Decomposition of soil organic matter by ectomycorrhizal fungi: Mechanisms and consequences for organic nitrogen uptake and soil carbon stabilization

Abstract

A major fraction of nitrogen (N) in boreal forest soils is found in organic forms associated with soil organic matter (SOM) and mineral particles. The capacity of ectomycorrhizal (ECM) fungal symbionts to access this N is debated, considering that these fungi have lost many of the genes for decomposing organic matter that were present in their saprotrophic ancestors. To gain a molecular-level understanding of the N-mining processes in ECM fungi, we developed an experimental approach where the processes of decomposition were studied in parallel with the changes in the structure and properties of the organic matter. We showed that ECM fungi have significant capacities to assimilate organic N associated with SOM and mineral surfaces. The decomposition mechanisms differ between species, reflecting the lignocellulose decomposition mechanisms found in their saprotrophic ancestors. During N-mining, the ECM fungi processed the SOM to a material with increased adsorptive properties to iron oxide mineral particles. Two pathways contributed to these changes: Extracellular modifications of the SOM and secretion of mineral surface reactive metabolites. Some of these metabolites have iron(III)-reducing activities and can participate in extracellular Fenton reactions and redox reactions at iron oxide mineral surfaces. We conclude that the traditional framework for understanding organic N acquisition by ECM fungi from recalcitrant SOM must be extended to a framework that includes how those decomposition activities affect the stabilization and reactivity of mineral-associated SOM. The activity through these complex networks of reactions is decisive for the overall effect of ECM fungal decomposition on nutrients and C-cycling in forest ecosystems.

Functional genomics gives new insights into the ectomycorrhizal degradation of chitin

“…It is widely thought that proteinaceous material (i.e. proteins, peptides, and amino acids) accumulating in SOM are the primary sources of organic N for EcM fungi (Op De Beeck et al ., 2018; Tunlid et al ., 2022). Differentiating protein degraders from nonprotein degraders has been repeatedly proposed (Abuzinadah et al ., 1986; Bending & Read, 1996; Chalot & Brun, 1998; Shah et al ., 2013).…”

“…Notably, it has been depicted that the organic N mining activities of EcM fungi might both reduce (Orwin et al ., 2011; Averill et al ., 2014; Fernandez & Kennedy, 2016) or increase SOM decomposition (Lindahl et al ., 2021; Pellitier et al ., 2021). These discrepancies about the net effect of EcM fungi on SOM stocks are likely related to a contrasted functional diversity within EcM communities regarding organic N acquisition (Lindahl et al ., 2021; Tunlid et al ., 2022). Consequently, identifying the EcM species participating in organic N mining, the decomposed N‐containing molecules, and the associated degradation mechanisms represent a major challenge for improving our knowledge of the fungal drivers of C and nutrient cycling in forest soils (Lindahl & Tunlid, 2015).…”

Heavy Metal Contamination in Soil: Implications for Crop Resilience and Abiotic Stress Management

“…For instance, some bacteria can convert less bioavailable forms of toxic metals/metalloids into more soluble forms that plants can take up [11]. Additionally, producing organic acids during decomposition can lead to the dissolution of metal complexes and increase the concentration of free metal ions in the soil solution [67].…”

“…However, releasing toxic metals/metalloids during organic matter decomposition can also pose risks, such as increased metal leaching to groundwater or uptake by nontarget organisms, which can have ecological and health implications [11,31,67,68].…”

The effects of diverse microbial community structures, driven by arbuscular mycorrhizal fungi inoculation, on carbon release from a paddy field

“…Fungal abundance is generally lower than bacterial abundance in soils; however, fungi play a key role in carbon cycling in terrestrial ecosystems (Juan-Ovejero et al 2020). Fungi have a good capacity to decompose recalcitrant organic matter, but at the same time, their products are resistant and are preferentially protected from decomposition through their interactions with clay minerals or soil aggregates (Klink et al 2022, Tunlid et al 2022.…”