Duckweeds for Remediating Water Contaminated with Organic Compounds

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This entry is adapted from the peer-reviewed paper 10.3390/plants12030589

Tiny aquatic plants from the Lemnaceae family, commonly known as duckweeds, are often regarded as detrimental to the environment because of their ability to quickly populate and cover the surfaces of bodies of water. Due to their rapid vegetative propagation, duckweeds have one of the fastest growth rates among flowering plants and can accumulate large amounts of biomass in relatively short time periods. Due to the high yield of valuable biomass and ease of harvest, duckweeds can be used as feedstock for biofuels, animal feed, and other applications. Thanks to their efficient absorption of nitrogen- and phosphate-containing pollutants, duckweeds play an important role in the restorative ecology of water reservoirs. The global distribution of duckweeds and their tolerance of ammonia, heavy metals, other pollutants, and stresses are the major factors highlighting their potential for use in purifying agricultural, municipal, and some industrial wastewater. In summary, duckweeds are a powerful tool for bioremediation that can reduce anthropogenic pollution in aquatic ecosystems and prevent water eutrophication in a simple, inexpensive ecologically friendly way.

duckweed phytoremediation organic compound wastewater

1. Organic Agrochemicals

With the increasing demand for food and the development of agriculture and aquaculture, tons of toxic agrochemicals such as pesticides, herbicides, and fungicides are produced and applied annually. A considerable amount of these chemicals applied on farmlands and aquaculture ends up in the aquatic environment without treatment, causing substantial pressure on the environment. Aquatic non-targeted organisms are more likely to be exposed to herbicides in multiple pulse events than long continuous exposure. Therefore, the potential of an organism to recover between exposures has important effects on the overall toxicity. In addition, the organism used for bioremediation must be able to tolerate relevant concentrations of the compound while taking up some of the compound to metabolize it. Studies to test the toxicity to and uptake of agrochemicals by duckweed have primarily used L. minor.

Most agrochemicals are tolerated by duckweed at low concentrations but are toxic at higher concentrations. Wilson and Koch (2013) evaluated the effects and potential recovery of L. minor exposed to the herbicide norflurazon for 10 days under controlled conditions ^[1]. Duckweed was severely inhibited by norflurazon, but there was a rapid recovery for all norflurazon concentrations tested after the plant was removed from the media ^[1]. Varga et al. (2020) evaluated the growth patterns and recovery potential of duckweed between multiple exposures to the herbicide isoproturon ^[2]. Growth was significantly inhibited during each exposure phase with significant cumulative effects in subsequent treatment cycles, resulting in a cumulative decrease in biomass production. However, inhibitory effects were reversible upon transferring plants to a herbicide-free nutrient solution. These results indicate that L. minor plants have a high potential for recovery even after multiple exposures to isoproturon.

Burns et al. (2015) investigated the ability of two duckweed species (L. minor and L. gibba) to recover from a 7-day exposure to different concentrations (0.4–208 µg/L) of the herbicide diuron ^[3]. Diuron significantly inhibited duckweed growth and biomass production after the initial 7-day exposure. Following transfer to herbicide-free media, recovery was observed for all effects at concentrations ranging 60–111 µg/L for L. minor and 60–208 µg/L for L. gibba. These results suggest that recovery is possible for primary producers at environmentally relevant concentrations that are considered significant in ecological risk assessment. The herbicide glyphosate can induce oxidative stress in plants through H₂O₂ formation by targeting the mitochondrial electron transport chain and the deleterious effects of the herbicide, glyphosate, on duckweed photosynthesis, respiration, and pigment concentrations were related to glyphosate-induced oxidative stress through H₂O₂ accumulation ^[4].

Even though agrochemicals are toxic to duckweed, researchers showed that duckweed was able to remove agrochemicals from the environment, indicating that this aquatic plant can efficiently eliminate organic contaminants and may ultimately serve as phytoremediation agents in the natural environment. Dosnon-Olette studied the effect of two herbicides, isoproturon and glyphosate, on L. minor growth ^[5] and showed that 10 µg/L isoproturon and 80 µg/L glyphosate had little effect on the growth rate and chlorophyll fluorescence of L. minor, which was able to remove 25% and 8% of the isoproturon and glyphosate, respectively, after a four-day incubation. Mitsou et al. (2006) studied the toxicity of the rice herbicide propanil to L. minor and found that propanil, at a concentration of 1 mg/L, did not affect the growth of L. minor, and did not induce antioxidative defenses within the plant. In addition, L. minor accumulated and metabolized the propanil ^[6]. Prasertsup and Ariyakanon (2011) explored the potential of water lettuce (Pistia stratiotes L.) and duckweed (L. minor) to remove different concentrations of the herbicide chlorpyrifos under greenhouse conditions. Low concentrations (0.1 and 0.5 mg/L) of chlorpyrifos had no significant effect on the growth of L. minor and P. stratiotes, but a higher concentration (1 mg/L) inhibited their growth. The maximum removal of chlorpyrifos (initial culture concentration of 0.5 mg/L) by P. stratiotes and L. minor was 82% and 87%, respectively ^[7]. Olette et al. (2008) compared the ability of three aquatic plants to remove three pesticides and found that compared to two other aquatic plants (Elodea canadensis and Elodea canadensis), L. minor more efficiently removed the pesticides, causing reductions of 50%, 11.5% and 42% for copper sulfate, dimethomorph, and flazasulfuron, respectively ^[8].

