representing at least four origins of symbiosis, decompose SOM extracted from forest soils.In the presence of glucose and when acquiring nitrogen, all species converted the organic matter in the SOM extract using oxidative mechanisms. The transcriptome expressed during oxidative decomposition has diverged over evolutionary time. Each species expressed a different set of transcripts encoding proteins associated with oxidation of lignocellulose by saprotrophic fungi. The decomposition ‘toolbox’ has diverged through differences in the regulation of orthologous genes, the formation of new genes by gene duplications, and the recruitment of genes from diverse but functionally similar enzyme families.The capacity to oxidize SOM appears to be common among ectomycorrhizal fungi. We propose that the ancestral decay mechanisms used primarily to obtain carbon have been adapted in symbiosis to scavenge nutrients instead.

Chemical changes in organic matter after fungal colonization in a nitrogen fertilized and unfertilized Norway spruce forest

“…Oxidative reactions are used by saprotrophic and ECM fungi in order to get access to nutrients in the OM (Martínez et al 2011;Shah et al 2016). These oxidative reactions include side chain oxidations, which can lead to an increase of carboxyl-C in the OM.…”

“…Unlike saprotrophs, ECM fungi forage the SOM to obtain nutrients such as N and P for the host plant and receive in return plant photosynthate C. Nevertheless, the ability of ECM fungi to produce oxidative enzymes suggests a potential role for these microbes in the decomposition of soil OM (Bödeker et al 2014;Phillips et al 2014). Furthermore, recent studies have shown that ECM fungi have retained similar oxidative capacity as saprotrophic fungi (Shah et al 2016). This oxidative capacity has been suggested to primarily assist the ECM fungi to mobilizing nutrients from soil OM such as N embedded in the soil organic complexes, rather than to obtain C from the soil OM (Lindahl and Tunlid 2015;Shah et al 2016).…”

“…Furthermore, recent studies have shown that ECM fungi have retained similar oxidative capacity as saprotrophic fungi (Shah et al 2016). This oxidative capacity has been suggested to primarily assist the ECM fungi to mobilizing nutrients from soil OM such as N embedded in the soil organic complexes, rather than to obtain C from the soil OM (Lindahl and Tunlid 2015;Shah et al 2016). However, decomposition and chemical changes of OM after ECM colonization are still poorly understood.…”

Molecular and Microscopic Insights into the Formation of Soil Organic Matter in a Red Pine Rhizosphere

“…Although pine naturally exist in a relationship with ectomycorrhizal and saprotrophic fungi which significantly contribute to C cycling by SOM decomposition [56,57], here we focused only on bacteria from the perspective of microbial ecology, to obtain information on the structure and function of the microbial community members that were able to sustain in these humics-free basic conditions.…”

Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees

“…In many temperate forests, both AM and EM trees commonly cooccur despite fundamental differences in nutrient acquisition strategies (19,20). EM fungi are, on the whole, better adapted to acquire nutrients from organic substrates than AM fungi (21,22). Thus, EM trees may exhibit greater dependence on mycorrhizal hyphal foraging than AM trees under conditions where nutrients largely occur in organic forms.…”