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J Biol Chem, Vol. 274, Issue 15, 10324-10330, April 9, 1999

Description of a Versatile Peroxidase Involved in the Natural Degradation of Lignin That Has Both Manganese Peroxidase and Lignin Peroxidase Substrate Interaction Sites

From the Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas, Velázquez 144, E-28006 Madrid, Spain

Two major peroxidases are secreted by the fungus Pleurotus eryngii in lignocellulose cultures. One is similar to Phanerochaete chrysosporium manganese-dependent peroxidase. The second protein (PS1), although catalyzing the oxidation of Mn²⁺ to Mn³⁺ by H₂O₂, differs from the above enzymes by its manganese-independent activity enabling it to oxidize substituted phenols and synthetic dyes, as well as the lignin peroxidase (LiP) substrate veratryl alcohol. This is by a mechanism similar to that reported for LiP, as evidenced by p-dimethoxybenzene oxidation yielding benzoquinone. The apparent kinetic constants showed high activity on Mn²⁺, but methoxyhydroquinone was the natural substrate with the highest enzyme affinity (this and other phenolic substrates are not efficiently oxidized by the P. chrysosporium peroxidases). A three-dimensional model was built using crystal models from four fungal peroxidase as templates. The model suggests high structural affinity of this versatile peroxidase with LiP but shows a putative Mn²⁺ binding site near the internal heme propionate, involving Glu³⁶, Glu⁴⁰, and Asp¹⁸¹. A specific substrate interaction site for Mn²⁺ is supported by kinetic data showing noncompetitive inhibition with other peroxidase substrates. Moreover, residues reported as involved in LiP interaction with veratryl alcohol and other aromatic substrates are present in peroxidase PS1 such as His⁸² at the heme-channel opening, which is remarkably similar to that of P. chrysosporium LiP, and Trp¹⁷⁰ at the protein surface. These residues could be involved in two different hypothetical long range electron transfer pathways from substrate (His⁸²-Ala⁸³-Asn⁸⁴-His⁴⁷-heme and Trp¹⁷⁰-Leu¹⁷¹-heme) similar to those postulated for LiP.

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