Low molecular weight chelators and phenolic compounds isolated from wood decay fungi and their role in the fungal biodegradation of wood

Abstract

A review of information, as well as new research results related to low molecular weight metal chelators isolated from wood decay fungi is presented. Low molecular weight compounds with metal chelating capability have been found to be produced by several white and brown rot wood decay fungi. Phenolate derivative chelators from the brown rot fungus Gloeophyllum trabeum (Gt-chelator) have been isolated by ultrafiltration (<1000 MW) and extraction with ethyl acetate. Selected chelators have been purified via HPLC and structural analysis performed by GC-MS analysis. The chelators isolated have not only a high affinity for the ferric form of iron but importantly, will mediate the reduction of this metal in redox cycling processes at pH values below neutrality. Depending on iron concentration and other environmental parameters, iron may remain bound to the chelator or can be released in the reduced ferrous form. The reduced state of iron can react with oxidants such as hydrogen peroxide where a Fenton type reaction will occur to generate oxygen radicals. The presence of the chelator in wood degraded by G. trabeum has been demonstrated by ELISA and TEM immunolabelling studies. Data are presented on the reduction of iron by Gt-chelator, the generation of oxygen radical species, and the degradation of cellulosic and phenolic compounds mediated by the Gt chelator. Also demonstrated are the `redox cycling' of the chelator as well as one-electron oxidation reactions mediated by the Gt chelator in the presence of Mn or Fe ions and hydrogen peroxide. A reaction scheme is presented and the role of oxalic acid as a phase transfer agent for iron in conjunction with low molecular weight, diffusible chelators in early through advanced stages of wood degradation is discussed. We show that oxalate plays a role in increasing the availability of iron via sequestration from iron (hydr)oxide complexes, allowing the Gt chelators, in a pH dependent reaction, to access this metal from the weak oxalate chelator. Chelators isolated from the brown rot fungus were found to reduce iron or other transition metals and sequester these metals. The chelator has a sufficiently low molecular mass to penetrate into the wood cell wall as shown in previous work. Data are presented showing that reactive oxygen species generated in the presence of the chelator can mediate the degradation of cellulosic and chlorinated phenolic compounds. We hypothesize that the Gt chelator fosters the production of reduced metals within the buffered environment of the wood cell wall and when in proximity to reactive oxygen species, such as hydrogen peroxide or other oxidants (produced in part via oxidation of the catecholate Gt chelators as well as cell wall lignocellulose components in the presence of the chelated metals), will react to form hydroxyl radicals which are capable of depolymerizing and oxidizing lignocellulose compounds. This hypothesis helps to explain the action of brown rot fungi in wood cell wall biodegradation and provides a mechanism to explain how brown rot fungi `control' the production of oxygen radicals, allowing their formation within the wood cell wall where they are effective against lignocellulose components, as opposed to being randomly generated in the extracellular environment around the fungal hyphae.