Microbial degradation of contaminants of emerging concern: metabolic, genetic and omics insights for enhanced bioremediation

Abstract

The perpetual release of natural/synthetic pollutants into the environment poses major risks to ecological balance and human health. Amongst these, contaminants of emerging concern (CECs) are characterized by their recent introduction/detection in various niches, thereby causing significant hazards and necessitating their removal. Pharmaceuticals, plasticizers, cyanotoxins and emerging pesticides are major groups of CECs that are highly toxic and found to occur in various compartments of the biosphere. The sources of these compounds can be multipartite including industrial discharge, improper disposal, excretion of unmetabolized residues, eutrophication etc., while their fate and persistence are determined by factors such as physico-chemical properties, environmental conditions, biodegradability and hydrological factors. The resultant exposure of these compounds to microbiota has imposed a selection pressure and resulted in evolution of metabolic pathways for their biotransformation and/or utilization as sole source of carbon and energy. Such microbial degradation phenotype can be exploited to clean-up CECs from the environment, offering a cost-effective and eco-friendly alternative to abiotic methods of removal, thereby mitigating their toxicity. However, efficient bioprocess development for bioremediation strategies requires extensive understanding of individual components such as pathway gene clusters, proteins/enzymes, metabolites and associated regulatory mechanisms. "Omics" and "Meta-omics" techniques aid in providing crucial insights into the complex interactions and functions of these components as well as microbial community, enabling more effective and targeted bioremediation. Aside from natural isolates, metabolic engineering approaches employ the application of genetic engineering to enhance metabolic diversity and degradation rates. The integration of omics data will further aid in developing systemic-level bioremediation and metabolic engineering strategies, thereby optimising the clean-up process. This review describes bacterial catabolic pathways, genetics, and application of omics and metabolic engineering for bioremediation of four major groups of CECs: pharmaceuticals, plasticizers, cyanotoxins, and emerging pesticides.

Keywords: biodegradation; cyanotoxins; metabolic engineering; metabolic pathways; omics; pesticides; pharmaceuticals; plasticizers.

FIGURE 1

Bacterial degradation pathways of sulfonamide antibiotics: (A) sulfamethazine (B) sulfamethoxazole (C) sulfadiazine and (D) sulfamethoxydiazine. Gene encoding of the respective enzymes are indicated in parenthesis. Enzyme abbreviations: FDMO, flavin-dependent monoxygenase; BR, 1,4-benzoquinone reductase; DSMO, dimethylsulfone monoxygenase. Question mark indicates enzyme catalysing reaction not known.

FIGURE 2

Bacterial degradation pathways of penicillin. Gene encoding of the respective enzymes are indicated in parenthesis. Multiple arrows indicate multiple metabolic steps. Enzyme abbreviations: BL, beta-lactamase; PA, penicillin acylase; BPAA, benzylpenicilloic acid amidase.

FIGURE 3

Bacterial degradation pathways of (A) erythromycin and (B) ciproflaxacin. Genes encoding of the respective enzymes are indicated in parenthesis. Multiple arrows indicate multiple metabolic steps. Enzyme abbreviations: EH, erythromycin hydrolase; GH, glycoside hydrolase.

FIGURE 4

Bacterial degradation pathways of chloramphenicol. Enzyme abbreviations: MO, multifunctional oxidase; CAT, chloramphenicol O-acetyltransferase type B; NR, nitroreductase; DH, haloacid or haloalkane dehalogenase. Gene encoding of the respective enzymes are indicated in parenthesis. Multiple arrows indicate multiple metabolic steps.

FIGURE 5

Bacterial degradation pathways of analgesics (A) ibuprofen (B) acetaminophen and (C) naproxen. Genes encoding respective enzymes are indicated in parenthesis. Multiple arrows indicate multiple metabolic steps. Enzyme abbreviations: THIDO, trihydroxyibuprofen dioxygenase; AM, aliphatic monoxygenase; ACS/T, acyl-CoA synthase/thiolase; HQMO, 1,4-hydroquinone monoxygenase; HQDO, hydroxyquinol-1,2-dioxygenase; ICL, ibuprofen CoA ligase; ICDO, ibuprofen-CoA dioxygenase; TL, thiolase; IBCDO, isobutylcatechol dioxygenase; DH, dehydrogenase; TT, tautomerase; DC, decarboxylase; HT, hydratase; AA, M20 aminoacylase family aminohydrolase; AH, aminohydrolase or guanidine deaminase; HBMO, 4-hydroxybenzoate 3-monoxygenase; HPDO, hydroxyquinol dioxygenase or 4-hydroxyphenylpyruvate dioxygenase; TDDM, tetrahydrofolate-dependent O-demethylase; NDO, naphthalene dioxygenase; PMO, phenol monoxygenase; GDO, gentisate dioxygenase; C12DO, catechol-1,2-dioxygenase.