Many organisms limit toxicity of environmental factors by not taking up these factors; however, successful bioremediation requires that the plant take up some of the compound and metabolize it into less-toxic byproducts. Dosnon-Olette et al. (2010) studied the factors affecting the rate of pesticide uptake by two duckweed species, L. minor and S. polyrhiza ^[9]. Increased sensitivity to the pesticide dimethomorph was observed with increasing duckweed population density, possibly explained by having less light due to crowding. Plant photosynthesis uses light as the energy source leading to the production of biochemical energy (e.g., ATP) and reducing power (NADPH), which in turn are used for carbon fixation. This light-dependent electron source contributes to the absobing and transformation pesticide dimethomorph. Panfili et al. (2019) showed that L. minor is suitable for cleaning water polluted with the herbicide terbuthylazine, and this potential can be successfully improved by treating the species with a biostimulant or a safener such as Megafol and benoxacor ^[10].

Tront and Saunders (2007) evaluated the uptake and accumulation of a fluorinated analog of 2,4-dichlorophenol, 4-chloro-2-fluorophenol (4-Cl-2-FP), by L. minor ^[11]. Time series data gathered from an experiment with an initial aqueous-phase concentration of 130 mM 4-Cl-2-FP showed that 4-Cl-2-FP was continuously removed from the aqueous phase and less than 2% of original 4-Cl-2-FP was detected in plant tissue within the time period of 77 h. An increasing amount of metabolites was detected in the plant tissue, comprising 18.9%, 28.6%, and 53.4% of original 4-Cl-2-FP at 10 h, 24 h, and 77 h, respectively. This means that over 95% of the initial compound accumulated by duckweed was broken down in the plant cells. Although many studies have focused on herbicides and their effects on aquatic plants, other agrochemicals also affect plants. For example, Yılmaz and Taş (2021) examined the effect of the synthetic pyrethroid insecticide zeta-cypermethrin on the growth and bioremediation of aquatic photosynthetic organisms and showed that L. minor used zeta-cypermethrin as a nutrient and increased its development in low zeta-cypermethrin concentration (150 µg/L) medium ^[12]. However, high concentrations (300–600 µg/L) were toxic and inhibited growth. In addition, L. minor removed 35.4–95.9% of zeta-cypermethrin, depending on the initial concentration.

2. Pharmaceuticals and Personal Care Products (PPCPs)

PPCPs, including antibiotics, painkillers, anti-inflammatory drugs, disinfectants, and aromatics, pose potential hazards to the environment and human health. These pollutants are becoming ubiquitous in the environment because they cannot be effectively removed by conventional wastewater treatment due to their toxic and recalcitrant nature. Though the PPCPs, and particularly pharmaceuticals are usually present in wastewaters at very low concentrations of nanograms per liter, their average annual world per capita is 15 g with 50–150 g in the most developed countries ^[13]^[14]. Considering that these compounds are often pretty stable, bioactive and bioaccumulative, they can present serious environmental and human health risks ^[15]^[16].

Toxicity to plants caused by pharmaceuticals is an important issue, and several plant species, including duckweed, have been considered for phytoremediation of pharmaceuticals in wetlands ^[17]. Like agrochemicals, most PPCPs are toxic to duckweeds. For example, three β-blockers, propranolo, atenolol and metoprolol, were found to be toxic to duckweed (L. minor), which was less sensitive than the arthropod Daphnia magna and the green alga Desmodesmus subspicatus ^[18]. Kaza et al. (2007) evaluated the toxicity of 13 pharmaceuticals, usually at ng/L to µg/L in the environment, to duckweed L. minor ^[19]. A total of 7 out of 13 drugs tested were toxic at concentrations below 100 mg/L. The antipsychotic drugs thioridazine and chlorpromazine were the most toxic substances, having effective concentrations (EC₅₀s) below 1 mg/L. Synthetic wastewater contaminated with the target compounds at 25 μg/L was prepared, and batch and continuous-flow experiments were conducted. Batch verification tests achieved removals of 98.8%, 96.4% and 95.4% for paracetamol, caffeine, and tricolsan, respectively. Overall removal of the PPCP contaminants was 97.7%, 98.0%, and 100% for paracetamol, caffeine, and tricolsan, respectively, by the constructed wetland system alone, while 97.5%, 98.2%, and 100%, respectively, were achieved by the lab-scale free water surface constructed wetland system ^[19].

