N-Acetylglucosaminidase activity, a functional trait of chitin degradation, is regulated differentially within two orders of ectomycorrhizal fungi: Boletales and Agaricales

Abstract

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.

Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome

“…The production of chitinases among bacteria is ecologically relevant since, apart from pathogenicity (Frederiksen et al, ), they are involved in N mobilization from fungal necromass. On the other hand, ECM fungi can also degrade chitin, but with opposite patterns of regulation between fungal families (Maillard, Didion, Fauchery, Bach, & Buée, ), which could counteract the effects measured at the phylum level in our study. In turn, our results might indicate that different functional groups of microbes can complement each other with positive effects on plant growth (van der Heijden & Hartmann, ).…”

First evidences that the ectomycorrhizal fungus Paxillus involutus mobilizes nitrogen and carbon from saprotrophic fungus necromass

“…In a previous study, Leake and Read (1990) compared the capacity of ericoid and ectomycorrhizal species to degrade crystalline α-chitin, suggesting the ability of P. involutus to use this crustacean's chitin as a source of nitrogen. Nevertheless, P. involutus was much less effective at degrading chitin than ericoid mycorrhizal fungi (Leake and Read, 1990), or than EM Agaricales species (Maillard et al, 2018). Nevertheless, a great variation of chitinases related to nutritional chitin acquisition, competitive interaction, autolysis or cell wall remodelling can be expressed in natural conditions (Kellner and Vandenbol, 2010;Langner and Göhre, 2016).…”

“…Consequently, the use of labelled pure chitin in future studies would allow to prove the degradation of fungal chitin polymers by P. involutus and quantify the proportions of C and N potentially mobilized from this polymer. This potential capacity should be checked also for other EM fungi, since some mycorrhizal groups probably have limited capacity to transform organic matter in comparison to certain lineages (Lindahl and Tunlid, 2015;Maillard et al, 2018).…”

“…Indeed, Leake and Read () have reported potential chitinolytic activities from EM fungi by quantifying the mycelial growth of diverse ericoid and EM fungi with chitin as the sole source of nitrogen. Complementary to these observations, enzymatic approaches confirmed the expression of proteolytic and chitinolytic activities from EM fungal mycelium in presence of saprotrophic fungal necromass, or pure chitin (Hodge et al ., ; Mucha et al ., ; Mucha et al, ; Maillard et al ., ). Moreover, Lindahl and Taylor () reported the frequent occurrence of N‐acetylhexosaminidase‐encoding genes in ectomycorrhizal fungi.…”

“…Therefore, rotting wood could constitute a particular niche for EM fungi involved in a symbiotic interaction with their host-tree roots. More precisely, it was suggested that certain EM fungi colonized dead wood acting as scavengers by degrading wood rot fungi (Buée et al, 2007;Rajala et al, 2012;Mäkipää et al, 2017;Maillard et al, 2018). The abilities of EM fungi to mobilize nutrients from dead organic matter have been suggested in numerous studies (Buée et al, 2005;Courty et al, 2007;Lindahl and Finlay, 2006;Talbot et al, 2013;Vaario et al, 2002).…”