FIGURE 6

Bacterial degradation pathways of testosterone and oestrone. Genes encoding respective enzymes are indicated in parenthesis. Multiple arrows indicate multiple metabolic steps. Enzyme abbreviations: HSDH, 17β-oestradiol dehydrogenase; OH, oestrone 4-hydroxylase; HODO, 4-hydroxyestrone 4,5-dioxygenase; OAOR, 2-oxoacid oxidoreductase; HSDH, hydroxysteroid dehydrogenase; KSDH, ketosteroid dehydrogenase; KSH, 3-ketosteroid 9α-hydroxylase; HSAMO, 3-hydroxy-9,10-secoandrosta-1,3,5 (10)-triene-9,17-dione hydroxylase; DHSADO, 3,4-dihydroxy-9,10-secoandrosta-1,3,5 (10)-triene-9,17-dione dioxygenase; DSHAH, 4,5–9,10-diseco-3-hydroxy-5,9,17-trioxoandrosta-1 (10),2-dien-4-oic acid hydrolase; HY, (2Z,4Z)−2-hydroxyhexa-2,4-dienoic acid hydratase; AL, aldolase; DH, acetoaldehyde dehydrogenase.

FIGURE 7

Bacterial degradation pathways of (A) fluoxetine and (B) metformin. Genes encoding respective enzymes are indicated in parenthesis. Multiple arrows indicate multiple metabolic steps. Enzyme abbreviations: MH, metformin hydrolase; GH, guanylurea hydrolase; GC, guanidine carboxylase; CD, carboxyguanidine deaminase; AH, allophanate hydrolase; NMG pathway, N-methylglutamate pathway.

FIGURE 8

Bacterial degradation pathway of microcystin-LR. Gene encoding of the respective enzymes are indicated in parenthesis. The primary, secondary and tertiary cleavage sites (and corresponding metabolic steps) are indicated numerically in circles. Multiple arrows indicate multiple metabolic steps.

FIGURE 9

Bacterial degradation pathways of plasticizers: di (2-ethylhexyl) phthalate, dibutyl phthalate, benzyl butyl phthalate and di-n-octyl phthalate. Genes encoding respective enzymes are indicated in parenthesis. Multiple arrows indicate multiple metabolic steps. Enzyme abbreviations: 0132MO, 0132 Monooxygenase; EstG2, Esterase G2; EstG3, Esterase G3; EstG5, Esterase G5; Peh, phthalate ester hydrolase A; MehpH, mono ethylhexyl phthalate hydrolase; Est2518, Esterase 2,518; EstB4375, Esterase B4375; Cut0019, Esterase cut0019; 34DHPDO, 3,4-dihydroxyphthalate dioxygenase; 45DHPDO, 4,5-dihydroxyphthalate dioxygenase; 34DHPDC, 3,4-dihydroxyphthalate decarboxylase; 45DHPDC, 4,5-dihydroxyphthalate decarboxylase; S5H, salicylate-5-hydroxylase; BDO, benzoate dioxygenase.

FIGURE 10

Metabolic pathways for degradation of various pesticides of emerging concern in bacteria. Genes encoding respective enzymes are indicated in parenthesis. Enzyme abbreviations: CPL, C-P lyase; GOR, Glyphosate oxydoreductase; ATT, AMPA aminotransferase; SO, Sarcosine oxidase; PN, Phosphonatase; MAD, methyl amine dehydrogenase; ADO, Aniline dioxygenase; C12DO, Catechol-1,2-dioxygenase; AH, amide hydrolase; CH, Carbendazim hydrolase; ABH, 2-Aminobenzimidazole hydrolase; BMO, 2-Hydrobenzimidazole monooxygenase; B12DO, Benzoate-1,2-dioxygenase; MO, monooxygenase; AO, Aldehyde oxidase; HL, Hydrolase; CNACH, 6-Chloronicotinic acid chlorohydrolase; OPH, Organophosphate hydrolase; PTE, Phosphotriesterase.