Environmental Pollution
Volume 242, Part B,
November 2018
, Pages 1748-1757
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Abstract
Reclaimed water is a historically underutilized resource. However, with increased population growth and global climate change, reclaimed water is evolving into an economical and sustainable water resource to meet the needs of citizens, industries, and agriculture. The use of recycled water for agricultural irrigation comes with the potential risk of environmental and food contamination by pharmaceuticals and personal care products (PPCPs). The levels of PPCPs in plants will depend on translocation and metabolism in plant tissues. However, relatively little is known about the metabolism of PPCPs in plants. In this study, the metabolism of the antibiotic sulfamethoxazole was investigated in Arabidopsis thaliana cells as well as cucumber seedlings grown under hydroponic conditions. Using high-resolution mass spectrometry and 14C tracing allowed for sulfamethoxazole metabolism to be comprehensively characterized through all metabolic phases. Six phase I and II metabolites were identified in A.thaliana cell cultures and cucumber seedlings. Sulfamethoxazole metabolism followed oxidation and then rapid conjugation with glutathione and leucine. Direct conjugation with the parent compound was also observed via acetylation and glucosylation. At the end of 96 and 168 h incubation, N4-acetylsulfamethoxazole was the major metabolite and >50% of the radiolabeled sulfamethoxazole became non-extractable in both A.thaliana cells and cucumber seedlings suggesting extensive phase III metabolism and detoxification. The study findings provided information for a better understanding of the uptake and metabolism of sulfamethoxazole in higher plants, highlighting the need to consider metabolic intermediates and terminal fate when assessing the risk of PPCPs in the soil-plant continuum.
Introduction
Over the past two decades, pharmaceuticals and personal care products (PPCPs) have emerged as contaminants of environmental concern due to their extensive use and continuous emission into the environment (Daughton and Terns, 1999; Pedersen etal., 2005; Boxall etal., 2012). PPCPs are released into the environment primarily through the disposal of treated wastewater and biosolids from wastewater treatment plants (WWTPs) (Carballa etal., 2004). As climate change and population growth places an increasing stress on freshwater resources, especially in arid and semi-arid regions, communities have turned to utilizing municipal treated water for agricultural irrigation, which may result in soil contamination by PPCPs (Barnett etal., 2005; Tal, 2006; NRC, 2012). Furthermore, the heavy use of some pharmaceuticals, particularly antibiotics, for disease control and growth promotion in intensive animal farming also contributes to contamination of agricultural fields when animal wastes are used for fertilization (Hu etal., 2010).
The presence of PPCPs in irrigation water and soil can lead to contamination of food crops if plants can substantially accumulate these compounds. Various studies over the last decade have sought to quantify plant uptake of PPCPs, and in general, only low levels of PPCPs have been found in edible tissues (ng/kg) (e.g., Wu etal., 2013, Wu etal., 2014). The majority of studies to date have only targeted the parent form of PPCPs for analysis. However, plants have a cascade of enzymes that may extensively transform xenobiotics such as PPCPs after uptake (Celiz etal., 2009; Fu etal., 2016). Recently several published studies have explored the metabolism of pharmaceuticals in plants (e.g. Huber etal., 2009, 2012; Fu etal., 2016; LeFevre etal., 2016; Marsik etal., 2017). Therefore, consideration of metabolism and biologically active metabolites is much needed for a better understanding of the fate and risks of PPCPs in the soil-plant system.
Higher plants have many detoxification enzymes similar to those in animals. These enzymes function in plants as a ‘green liver’ (Sandermann, 1994). In general, metabolism of xenobiotics includes three phases. Phase I involves modification reactions such as oxidation, hydrolysis, and dealkylation reactions introducing reactive sites to the molecule. Phase II is characterized by conjugation with large polar biomolecules, such as sugars and amino acids, to further increase the polarity of the xenobiotic. Phase III is typified by sequestration, resulting in the formation of bound residues (Sandermann, 1992; Sandermann, 1994, Miller etal., 2016). As shown for many xenobiotics in mammals and plants metabolites from phases I and II often retain biological activity (Osborne etal., 1990; Pichersky and Gang, 2000; Miller etal., 2016), and therefore should not be discounted.
