Impact of long-term irrigation with municipal reclaimed wastewater on the uptake and degradation of organic contaminants in lettuce and leek
Graphical abstract
Introduction
In arid and semi-arid agricultural area, in both developed and developing countries, irrigation of crops with treated wastewater (TWW) is already a common practice as a result of water scarcity due to climate change as well as to continuously growing population (Carter et al., 2019; Ait-Mouheb et al., 2018). A large body of literature has demonstrated that crop plants can accumulate organic contaminants and more specifically pharmaceuticals and personal care products (PPCPs) (Fu et al., 2019). However, studies have been carried out by using different plant-growth methods (e.g., hydroponic cultivation, crops in pots under greenhouse, field cultivation conditions) with different sets of contaminants, different types of plants and different irrigation methods resulting to some inconsistency in conclusions. Limited data is actually available under real field growing conditions of crops using appropriate irrigation regimes (Goldstein et al., 2014; Riemenschneider et al., 2016; Wu et al., 2014; Christou et al., 2017; Picó et al., 2019), besides most of the studies did not focus on long term introduction of contaminants in soil-plant system through irrigation, neither their fate/behavior in soil which can affect their fate and uptake in plants at the same time. Therefore, it is crucial to conduct such experiments following the risk introduced by wastewater irrigation at long-term field conditions, taking in consideration contaminants fate in the whole soil-plant system. PPCPs concentration levels, which have been found in edible parts of food crops are in the ng/g to low μg/g range, hence revealing the potential for human exposure to PPCPs as a result of irrigation with TWW (Gonzalez Garcia et al., 2019). The European Commission has proposed in May 2018 new guidelines to facilitate water reuse in the EU for agricultural irrigation (EC European Commission, 2018) which are mainly focused on water physico-chemical constituents and pathogen indicators. However, the problem of organic contaminants has been mentioned in annexes, calling for more research in this field before including their levels as stricter requirements for water quality, if needed. Soil properties, water quality, the nature of the PPCPs and their physico-chemical properties as well as plant physiology (i.e. type of crops) have been considered major governing factors in determining plant uptake (Wu et al., 2015). Generally, plant uptake of neutrally charged PPCPs is greater than ionic compounds, because anionic PPCPs are repelled by cell membranes with negative electrical potential, and cationic species are attracted to the cell membranes thus limiting their movement into plants (Chuang et al., 2019). In addition, experimental results revealed that the potential for PPCPs uptake by crop plants decreased in the order of leafy green vegetables > root vegetables > cereals and fodder crops > fruit vegetables (Christou et al., 2019). Water flow is believed to be the primary carrier for uptake and transport of PPCPs in plants and transpiration may be a strong predictor for the accumulation of structurally diverse PPCPs in above-ground plant tissues (Nason et al., 2019). Others studies have shown the relevance of the PPCPs concentrations in soil pore water and consequently their bioavailability to plant uptake (Li et al., 2019). In contrast, the role of the behavior/fate of PPCPs in soil under field cultivation conditions has been poorly considered because research efforts have typically focused on short-term TWW irrigation scenarios, when plants were exposed for only short-time periods to PPCPs. The role of soil as a regulator and/or attenuator of the amount of PPCPs available for plant uptake due to sorption and degradation processes has probably been underestimated. One of the research need is therefore a better understanding of the behavior and fate of PPCPs in soil following chronic or long terms irrigation of TWW in agro-food systems to investigate the relevance of PPCPs exposure time on the plant uptake processes and on the subsequent effects on PPCPs degradation. The reduction of PPCPs uptake by plants is generally related to sorption processes to soil, especially for those chemicals with strong hydrophobicity or positive charge but also to transformation processes such as photolysis at the soil-surface and biodegradation (Fu et al., 2019). Plant uptake might be therefore reduced, if attenuation processes outbalance the continuous input of chemicals. In addition, there is the potential for agricultural soil to develop accelerated biodegradation due to microorganisms adaptation processes, accounting for the non-accumulation of drugs such macrolide antibiotics over multiple crop cycles (Topp et al., 2016). Another research gap might be the role of active transport carriers in PPCPs plant uptake. Most current literature quantifying PPCPs accumulation in crop plants focuses on passive processes such as diffusion across membranes, ion trapping, and sorption. However, some results suggest that in some cases plant transporter proteins may be important for accumulation of certain PPCPs, as has been assumed for metformin (Eggen and Lillo, 2016) and amitriptyline (Nason et al., 2019). Understanding the biological aspects of plant accumulation of PPCPs is important not only in environmental risk assessment but also from a remediation perspective (e.g. removal in engineered treatment wetlands). Consequently, the major aim of this work was to contribute to fill these scientific gaps by investigating the behavior of selected organic contaminants (mainly PPCPs) in the wastewater-soil-plant system for the specific conditions of greenhouse-grown of lettuce and leek irrigated with different kinds of wastewater including raw municipal wastewater (RWW), lagoon-based secondary treated wastewater (TWW) and spiked TWW with 14 pollutants under realistic agricultural scenarios over multiple crop cycles. Specific objectives were i) to investigate the impact of the fate of targeted PPCPs in soil on plant uptake ii) to understand the main driving processes of their uptake in plant, iii) to investigate the fate of selected PPCPs in lettuce leaves to evaluate implications of irrigation with TWW containing these PPCPs for food safety and human exposure via dietary intake.
Section snippets
Chemicals
Fourteen organic contaminants that were commonly detected in TWW were selected in this study including pharmaceuticals (ciprofloxacin (CIP), sulfamethoxazole (SMX), citalopram (CTP), diclofenac (DCF), valsartan (VAL), irbesartan (IRB), carbamazepine (CBZ), metoprolol (MTP), hydrochlorothiazide (HCT), clarithromycin (CLT)), food additives (acesulfame (ASF), sucralose (SUC)), the fungicide climbazole (CLB, human medicine) and the corrosion inhibitor 1H-benzotriazole (BNZ). The transformation
Occurrence and accumulation patterns of contaminants (mainly PPCPs) in soil and leaves
Only a few studies have reported the uptake and accumulation of organic contaminants by crop plants irrigated with TWW under realistic agricultural growing and irrigation conditions. Even fewer studies have reported their concentration values both in soil and in the edible part of the crop allowing for BCF calculation. In spite of poor controllable and reproducible conditions, field studies were implemented because they enabled an appropriate risk assessment of wastewater-borne contaminants to
Conclusions
Crops irrigation with TWW represents a recognized pathway for human exposure to organic contaminants with possible health implications. However, this study confirmed that the accumulation of 14 compounds in soil and in lettuce leaves irrigated with spiked TWW at 10 μg/L concentration level was very limited. These results relied on the implementation of real greenhouse cultivation conditions, the repeated application of spiked TWW over five successive lettuce crop cycles and a large number of
CRediT authorship contribution statement
Rayana Manasfi: Analysis – writing – original draft, review & editing
Monica Brienza: Experimental data interpretation
Nassim Ait-Mouheb: Implementation of field experiments
Nicola Montemurro: Analytical methods for organic contaminants
Sandra Perez: Analytical methods for organic contaminants
Serge Chiron: Conceptualization – writing, review & editing
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This research was financially supported by the Water and Agriculture, Food Security and Climate Change Joint Programming Initiatives (JPIs) through the research project AWARE “Assessing the fate of pesticides and waterborne contaminants in agricultural crops and their environmental risks”, the French Rhône-Méditerranée-Corse Water Agency for the experimental platform for the reuse of reclaimed wastewater in irrigation (Murviel-lès-Montpellier) project and the Spanish Ministry of Science and
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