Creation of metal-complexing agents, reduction of manganese dioxide, and promotion of manganese peroxidase-mediated Mn(III) production by cellobiose:quinone oxidoreductase from Trametes versicolor.

B.P Roy,M.G Paice,F.S Archibald,S.K Misra,L.E Misiak

doi:10.1016/s0021-9258(17)32084-7

Abstract

Culture supernatants of the white-rot fungus Trametes versicolor were found to contain Mn(III)-complexing agents able to effectively promote manganese-dependent peroxidase (MnP)-mediated oxidation of phenol red. The high molecular weight fractions of these supernatants contained carbohydrate polymers that functioned as effective Mn(III)-complexing agents. Gluconic and glucuronic acids were also found to be effective Mn(III)-complexing ligands capable of supporting MnP-mediated phenol red oxidation, as was the cellobionic acid formed from cellobiose by cellobiose:quinone oxidoreductase (CBQase) (EC 1.1.5.1). The formation of cellulose-derived sugar acid manganese-complexing agents by CBQase increased in the presence of wood pulp and cellulolytic enzymes. CBQase, while oxidizing cellobiose, reduced insoluble Mn(IV)O2 to Mn(II) or Mn(III) by a reaction whose rate is determined by the nature of the manganese-complexing agents present. A model is proposed to explain how oxidation of carbohydrate and reduction of MnO2 and quinones by CBQase may complement oxidation by MnP, thus promoting lignin biodegradation.

Highlights

Culture supernatants tohfe white-rot funguns umetes known, it habseen suggested that cel1obiose:quinone uersicolor werefound to containMn(II1)-complexing oxidoreductase (CBQase)’ may be important [3,4,5,6,7,8]
Gluconic andglucu- the manganese-dependentperoxidases (MnP),oxidize Mn(1I)to ronic acids were found to be effective Mn(II1)-com- Mn(II1)when appropriate Mn(II1)-complexingagents arepresplexing ligandscapable of supportingMnP-mediated phenol red oxidationa,s was the cellobionic acid formed from cellobiose bycel1obiose:quinoneoxidoreductase (CBQase)(EC 1.1.5.1).“he formation ocfellulose-derived sugar acid manganese-complexingagentsby CBQaseincreased in the presence of wood pulp and cellulolytic ent
Since only the tion of the high molecular weight (HMW) manganese-complexing material from I: uer- soluble fraction (-4% with CBQase and 15%with CBQase and sicolor cultures, and this HMW material could function as a cellulase) ofthe incubation mixture was usedin themanganesemanganese-complexing agent for MnP activity, we thought that complexing assay, the total number of potential manganesesimple sugar acids might be effective Mn(II1)-complexing complexing sites formed by CBQase and the consequent imagents

Summary

RESULTS

T versicolor Extracellular Manganese-complexing ActivityTo measure potentialmanganese-complexing agents inligninolytic cultures of T versicolor, a MnP assayfollowing phenol red oxidation was used [17, 26, 27]. Comparing the manganesecomplexing efficiencies of crude culture supernatant fractions indicated (Table I) that, with constantaddedMnP activity, CBQase, Manganese-compleAxginegnts, and M n

HWKP alone Controld

Glucoisosaccharinic acid

AA min"

DISCUSSION

CELLULASE CELLULOSE