In this study, sulfamethoxazole was selected as the compound of interest because of its prevalence in WWTP effluents and increasing concerns over the propagation of antibiotic resistance (Yao etal., 2012; WHO, 2016). Since its introduction in 1961 sulfamethoxazole has been widely prescribed due to its potency against both gram-positive and gram-negative bacteria (Brunton etal., 2011). Currently, sulfamethoxazole's has been detected from ng L−1 to μg L−1 in surface and effluent waters and μg kg−1 to mg kg−1 in soils and manure (Hu etal., 2010; Shelver etal., 2010; Brausch etal., 2012). Recent long-term studies of waste-water application under realistic field conditions have highlighted the potential for sulfamethoxazole to be taken up and translocated in crop plants, including to the fruit (Christou etal., 2017).
The structures of sulfamethoxazole metabolites, including conjugates from Phase II metabolism, were identified using high-performance liquid chromatography coupled with time-of-flight high-resolution mass spectrometry (HPLC-TOF-HRMS) and further quantified using ultra-high performance liquid chromatography in tandem with a triple quadrupole mass spectrometry (UPLC-TQD-MS/MS). Furthermore, Phase III terminal products in the form of bound residues were quantified using 14C labeling.
Arabidopsis thaliana cells were selected as the experimental organism due to their extensive use in the literature, commercial availability, and their membership in the commonly consumed Brassica family (e.g., cabbage, broccoli, kale). Further, Arabidopsis thaliana plants are found worldwide under several common names (e.g., Wall cress, mouse-ear cress, shiro-inu-nazuna) and are consumed by a wide variety of animals as well as humans (van Poecke and Dicke, 2004, TAIR institute, 2018). Cucumber (Cucumis sativus) was selected in the hydroponic experiment due to the fact that it is often consumed raw, rapid growth, and amiability to soilless culture (Texas A&M, AgriLife, 2018).
Section snippets
Chemicals and solvents
Non-labeled sulfamethoxazole was purchased from MP Biomedicals (Solon, OH). Sulfamethoxazole-d4 was purchased from C/D/N Isotopes (Pointe-Claire, Quebec, Canada) and 14C-labeled sulfamethoxazole was obtained from American Radiolabeled Chemicals (Saint Louis, MO). Stock solutions of 14C-sulfamethoxazole and non-labeled sulfamethoxazole were prepared in methanol to reach a specific radioactivity of 1.2 × 103 dpm μL−1 and a chemical concentration of 1.0 mg mL−1, respectively. HPLC grade
Kinetics of parent, extractable and non-extractable residues
The metabolism of sulfamethoxazole in Arabidopsis thaliana cells was validated using a range of controls. No sulfamethoxazole was detected in the media or cell blanks, and there was no detectable disappearance of sulfamethoxazole in the cell-free media, suggesting the absence of contamination or abiotic transformation. Moreover, no significant difference was seen in the cell mass between the chemical-free control and the treatments indicating that sulfamethoxazole did not affect the growth of
Conclusions
Results from this study demonstrated that 14C tracing, high-resolution mass spectrometry, and cell and hydroponic cultures may be used in a complementary manner to obtain a complete depiction of plant metabolism of emerging contaminants. The antibiotic sulfamethoxazole was found to be taken up and metabolized extensively by A.thaliana cells and cucumber seedlings. The Phase I metabolism involved the oxidation of the amine group, which was followed by Phase II reactions including conjugation
Acknowledgments
The authors would like to thank Dr. Qiuguo Fu, currently at the EAWAG, Swiss Federal Institute of Aquatic Science and Technology for aid with HPLC HR-MS data analysis, the U.S. Environmental Protection Agency STAR program (Award No: R835829) and the National Science Foundation-the Water SENSE Integrative Graduate Education Research Training program (No. DGE-1144635) for funding support.
