Uptake and bioaccumulation of perfluoroalkyl acids in edible crops via land-applied biosolids and reclaimed water

Abstract

Perfluoroalkyl acids (PFAAs) are persistent, bioaccumulative, and toxic anthropogenic compounds that are both lipophobic and hydrophobic. This dual nature makes them both oil and water repellent, giving them a myriad of applications (e.g., non-stick packaging, stain-resistant textiles). Due to their widespread use, municipal wastewaters are a collection vehicle for these compounds; however, most conventional wastewater treatment plants (WWTPs) are ineffective at removing PFAAs. Due to their unique nature, these compounds reside in significant quantities in both the aqueous effluent and the treated sludge (i.e., biosolids) of WWTPs. Sustainability movements coupled with growing water scarcity encourage the land application of both biosolids and reclaimed water from WWTPs. However, concerns around these practices have recently arisen, particularly with respect to the potential uptake and subsequent bioaccumulation of PFAAs into food crops. The objective of this study was to understand the factors controlling the uptake of PFAAs via land-applied biosolids and reclaimed water by food crops under conditions representative of current agricultural practices. In this study, greenhouse experiments were used to investigate various types of fresh food crops including lettuce, tomato, snap pea, radish, and celery grown in an industrially impacted biosolids-amended soil, a municipal biosolids-amended soil, and an unamended control soil. Concentrations of PFAAs in the edible portions of crops grown in soil amended with PFAA industrially impacted biosolids were high, whereas the edible compartments of crops grown in the municipal biosolids-amended soil and in the control soil were relatively low. Significant uptake factors and bioaccumulation trends of PFAAs were explored. Strong carbon chain length dependency trends were observed; short-chain PFAAs accumulated in much higher concentrations than long-chain PFAAs. In general, bioaccumulation factors decreased up to 0.5 log units for each additional carbon. To further explain the data, the roles of crop anatomy and PFAA properties in controlling PFAA bioaccumulation were explored. Fruit crops accumulated high amounts of short-chain PFAAs but fewer long-chain PFAAs than did shoot or root crops, presumably due to an increasing number of biological barriers as the contaminant is transported throughout the plant (roots to shoots to fruits). These data were incorporated into a preliminary conceptual framework for PFAA accumulation in edible crops. In addition, a limited-scale field study of biosolids-amended soils was conducted to verify greenhouse findings. The greatest accumulation was seen for short-chain PFAAs in both field-grown lettuce and tomato. PFAA levels measured in lettuce and tomato grown in field soil amended with only a single application of biosolids (at an agronomic rate for nitrogen) were predominantly below the limit of quantitation. In addition, corn stover, corn grains, and soil were collected from several full-scale biosolids-amended farm fields. At these fields, all PFAAs were below the limit of quantitation in the corn grains and only trace amounts were detected in the corn stover. Finally, this study used authentic reclaimed water augmented with varying doses of PFAAs to investigate the potential uptake and dose-dependency trends in greenhouse grown lettuce and strawberry. Concentrations of PFAAs in lettuce leaves and strawberry fruit were measured for each incremental dose, while concentrations in strawberry shoot and root were measured for selected doses. Short-chain PFAAs showed the overall highest accumulation of any PFAAs in the edible parts of both lettuce and strawberry. Concentrations increased linearly with increasing dose for almost all PFAAs, with the exception of the long-chain PFAAs in strawberry fruit, which remained at a constant concentration regardless of dose. Chain length dependency trends were evident in both lettuce shoot and strawberry fruit, with decreasing concentrations occurring with increasing chain length. Lettuce grown in soils with varying organic carbon content was used to assess the impact of organic carbon sorption on PFAA bioaccumulation. In general, a higher fraction of organic carbon in the soil correlated to less bioaccumulation of PFAAs in lettuce. Bioaccumulation factors were also correlated to carbon chain length of PFAAs showing approximately a 0.4 to 0.6 log decrease per carbon. This study confirms that PFAAs are able to be taken up and bioaccumulate in food crops via both biosolids and reclaimed water. PFAA bioaccumulation potential is highly dependent on analyte, crop, PFAA concentration in the uptake matrix, and the organic carbon content and quality of the soil. With industry trends shifting toward the use of short-chain PFAAs, it is important to recognize this increased potential of PFAA entry into the terrestrial food chain via plants. If the current use of land-applied biosolids and reclaimed water for food crops is to be sustained or increase in future years, these concerns about the potential contamination of food products must be fully addressed through careful scientific study, evaluation, and communication with the public.