Microbial biodegradation of aromatic alkanoic naphthenic acids is affected by the degree of alkyl side chain branching

Abstract

Naphthenic acids (NAs) occur naturally in oil sands and enter the environment through natural and anthropogenic processes. NAs comprise toxic carboxylic acids that are difficult to degrade. Information on NA biodegradation mechanisms is limited, and there are no studies on alkyl branched aromatic alkanoic acid biodegradation, despite their contribution to NA toxicity and recalcitrance. Increased alkyl side chain branching has been proposed to explain NA recalcitrance. Using soil enrichments, we examined the biodegradation of four aromatic alkanoic acid isomers that differed in alkyl side chain branching: (4 0 -n-butylphenyl)-4-butanoic acid (n-BPBA, least branched); (4 0 -iso-butylphenyl)-4-butanoic acid (iso-BPBA); (4 0 -sec-butylphenyl)-4-butanoic acid (sec-BPBA) and (4 0 -tert-butylphenyl)-4-butanoic acid (tert-BPBA, most branched). n-BPBA was completely metabolized within 49 days. Mass spectral analysis confirmed that the more branched isomers iso-, sec-and tert-BPBA were transformed to their butylphenylethanoic acid (BPEA) counterparts at 14 days. The BPEA metabolites were generally less toxic than BPBAs as determined by Microtox assay. n-BPEA was further transformed to a diacid, showing that carboxylation of the alkyl side chain occurred. In each case, biodegradation of the carboxyl side chain proceeded through betaoxidation, which depended on the degree of alkyl side chain branching, and a BPBA degradation pathway is proposed. Comparison of 16S rRNA gene sequences at days 0 and 49 showed an increase and high abundance at day 49 of Pseudomonas (sec-BPBA), Burkholderia (n-, iso-, tert-BPBA) and Sphingomonas (n-, sec-BPBA).

Next-Generation Sequencing of Microbial Communities in the Athabasca River and Its Tributaries in Relation to Oil Sands Mining Activities

“…Another genus positively correlated with NA concentration was Achromobacter, which is a strict aerobe. This observation is in line with observations from other studies showing that species from this genus are capable of NA degradation (2,3,19). The strongest positive correlation observed for Archaea, however, was between the methanogen genus (strict anaerobe) Methanobrevibacter (Methanobacteriales) and NAs, TPHs, TSHs, and TAHs.…”

Occurrences and Behaviors of Naphthenic Acids in a Petroleum Refinery Wastewater Treatment Plant

“…This conclusion is consistent with the results of microbial biodegradation of individual aromatic alkanoic NAs. 30,33 Furthermore, estrogenic activities in wastewater from different treatment units were determined, since the aromatic NA fraction was reported to have an estrogenic effect. 31,32 Estrogenic activities were not observed in the sample extracts possibly due to the low concentrations of NA mixtures, but antiestrogenic activities were found in wastewater from physicochemical treatment units with ER antagonist potency ranging from 750 to 2100 ng Tamoxifen/L (Figure 4 and SI Figure S5).…”

Aerobic Biofilms Grown from Athabasca Watershed Sediments Are Inhibited by Increasing Concentrations of Bituminous Compounds

“…However, when directly confronted with aromatic compounds, bacteria appeared to be more sensitive, with half-maximal effective concentrations (EC 50 ) of luminescent bacterial assays for different PAHs ranging from 0.53 to 24.39 ppm (g ml Ϫ1 ) (21,22). In contrast, the EC 50 of naphthenic acids in luminescent bacterial assays was reported to range from 41.9 to 64.9 ppm (mg liter Ϫ1 ) (14), and even the more toxic aromatic alkanoic naphthenic acids and their degradation products had EC 50 s ranging from 9.4 to 69.2 ppm (mg liter Ϫ1 ) (13). In the current study, NAs were measured as a class using liquid chromatography-tandem mass spectrometry and no species identification data are available, but the concentrations estimated in the reactors (Յ0.2 ppm, assuming a complete dissolution in the recirculated water) are considerably lower than those reported in the toxicological tests described above.…”

“…Although some bacteria can metabolize them (11)(12)(13), naphthenic acids can have negative effects on bacteria (14,15), algae (16,17), and cyanobacteria (18). Aromatic hydrocarbons are also known to be toxic to a variety of microbial processes (19,20) and to bacteria (21,22).…”