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Cited by (42)
Accumulation and risk assessment of antibiotics in edible plants grown in contaminated farmlands: A review
2022, Science of the Total Environment
The extensive occurrence of antibiotics in farmland soil might threaten food safety. The bioaccumulation potential of antibiotics in edible vegetables and crops grown under realistic farming scenarios was reviewed and the human health risk was assessed. A total of 51 antibiotics were documented in 37 species of daily consumed crops. Among different classes of antibiotics, tetracyclines (TCs) exhibited higher residue levels in plants than quinolones (QNs), sulfonamides (SAs), and macrolides (MLs), with median values ranging from 5.10 to 15.4 μg/kg dry weight. The favored accumulation of TCs in plants was probably linked to their relatively higher residual concentrations in soils and greater bioconcentration factors. Compared with the plants grown in open field, accumulation of antibiotics was higher in plant grown under greenhouse condition, probably due to the higher residue levels of antibiotics in the greenhouse soil with intensive application of manure. Cocktails of antibiotics were investigated in potato, corn, carrot, tomato, lettuce, and wheat. Among them, corn exhibited relatively high median concentrations of antibiotics (0.400–203 μg/kg dry weight). Antibiotics tended to accumulate in plant root and their concentrations in fruit were generally low. Risk assessment revealed that human health risk was under the alert line through the daily consumption of antibiotic contaminated vegetables and food crops.
Effects of tetracycline, sulfonamide, fluoroquinolone, and lincosamide load in pig slurry on lettuce: Agricultural and human health implications
2022, Environmental Research
The application of pig slurry as fertilizer in agriculture provides nutrients, but it can also contain veterinary medicines, including antibiotic residues (ABs), which can have an ecotoxicological impact on agroecosystems. Furthermore, uptake, translocation, and accumulation of ABs in crops can mobilize them throughout the food chain. This greenhouse study aims to assess AB uptake from soil fertilized with pig slurry and its phenotypical effects on Lactuca sativa L. The plants were cropped in loamy clay soil dosed at 140kg total N/ha and containing antibiotics (lincomycin, sulfadiazine, oxytetracycline, and enrofloxacin) at different concentration levels (0, 0.05, 0.5, 5, 50, and 500mg/kg fresh weight, fw). Whereas sulfadiazine (11.8ng/g fw) was detected in lettuce leaves at the intermediate doses (0.5mg/kg), lincomycin and its transformation products (hydroxy/sulfate) were only detected at the 50mg/kg fw dose. In addition, increased AB doses in the pig slurry resulted in decreased lettuce fresh weight and lipid and carbohydrate content and became lethal to lettuce at the highest AB concentrations (500mg/kg fw). Nevertheless, even at higher doses, the AB content in lettuce following pig-slurry fertilization did not pose any direct significant human health risk (total hazard quotient<0.01). However, the promotion of antimicrobial resistance in humans due to the intake of these vegetables cannot be ruled out.
Fate of carbamazepine and its effect on physiological characteristics of wetland plant species in the hydroponic system
2022, Science of the Total Environment
Plants play a cardinal role in removing various pollutants through the synergistic interaction with filling materials and microbes of constructed wetlands (CWs). However, the information regarding the selection of plant species to remove pharmaceutically active compounds (PhACs) is not adequate. The present study attempted to select an appropriate plant species for CWs, considering their characteristics and physiological response to PhACs. In this regard, batch hydroponics studies were carried out to assess the removal, fate, and antioxidative response of carbamazepine (CBZ) in four wetland plant species (Canna indica, Colocasia esculenta, Phragmites australis, and Chrysopogon zizanioides). The specific uptake potential of CBZ (in terms of plant dry biomass) was found to be in the order: C. indica (14.48 mg/g) > P. australis (11.71 mg/g) > C. esculenta (8.67 mg/g) > C. zizanioides (6.04 mg/g). The results showed that exposure to CBZ (0–30 days) caused an accumulation of reactive oxygen species (ROS) in the plant tissues, causing a decline in chlorophyll content, root activity, and increased oxidative stress. However, the selected plants could recover from the oxidative damages to a certain extent in the recuperation phase (31–60 days). C. indica exhibited relatively lesser ROS accumulation and oxidative damage during the experimental phase than other selected plants. The study also showed that plant biomass, transpiration rate, chlorophyll content, root exudates, and root activity influenced the removal of CBZ by various plants (r – 0.76 to 0.98, P < 0.05). The mass balance analysis indicated that a significant proportion of CBZ (49.2 to 72.7 %) underwent metabolism in the plant tissues. Apart from higher removal, lesser accumulation, and lower oxidation stress, multi-criteria decision analysis showed that C. indica is a potential plant species for the removal of CBZ.
