Detection of naphthenic acid uptake into root and shoot tissues indicates a direct role for plants in the remediation of oil sands process-affected water

Bitumen extraction from surface-mined oil sands deposits results in the accumulation of large volumes of oil sands process-affected water (OSPW). Naphthenic acids (NAs) are primary contributors to OSPW toxicity and have been a focal point for the development of OSPW remediation strategies. Phytoremediation is an approach that utilizes plants and their associated microbes to remediate contaminants from soil and groundwater. While previous evidence has indicated a role for phytoremediation in OSPW treatment through the transformation and degradation of NAs, there are no reports that demonstrate the direct uptake of NAs into plant tissue. Using NAs labelled with ¹⁴C radioisotopes (¹⁴C-NAs) paired with whole-plant autoradiography, we show that NAs representing aliphatic (linear), single-ring, and diamondoid compounds were effectively removed from hydroponic solution and OSPW-treated soil by sandbar willow (Salix interior) and slender wheatgrass (Elymus trachycaulus) and their associated microbiomes. The NA-derived ¹⁴C label accumulated in root and shoot tissues of both plant species and was concentrated in vascular tissue and rapidly growing sink tissues, indicating that ¹⁴C-NAs or their metabolic derivatives were incorporated into physiological processes within the plants. Slender wheatgrass seedlings grown under axenic (sterile) hydroponic and soil conditions also effectively removed all ¹⁴C-NAs, including a highly stable diamondoid NA, demonstrating that plants can directly take up simple and complex NAs without the assistance of microbes. Furthermore, root and shoot tissue fractionation into major biomolecule groups suggests that NA-derived carbon is allocated toward biomolecule synthesis rapidly after NA treatment. These findings provide evidence of plant-mediated uptake of NAs and support a direct role for plants and their associated microbes in the development of future large-scale OSPW phytoremediation strategies.