Diamondoids are not forever: microbial biotransformation of diamondoid carboxylic acids

Abstract

Summary Oil sands process‐affected waters (OSPW) contain persistent, toxic naphthenic acids (NAs), including the abundant yet little‐studied diamondoid carboxylic acids. Therefore, we investigated the aerobic microbial biotransformation of two of the most abundant, chronically toxic and environmentally relevant diamondoid carboxylic acids: adamantane‐1‐carboxylic acid (A1CA) and 3‐ethyl adamantane carboxylic acid (3EA). We inoculated into minimal salts media with diamondoid carboxylic acids as sole carbon and energy source two samples: (i) a surface water sample (designated TPW) collected from a test pit from the Mildred Lake Settling Basin and (ii) a water sample (designated 2 m) collected at a water depth of 2 m from a tailings pond. By day 33, in TPW enrichments, 71% of A1CA and 50% of 3EA was transformed, with 50% reduction in EC20 toxicity. Similar results were found for 2 m enrichments. Biotransformation of A1CA and 3EA resulted in the production of two metabolites, tentatively identified as 2‐hydroxyadamantane‐1‐carboxylic acid and 3‐ethyladamantane‐2‐ol respectively. Accumulation of both metabolites was less than the loss of the parent compound, indicating that they would have continued to be transformed beyond 33 days and not accumulate as dead‐end metabolites. There were shifts in bacterial community composition during biotransformation, with Pseudomonas species, especially P. stutzeri, dominating enrichments irrespective of the diamondoid carboxylic acid. In conclusion, we demonstrated the microbial biotransformation of two diamondoid carboxylic acids, which has potential application for their removal and detoxification from vast OSPW that are a major environmental threat.

Differential protein expression during growth on model and commercial mixtures of naphthenic acids in Pseudomonas fluorescens Pf‐5

“…For example, Johnson et al ( 2011 ) showed that Pseudomonads increased in abundance during the degradation of certain NAs in mixed communities. This is supported by Folwell et al ( 2020 ) who showed that enrichment cultures dominated by Pseudomonads, especially P . stutzeri , degraded diamondoid carboxylic acids (e.g., adamantane‐1‐carboxylic acid (A1CA)), whereas other organisms such as Rhodococcus sp .…”

“…Previous studies have shown that microbial biodegradation decreases OSPW toxicity over time (Frank et al, 2009 ; Johnson et al, 2011 ; Quagraine et al, 2005 ) and the use of microorganisms is a potential remediation strategy for oil sands operators. However, NA biodegradation is affected by chemical structure and the more recalcitrant NAs contain multiple branched alkyl chains and methyl substitution of the cycloalkane rings (Johnson et al, 2012 ; Smith et al, 2008 ), as well as the highly branched and multi‐ringed diamondoid NAs, found in tailings ponds (Ahad et al, 2018 ; Demeter et al, 2015 ; Folwell et al, 2020 ; Paulssen & Gieg, 2019 ). Despite their recalcitrance, several NA‐degrading communities and species have been identified including Pseudomonas putida and Pseudomonas fluorescens (Del Rio et al, 2006 ; Johnson et al, 2013 ).…”

Pros and Cons of Separation, Fractionation and Cleanup for Enhancement of the Quantitative Analysis of Bitumen-Derived Organics in Process-Affected Waters—A Review

“…Effective OSPW detoxification strategies [10][11][12][13][14][15] rely on a thorough understanding of the organic compounds that contribute to toxicity [5,7]. Mass spectrometry (MS) is the most common method of detection for organic compounds in OSPW, with the simplest and least expensive approach being unit mass resolution quadrupole MS. Quadrupoles with unit mass resolution have limited applications due to low resolution.…”