A molecular modeling analysis of polycyclic aromatic hydrocarbon biodegradation by naphthalene dioxygenase

Abstract

A theoretical analysis was performed to examine the role of naphthalene dioxygenase (NDO) enzymes in determining differences in biodegradability and biodegradation rates of two- to four-ring polycyclic aromatic hydrocarbons (PAHs) via oxygenation and desaturation reactions. Investigation of the thermodynamics of PAH biodegradation reactions catalyzed by NDO revealed that enthalpies of reaction can explain reaction patterns or regioselectivity of the enzyme in limited cases. Molecular modeling analysis of the size and shape constraints of PAH-enzyme interactions suggests that PAHs bigger than approximately four rings and compounds with alpha substituents or other structural features contributing to increased width at the end of the substrate near the active site are expected to have binding difficulties. This explains some regioselectivity observations, in that thermodynamically favorable sites on some PAH molecules cannot be positioned correctly to be oxidized at the active site. The enzyme fit analysis also suggests that slower biodegradation rates are expected for compounds with larger widths because of the unique positioning that is required for reaction to occur. An inverse relationship between a molecular descriptor of compound width and previously obtained biodegradation rates suggests that this descriptor may be valuable for predicting relative biodegradation rates of PAHs with dioxygenases other than NDO.

Multisubstrate kinetics of PAH mixture biodegradation: analysis in the double-logarithmic plot

“…1). It is in agreement with conclusions from the study (Wammer and Peters 2006) showing that the rate of hydrocarbon oxidation by naphthalene oxygenase is determined mainly by the structure but not thermodynamic characteristics of a substrate.…”

Substrate Specificity and Structural Characteristics of the Novel Rieske Nonheme Iron Aromatic Ring-Hydroxylating Oxygenases NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1

“…When the sizes of the aromatic substrates were examined with respect to the active sites of the enzymes, the dimensions of active sites seemed least likely to be problematic from the standpoint of fit. In the case of fluoranthene, which has the van der Waals dimensions 11.4 Å (length) by 9.5 Å (width) by 3.8 Å (thickness) (33), the substrate-binding pocket of NidA3, with the approximate dimensions of 16 Å by 10 Å by 17 Å, satisfies the spatial requirement for the acceptance of fluoranthene (Fig. 5b and Table 3).…”

Root Exudation: The Ecological Driver of Hydrocarbon Rhizoremediation

“…C2,3O is carried by the TOL plasmid of Pseudomonas putida mt-2 (ATCC 23973) and the bacterium degrades m-xylene to CO 2 , acetate, acetaldehyde, and pyruvate. On the other hand, biodegradation pathways of aromatic hydrocarbon by bacteria are initiated by aromatic hydrocarbon dioxygenases [292]. The three-component naphthalene dioxygenase enzyme system catalyzes the first step in the aerobic degradation of naphthalene by Pseudomonas sp.…”

“…The three-component naphthalene dioxygenase enzyme system catalyzes the first step in the aerobic degradation of naphthalene by Pseudomonas sp. strain NCIB 9816-4 [293,294]: naphthalene + NADH + H + + O 2 Ø (1R,2S)-1,2-dihydronaphthalene-1,2-diol + NAD + [292]. C2,3O and nahAc genes are commonly found on the same plasmid [228] with C2,3O often present in multiple copies [295,296].…”