Functional genomics gives new insights into the ectomycorrhizal degradation of chitin

Abstract

Summary Ectomycorrhizal (EcM) fungi play a crucial role in the mineral nitrogen (N) nutrition of their host trees. While it has been proposed that several EcM species also mobilize organic N, studies reporting the EcM ability to degrade N‐containing polymers, such as chitin, remain scarce. Here, we assessed the capacity of a representative collection of 16 EcM species to acquire 15N from 15N‐chitin. In addition, we combined genomics and transcriptomics to identify pathways involved in exogenous chitin degradation between these fungal strains. Boletus edulis, Imleria badia, Suillus luteus, and Hebeloma cylindrosporum efficiently mobilized N from exogenous chitin. EcM genomes primarily contained genes encoding for the direct hydrolysis of chitin. Further, we found a significant relationship between the capacity of EcM fungi to assimilate organic N from chitin and their genomic and transcriptomic potentials for chitin degradation. These findings demonstrate that certain EcM fungal species depolymerize chitin using hydrolytic mechanisms and that endochitinases, but not exochitinases, represent the enzymatic bottleneck of chitin degradation. Finally, this study shows that the degradation of exogenous chitin by EcM fungi might be a key functional trait of nutrient cycling in forests dominated by EcM fungi.

Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems

“…In particular, we highlight the high expression of AA5 (oxidases), GH5_9 (β‐1,3‐glucanases), GH18 (chitinases), GH20 (β‐N‐acetylglucosaminidases), and GH128 (β‐1,3‐glucanases) families within the ectomycorrhizal guild. Moreover, recent studies have confirmed that certain ectomycorrhizal fungal species use GH18 and GH20 to depolymerize chitin by hydrolytic mechanisms and that degradation of FCW, and in particular chitin, by ectomycorrhizal fungi might be a key functional trait of N cycling in forest soil (Lindahl & Taylor, 2004; Maillard et al ., 2023). However, some traits (i.e.…”

“…In addition, a significant fraction of plant C is converted into microbial biomass or other microbial products. During fungal decomposition, necromass is recycled by active soil microorganisms, including other fungi (Maillard et al ., 2023). A better understanding of the processes carried out by different fungal groups can be obtained using metagenomics and metatranscriptomics, which enable the description of in situ functional complementarities and competition between functional guilds.…”

Suillus: an emerging model for the study of ectomycorrhizal ecology and evolution

“…Furthermore, Suillus can act as hosts themselves for a diversity of fungi and bacteria, including related fungi in the genera Gomphidius and Chroogomphus (Olsson et al, 2000;Fig. 1o,p) and bacteria that both associate with living hyphae and mycorrhizas (Izumi et al, 2006;Timonen & Hurek, 2011), and actively decompose dead mycelia (Maillard et al, 2022(Maillard et al, , 2023. Together, these traits offer exciting opportunities to help solve a broad range of ecological and evolutionary questions.…”

“…Protein decomposition appears to be dependent on forest age, with Suillus species in younger forests having lower protein decomposition activity (Rineau et al ., 2016), which could be advantageous given that more mature forests contain higher levels of organic nitrogen. Genomic and functional assays have demonstrated that S. luteus also uses endochitinases to decompose complex chitin polymers (Maillard et al ., 2023). Initial work suggests that in low‐carbon soils, S. salmonicolor ( cothurnatus ), like some other ECM species, can prime decomposition by saprotrophic fungi (Bhatnagar et al ., 2021).…”

The mycorrhizal symbiosis: research frontiers in genomics, ecology, and agricultural application

“…As ancestral ECM lineages shifted toward symbiotic relationships, the need for these degradative enzymes diminished, resulting in their gradual loss over evolutionary time (Martin & Selosse, 2008; Wolfe et al ., 2012; Lebreton et al ., 2021). This makes mycorrhizal fungi dependent on their host plants for C. Nevertheless, many of the sequenced fungi have maintained a unique array of PCWDEs, including endoglucanases and oxidoreductases/laccases, suggesting that several ECM fungi possess diverse abilities to scavenge plant and microbial detritus (necromass) from soil and litter (Bödeker et al ., 2014; Veneault‐Fourrey et al ., 2014; Op De Beeck et al ., 2018; Pellitier & Zak, 2018; Nicolás et al ., 2019; Floudas et al ., 2020; Maillard et al ., 2023). Fine‐tuned regulation of these PCWDE genes is necessary to avoid triggering plant defense responses (Miyauchi et al ., 2020).…”