Microbial Degradation of Naphthalene and Substituted Naphthalenes: Metabolic Diversity and Genomic Insight for Bioremediation

Abstract

Low molecular weight polycyclic aromatic hydrocarbons (PAHs) like naphthalene and substituted naphthalenes (methylnaphthalene, naphthoic acids, 1-naphthyl N-methylcarbamate, etc.) are used in various industries and exhibit genotoxic, mutagenic, and/or carcinogenic effects on living organisms. These synthetic organic compounds (SOCs) or xenobiotics are considered as priority pollutants that pose a critical environmental and public health concern worldwide. The extent of anthropogenic activities like emissions from coal gasification, petroleum refining, motor vehicle exhaust, and agricultural applications determine the concentration, fate, and transport of these ubiquitous and recalcitrant compounds. Besides physicochemical methods for cleanup/removal, a green and eco-friendly technology like bioremediation, using microbes with the ability to degrade SOCs completely or convert to non-toxic by-products, has been a safe, cost-effective, and promising alternative. Various bacterial species from soil flora belonging to Proteobacteria (Pseudomonas, Pseudoxanthomonas, Comamonas, Burkholderia, and Novosphingobium), Firmicutes (Bacillus and Paenibacillus), and Actinobacteria (Rhodococcus and Arthrobacter) displayed the ability to degrade various SOCs. Metabolic studies, genomic and metagenomics analyses have aided our understanding of the catabolic complexity and diversity present in these simple life forms which can be further applied for efficient biodegradation. The prolonged persistence of PAHs has led to the evolution of new degradative phenotypes through horizontal gene transfer using genetic elements like plasmids, transposons, phages, genomic islands, and integrative conjugative elements. Systems biology and genetic engineering of either specific isolates or mock community (consortia) might achieve complete, rapid, and efficient bioremediation of these PAHs through synergistic actions. In this review, we highlight various metabolic routes and diversity, genetic makeup and diversity, and cellular responses/adaptations by naphthalene and substituted naphthalene-degrading bacteria. This will provide insights into the ecological aspects of field application and strain optimization for efficient bioremediation.

Keywords: biodegradation; bioremediation; cellular responses and evolution; gene transfer mechanisms; genetic diversity; metabolic pathways; naphthalene; substituted naphthalenes.

FIGURE 1

Sources and routes for entry of low molecular weight polycyclic aromatic hydrocarbons through various ecological compartments and various factors affecting biota. Dotted lines indicate the interaction among various compartments of the ecosystem.

FIGURE 2

Taxonomic diversity and ecological distribution of bacterial members from the environment contaminated with naphthalene and naphthalene derivatives.

FIGURE 3

Pathways for the degradation of naphthalene, methylnaphthalenes, naphthoic acid, and Carbaryl. Numbers within circles represent enzymes responsible for sequential conversion of naphthalene and its derivatives to its subsequent products. 1, Naphthalene dioxygenase (NDO); 2, cis-dihydrodiol dehydrogenase; 3, 1,2-dihydroxynaphthalene dioxygenase; 4, 2-hydroxychromene-2-carboxylate isomerase; 5, trans-O-hydroxybenzylidene pyruvate hydratase-aldolase; 6, salicylaldehyde dehydrogenase; 7, salicylate 1-hydroxylase; 8, catechol 2,3-dioxygenase (C23DO); 9, 2-hydroxymuconic semialdehyde dehydrogenase; 10, 2-oxopent-4-enoate hydratase; 11, 4-hydroxy-2-oxovalerate aldolase; 12, acetaldehyde dehydrogenase; 13, catechol 1,2-dioxygenase (C12DO); 14, muconate cycloisomerase; 15, muconolactone delta-isomerase; 16, β-ketoadipate enol-lactone hydrolase; 17, β-ketoadipate succinyl-CoA transferase; 18, β-ketoadipyl-CoA thiolase; 19, succinyl-CoA:acetyl-CoA succinyl transferase; 20, salicylate 5-hydroxylase; 21, gentisate 1,2-dioxygenase (GDO); 22, maleylpyruvate isomerase; 23, fumarylpyruvate hydrolase; 24, methylnaphthalene hydroxylase (NDO); 25, hydroxymethylnaphthalene dehydrogenase; 26, naphthaldehyde dehydrogenase; 27, 3-formylsalicylate oxidase; 28, hydroxyisophthalate decarboxylase; 29, carbaryl hydrolase (CH); 30, 1-naphthol 2-hydroxylase.

FIGURE 4

Metabolic pathway for the degradation of naphthalene sulfonates. Numbers within circles represent enzymes responsible for the metabolism of naphthalene sulfonates and are similar/the same as described in Figure 3.

FIGURE 5

The genetic organization and diversity observed in the degradation of naphthalene in bacterial members; (A) naphthalene upper pathway, naphthalene to salicylate metabolism; (B) naphthalene lower pathway, salicylate to central carbon pathway via catechol; and (C) salicylate to central carbon pathway via gentisate.

FIGURE 6

The genetic organization involved in the degradation of Carbaryl by Pseudomonas sp. C5pp.

FIGURE 7

Different cellular response strategies of an ideal aromatic degrading bacterium for efficient biodegradation of xenobiotic pollutants.

FIGURE 8

Schematic diagram showing various bioremediation strategies for degradation/cleanup of xenobiotic aromatic pollutants.