Biotransformation of sulfamethoxazole by microalgae: Removal efficiency, pathways, and mechanisms
2022, Water Research
Recently, the biotransformation of sulfamethoxazole (SMX) by microalgae has attracted increasing interest. In particular, cytochrome P450 (CYP450) has been suggested to be the main enzymatic contributor to this biodegradation. However, the molecular evidence of CYP450 enzymes being involved in SMX biodegradation remains relatively unclear, hindering its applicability. Herein, the biodegradation of SMX by Chlorella sorokiniana (C. sorokiniana) was investigated, and comprehensively elucidated the reaction mechanism underlying CYP450-mediated SMX metabolism. C. sorokiniana was able to efficiently remove over 80% of SMX mainly through biodegradation, in which CYP450 enzymes responded substantially to metabolize SMX in cells. Additionally, screening of transformation products (TPs) revealed that N4-hydroxylation-SMX (TP270) was the main TP in the SMX biodegradation pathway of microalgae. Molecular dynamics (MD) simulation suggested that the aniline of SMX was the most prone to undergo metabolism, while density functional theory (DFT) indicated that SMX was metabolized by CYP450 enzymes through H-abstraction-OH-rebound reaction. Collectively, this work reveals key details of the hydroxylamine group of SMX, elucidates the SMX biodegradation pathway involving CYP450 in microalgae in detail, and accelerates the development of using microalgae-mediated CYP450 to eliminate antibiotics.
Retention of sulfamethoxazole by cinnamon wood biochar and its efficacy of reducing bioavailability and plant uptake in soil
2022, Chemosphere
The objective of this research was to evaluate the efficacy of cinnamon wood biochar (CWBC) in adsorbing sulfamethoxazole (SUL), which alleviates bioavailability and plant uptake. Batch studies at various pH, contact times, and initial SUL loading were used to study SUL adsorption in CWBC, soil, and 2.5% CWBC amended soil. SUL mitigation from plant uptake were examined using Ipomoea aquatica at different SUL contamination levels in the soil. The kinetic results were described by pseudo-second-order with maximum adsorption capacities () of 95.64 and 0.234mg/g for pristine CWBC and amendment, respectively implying that chemical interactions are rate-determining stages. Hill and Toth's model described the isotherm data for pristine CWBC, soil and CWBC amended soil as of 113.44, 0.72, and 3.45mg/g. Column data showed a great mobilization of SUL in loamy sand; however, when CWBC was added to the loamy sand, the mobilization was drastically reduced by 98.8%. The Ipomoea aquatica showed a great potential to SUL uptake and it depended on the contamination level; the SUL accumulation in plant was 9.6–13.8 and 19.1–48mg/kg when soil was spiked with 5 and 50mg/kg, respectively. The addition of 2.5% CWBC reduced root and shoot uptake by 30 and 95%, respectively in 5mg/kg of SUL, whereas with 50mg/kg of SUL, the root and shoot uptake was reduced by 60 and 61%, respectively. The current study suggested CWBC as a possible adsorbent that may be employed to reduce SUL bioavailability in environmental matrices.
Microalgal mediated antibiotic co-metabolism: Kinetics, transformation products and pathways
2022, Chemosphere
The mutual interaction of a microalga Chlorella vulgaris with four antibiotics viz. sulfamethoxazole (SMX), trimethoprim (TMP), azithromycin (AZI), and levofloxacin (LEV) individually and in mixture was studied in batch culture. SMX, TMP, and LEV stimulated algal growth, while AZI inhibited its growth. The Combination Index (CI)-isobologram indicated antagonism of the antibiotic mixture on the growth of C. vulgaris. Higher removal efficiency was observed in the mixed antibiotic than in the single antibiotic batch cultures. Biodegradation was the main antibiotic removal mechanism with a similar antibiotic biosorption pattern in single and mix antibiotic cultures. Scanning electron microscopy and Fourier transform infrared spectrophotometry showed minor biochemical alterations on algal cells surface and a stable algal population. Monod kinetics model was successfully applied to understand the growth with respect to the removal efficiency of C. vulgaris in single and mix antibiotic batch cultures. Results indicated relatively higher specific growth rate in the mix antibiotic batch culture with removal efficiency in the order of SMX>LEV>TMP>AZI. In total, 46 metabolites with 18 novel ones of the four antibiotics were identified by using high-resolution mass spectrometry based on the suspect screening approach to propose the potential transformation pathways. Most of the transformation products demonstrated lower toxicity than their respective parents. These findings implied that C. vulgaris could be an outstanding candidate for advanced treatment of antibiotic removal in wastewater.
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