Stimulation of Mn peroxidase activity: a possible role for oxalate in lignin biodegradation.

Abstract

Oxalate is produced by numerous wooddegrading fungi. Our studies here show that the white-rot fungus Phanerochaete chrysosponum produces extracellular oxalate under conditions that induce synthesis of the ligninolytic system. Little or no oxalate was detected in cultures grown under high nutrient nitrogen or carbon. This extracellular oxalate was identified and quantitated by HPLC. Its identity was further substantiated by its decomposition by the enzyme oxalate oxidase. The oxalate content of the extracellular fluid (peaking at 60 ,M) paralleled the extracellular activity of the lignin-degrading enzyme, Mn peroxidase. Significantly, we demonstrated that oxalate, at physiological concentrations, substantially stimulated Mn peroxidase-catalyzed phenol red oxidation, presumably by its ability to chelate Mn. Stopped flow studies also indicate that oxalate accelerates the turnover of Mn peroxidase. Furthermore, we discovered that oxalate can support Mn peroxidase-catalyzed oxidations in the absence of exogenous H202 and in the presence of dioxygen. These results allow us to propose an important role for oxalate, a ubiquitous compound produced by wood-destroying fungi, in lignin biodegradation.

Experimental calcium-oxalate crystal production and dissolution by selected wood-rot fungi

“…By contrast, the enzymatic degradative system of white-rot fungi has an optimal pH action much higher (pH around 3e4,5, and exceptionally 5; Westermark and Ericksson, 1974;Hatakka, 1994;Swamy and Ramsay, 1999), and thus enzymatic rather than abiotic degradation could be favored. In the process of lignin degradation by white-rot fungi, degradation of oxalate by the oxalate decarboxylase (Micales, 1997;Watanabe et al, 2003) or the oxalate oxidase (Dutton and Evans, 1996) could degrade oxalate as a source of H 2 O 2 that can be utilized afterwards as an oxidant by lignin or manganese peroxidase (for example see Kuan and Tien, 1993). In addition, the activity of an intracellular oxalate decarboxylase has been shown in at least four species of white-rot fungi (Dichomitus squalens, Phanerochaete sanguinea, Trametes ochracea, and T. versicolor), which was also tentatively assigned to a role in the production of important intermediates in the degradation of lignin (Makela et al, 2002).…”

High-Resolution Crystal Structure of Manganese Peroxidase: Substrate and Inhibitor Complexes,

“…Whether a Mn II -chelator complex binds to the enzyme to form a ternary complex or the chelator simply facilitates release of Mn III via ligand displacement has not been completely resolved. However, the crystal structure of MnPMn II in the absence of chelators suggests that the later alternative is more likely (14,16,27,30,31).…”

Formation of a Bis(histidyl) Heme Iron Complex in Manganese Peroxidase at High pH and Restoration of the Native Enzyme Structure by Calcium

“…The released Mn 3+ is stabilized by organic acid chelators, such as oxalate and malonate, which are secreted by the fungus (16,17). The Mn 3+ -chelator complex is capable of diffusing from the enzyme to oxidize terminal substrates including lignin substructures, phenolic compounds, and pollutants (2, 3 and references therein, 18).…”