Oxidative Cleavage of a Phenolic Diarylpropane Lignin Model Dimer by Manganese Peroxidase from Phanerochaete chrysosporium

In the presence of Mn^II and H₂O₂, homogeneous manganese peroxidase oxidized 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1,3-dihydroxypropane (I) to yield 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1-oxo-3-hydroxypropane (II), 2,6-dimethoxy-1,4-benzoquinone (III), 2,6-dimethoxy-1,4-dihydroxybenzene (IV), 1-(4-methoxyphenyl)-1-oxo-2-hydroxyethane (V), 1-(4-methoxyphenyl)-1,2-dihydroxyethane (VI), syringaldehyde (VIII), and 2-(4-methoxyphenyl)-3-hydroxypropanal (IX). Chemically prepared manganese(III) malonate catalyzed the same reactions. Oxidation of I in H₂¹⁸O under argon resulted in >80% incorporation of ₁₈O into the phenylglycol VI, the hydroquinone IV, and the quinone III. Oxidation of I in H₂¹⁸O under aerobic conditions resulted in 40% incorporation of ₁₈O into VI but no ₁₈O incorporation into V. Finally, oxidation of I under ₁₈O₂ resulted in 89% and 28% incorporation of ₁₈O into V and VI, respectively. These results are explained by mechanisms involving the one-electron oxidation of the substrate I by enzyme-generated Mn^III to produce a phenoxy radical intermediate I'. Subsequent C_α-C_β bond cleavage of the radical intermediate yields syringaldehyde (VIII) and a C₆-C₂ benzylic radical. Syringaldehyde is oxidized by Mn^III in several steps to a cyclohexadiene cation intermediate I'', which is attacked by water to yield the benzoquinone III. The C₆-C₂ radical is scavenged by O₂ to form a peroxy radical that decomposes to V and VI. The C₆-C₂ radical is also oxidized by Mn^III, leading to the formation of VI. Alternatively, the radical I' undergoes subsequent oxidation by Mn^III to yield a cyclohexadiene cation I''. Attack of the cation by water yields a triol that undergoes alkylphenyl cleavage to yield the phenylpropanal IX and the hydroquinone IV. The latter is oxidized by Mn^III to yield the quinone III. Finally, the cation intermediate I'' loses a proton to yield a quinone methide that rearranges to form the diarylpropanone II. In these reactions, Mn^III generated by manganese peroxidase catalyzes both formation of the substrate phenoxy radical and oxidation of carbon-centered radical intermediates, to yield reactive cations.