Synthetic Oxalate/ß-glucan Fungal Extracellular Matrix Demonstrates Potential Inhibition of Extracellular Enzyme Diffusion into Wood Cell Walls, and Calls into Question the Role of Enzymes in Wood Decay
IRG/WP 25-11053
B Goodell, G A Tompsett, G Perez-Gonzalez, K Mastalerz, M Timko
ß-glucan is the major component of the extracellular matrix (ECM) of many fungi, including wood degrading fungi. Many of these species also secrete oxalate into the ECM. Our research demonstrates that ß-glucan forms a novel, previously unreported, hydrogel at room temperature with oxalate. This finding better explains the gel-like nature of the fungal ECM. Oxalate, at relatively low levels, was found to alter the rheometric properties of the ß-glucan hydrogels and modelling showed that the ß-glucan hydrogen bonds with oxalate in a non-covalent matrix to allow formation of that relatively stiff extracellular gel matrix. Changing the oxalate concentration of the ß-glucan/oxalate matrix also impacted the diffusion of a high molecular weight protein, that simulated extracellular enzymes, through the gels. This finding has relevance to the diffusion of extracellular enzymes into substrates such as wood during fungal wood decay, and the synthetic model helps to explain why some types of wood decay fungi such as brown rot fungi, rely on non-enzymatic degradation schemes for carbon cycling and in the decay of wood structures. We suggest that under some conditions of relatively low oxalate concentration in the ECM, the diffusion of extracellular enzymes would virtually stop, thus preventing the movement of those enzymes into the wood cell wall. This research also has potential impact on the diffusion of metabolites in association with pathogenic/biomedical fungi in that some pharmacological anti-microbial compounds are relatively large at the molecular level. What this means is that the fungal extracellular matrix may inhibit the passage of these anti-microbial compounds into the fungus, preventing useful prophylactic or curative activity. By enacting strategies that could alter the secretion of oxalate by fungi (and potentially also in other microorganisms such as bacteria), the rheometric and diffusional properties of the ECM could potentially be altered, and this strategy could be used to alter (stop or control) wood decay, but conversely could also be used to make fungi more susceptible to drug treatments with antifungal compounds in the medical realm. Discussion is provided on how wood treatment to alter the ECM could provide novel strategies for the development of new wood preservatives.
Portions of this research have previously been published in the Peer Reviewed Journal, iScience. document: https://doi.org/10.1016/j.isci.2023.106851.