Oxidative degradation of phenanthrene by the ligninolytic fungus Phanerochaete chrysosporium

Abstract

The ligninolytic fungus Phanerochaete chrysosporium oxidized phenanthrene and phenanthrene-9,10quinone (PQ) at their C-9 and C-10 positions to give a ring-fission product, 2,2'-diphenic acid (DPA), which was identified in chromatographic and isotope dilution experiments. DPA formation from phenanthrene was somewhat greater in low-nitrogen (ligninolytic) cultures than in high-nitrogen (nonligninolytic) cultures and did not occur in uninoculated cultures. The oxidation of PQ to DPA involved both fungal and abiotic mechanisms, was unaffected by the level of nitrogen added, and was significantly faster than the cleavage of phenanthrene to DPA. Phenanthrene-trans-9,10-dihydrodiol, which was previously shown to be the principal phenanthrene metabolite in nonligninolytic P. chrysosporium cultures, was not formed in the ligninolytic cultures employed here. These results suggest that phenanthrene degradation by ligninolytic P. chrysosporium proceeds in order from phenanthrene-PQ-* DPA, involves both ligninolytic and nonligninolytic enzymes, and is not initiated by a classical microsomal cytochrome P-450. The extracellular lignin peroxidases of P. chrysosporium were not able to oxidize phenanthrene in vitro and therefore are also unlikely to catalyze the first step of phenanthrene degradation in vivo. Both phenanthrene and PQ were mineralized to similar extents by the fungus, which supports the intermediacy of PQ in phenanthrene degradation, but both compounds were mineralized significantly less than the structurally related lignin peroxidase substrate pyrene was.

Biodegradation of phenanthrene by Phanerochaete chrysosporium: on the role of lignin peroxidase

“…Phenanthrene; 11, phenanthrene-trons 9,10-dihydrodiol; 111, 9-phenanthrol; IV, phenanthrene-9,lO-quinone; V, Z.Z'-diphenic acid: VI, 2,2'-biphenyldimethanol; VII, 9-phenanthryl-~-u-glucopyranoside. This pathway was adapted from pathways proposed by Sutherland et al (1991) andHammel et al (1992). The oxidation of 0-phenanthrol to form phenanthrene-9,lO-quinone illustrates how the two pathways are linked.…”

“…Figure 5 is a proposed pathway for phenanthrene degradation as it occurs in P. chrysosporium under ligninolytic and nonligninolytic conditions. This pathway incorporates components of the nonligninolytic pathway proposed by Sutherland et al (1991) and shows how it is linked to the ligninolytic pathway proposed by Hammel et al (1992).…”

“…It thus appears reasonable to suggest that, at the onset of idiophase (when cultures become ligninolytic), lignin peroxidases may function to link these two pathways.Phenanthrene and many other polycyclic aromatic hydrocarbons (PAHs) are degraded by the wood rotting basidiomycete Phanerochaete chrysosporium (Bumpus 1989). Experiments using radiolabelled PAHs demonstrate that carbon dioxide is the final oxidation product (Bumpus 1989;Hammel et al 1991Hammel et al , 1992Haemmerli et al 1986; Sanglard et a/. 1986) of many PAHs in this fungus under ligninolytic conditions.…”

“…Although 3-phenanthrol and 4-phenanthrol were produced in these cultures, the major pathway appeared to involve reaction products oxygenated in the C-9 position. In a more recent study (Hammel et al 1992) it was shown that under ligninolytic conditions, phenanthrene was oxidized to the phenanthrene-9,lO-quinone followed by aromatic ring cleavage to form 2,2'diphenic acid. However, lignin peroxidases did not catalyse either of these reactions.In the present study, we showed that 9phenanthrol, a phenanthrene oxidation product formed in nonligninolytic cultures of P. chrysosporium, is oxidized by lignin peroxidase H8 to phenanthrene-9,lO-quinone.…”

Extent of humification of anthracene, fluoranthene, and benzo[α]pyrene byPleurotus ostreatusduring growth in PAH‐contaminated soils

“…Furthermore, the vast majority of the aforementioned work has focused on one single organism (P. chrysosporium); research has only recently begun to examine other species. Liquid-culture degradation of PAHs by white-rot fungi involves conversion to polar organics (quinones and ringcleavage carboxylic acids), aqueous-soluble products and, in some cases, CO 2 (Sanglard et al 1986;Bumpus 1989;Hammel et al 1991;Sutherland et al 1991;Hammel et al 1992). Substantial species-specific variability exists with regard to the nature of products formed during PAH transformations (Field et al 1992;Vyas et al 1994;Bogan and Lamar 1996).…”