A widespread mechanism in ectomycorrhizal fungi to access nitrogen from mineral‐associated proteins

Abstract

A large fraction of nitrogen (N) in forest soils is present in mineral-associated proteinaceous compounds. The strong association between proteins and minerals limits microbial accessibility to this source, which is a relatively stable reservoir of soil N. We have shown that the ectomycorrhizal (ECM) fungus Paxillus involutus can acquire N from iron oxide-associated proteins. Using tightly controlled isotopic, spectroscopic and chromatographic experiments, we demonstrated that the capacity to access N from iron oxide-associated bovine serum albumin (BSA) is shared with the ECM fungi Hebeloma cylindrosporum and Piloderma olivaceum. Despite differences in evolutionary history, growth rates, exploration types and the decomposition mechanisms of organic matter, their N acquisition mechanisms were similar to those described for P. involutus. The fungi released N from mineralassociated BSA by direct action of extracellular aspartic proteases on the mineral-associated BSA, without initial desorption of the protein. Hydrolysis was suppressed by the adsorption of proteases to minerals, but this adverse effect was counteracted by the secretion of compounds that conditioned the mineral surface. These data suggest that the enzymatic exudate-driven mechanism to access N from mineral-associated proteins is found in ECM fungi of multiple lineages and exploration types.

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

“…A recent discovery is the large capacity of ECM fungi with diverse evolutionary origins to reductively dissolve iron minerals (Wang et al, 2020(Wang et al, , 2021. The mechanisms of these electron-transfer reactions are not known, but in agreement with mechanisms identified in iron-reducing bacteria (Glasser et al, 2017), we hypothesize that electrons are transferred from the cell to the mineral surface by small, secreted molecules, i.e., extracellular electron shuttles (EESs).…”

“…Accordingly, mineralassociated proteins are rarely considered as bioavailable N for soil microorganisms (Jilling et al, 2018). This assumption is challenged by recent results showing that the ECM fungi P. involutus, Hebeloma cylindrosporium, and Piloderma olivaceum assimilate N from iron mineral-associated proteins by hydrolyzing the protein directly at the mineral surface without initial desorption (Wang et al, 2020(Wang et al, , 2021. This proteolytic surface activity was moderated by the secretion of low-molecular-weight metabolites that conditioned the mineral surface and thereby facilitated proteolysis.…”

“…This proteolytic surface activity was moderated by the secretion of low-molecular-weight metabolites that conditioned the mineral surface and thereby facilitated proteolysis. The chemical structures of these metabolites have not been characterized in detail, but IR spectroscopy indicated a chemical diversity that differed between ECM fungal species (Wang et al, 2020(Wang et al, , 2021.…”

Peat loss collocates with a threshold in plant–mycorrhizal associations in drained peatlands encroached by trees

“…The coniferous trees that typically encroach drained, acidic peatlands associate with ectomycorrhizal (EcM) fungi. Unlike ErM fungi, some EcM taxa have retained the ability to decay complex organic compounds using class II peroxidases (B€ odeker et al, 2009;Kohler et al, 2015;Lindahl & Tunlid, 2015;Shah et al, 2016), presumably to access nitrogen bound in soil organic matter (N-SOM;Nicol as et al, 2019;T. Wang et al, 2021).…”

“…The coniferous trees that typically encroach drained, acidic peatlands associate with ectomycorrhizal (EcM) fungi. Unlike ErM fungi, some EcM taxa have retained the ability to decay complex organic compounds using class II peroxidases (Bödeker et al ., 2009; Kohler et al ., 2015; Lindahl & Tunlid, 2015; Shah et al ., 2016), presumably to access nitrogen bound in soil organic matter (N‐SOM; Nicolás et al ., 2019; Pellitier & Zak, 2021; T. Wang et al ., 2021). These peroxidases have some of the greatest known capacity to decay soil organic matter (Janusz et al ., 2017) and are necessary to access N‐SOM because, in Sphagnum peatlands, polypeptides are rapidly complexed into protein‐polyphenol complexes that are largely protected from hydrolytic enzymes (Bragazza & Freeman, 2007).…”