In other work, Reinhold et al. (2010) tested the potential of both live and inactivated duckweed in removing pharmaceuticals in a microcosm wetland system ^[20]. Indeed, both live and inactivated duckweeds actively increased aqueous depletion of fluoxetine, ibuprofen, 2,4-dichlorophenoxyacetic acid, and the hand sanitizer triclosan. Some PPCPs can be used as a carbon source by duckweeds.

Amy-Sagers et al. (2017) conducted laboratory ecotoxicological assessments for a large range of concentrations of sucralose (an artificial sweetener) and fluoxetine (an antidepressant) on L. minor physiology and photosynthetic function ^[21]. Their results showed that, unlike humans who cannot break down and utilize sucralose, L. minor can use sucralose as a sugar substitute to increase its green leaf area and photosynthetic capacity. However, fluoxetine (323 nM) significantly decreased L. minor root growth, daily growth rate, and asexual reproduction.

2.1. Antibiotics

Although most antibiotics are toxic to duckweeds, they can tolerate and phytoremediate those compounds from the environment with different efficiency depending on particular types and concentrations of the antibiotic. Cascone et al. (2004) evaluated the phytotoxicity of the fluoroquinolone antibiotic flumequine on L. minor and plant drug uptake ^[22]. Flumequine, at all concentrations between 50 and 1000 µg/L tested, affected plant growth, but duckweed continued to grow over a five-week period. In media containing flumequine, a large proportion of the drug (about 96% at all concentrations tested) was degraded in the presence of Lemna. Gomes et al. (2017) studied the mechanism by which PPCPs affect duckweeds and found that in L. minor, high concentrations of the common antibiotic ciprofloxacin disrupted the normal electron flow in the respiratory electron transport chain and induced hydrogen peroxide production, thus changing the photosynthetic, respiratory pathway, and oxidative stress capacity of duckweed and affecting its ability to remove ciprofloxacin ^[23]. Therefore, when the concentration of antibiotics is high, the metabolism of duckweed changes, affecting its ability to remove the antibiotics. Singh et al. (2018) evaluated the potential toxicity of the antibiotic amoxicillin on the duckweed S. polyrhiza and found it was toxic, even at low concentrations ^[24]. Nonetheless, the duckweed contributed directly to the degradation of antibiotics in the water. In other study, the same group ^[25] estimated the phytotoxicity and degradation by S. polyrhiza of the antibiotic ofloxacin. The high concentrations of ofloxacin caused a reduction in biomass (4.8–41.3%), relative root growth, protein (4.16–11.28%) and photopigment contents. The fronds treated with ofloxacin showed an increased level of antioxidative enzymes (catalas, ascorbate peroxidase and superoxide dismutase) than control. The residual ofloxacin content in the medium was significantly reduced (93.73–98.36%) by day seven and phytodegradation was suggested to be the main mechanism for removal of this antibiotic.

The specific mechanism of PPCP removal by duckweeds depends on the type of PPCP and the duckweed species. Iatrou et al. (2017) explored the mechanism of removal effect of four kinds of antibiotics by L. minor ^[26]. The removal efficiencies of L. minor were 100% (cefadroxil), 96% (metronidazole), 59% (trimethoprim), and 73% (sulfamethoxazole), respectively. Plant uptake and biodegradation were the major mechanisms accounting for metronidazole removal; the most important mechanism for trimethoprim was plant uptake.

2.2. Analgesics and Anti-Inflammatory Drugs

The anti-inflammatory drugs and analgesics that do not require prescription in many countries, such as ibuprofen or paracetamol, are widely spread in the environment. Matamoros et al. (2012) found that caffeine and ibuprofen are removed by biodegradation and/or plant uptake by three aquatic plants, including the duckweed L. minor, and the removal rate was 83–99% in a microcosm wetland system ^[27]. In the presence of 1 mg/L ibuprofen, an increase in L. gibba frond number (+12%) and multiplication rate (+10%) was seen, while no variations in photosynthetic pigment content were observed ^[28]. Moreover, ibuprofen and 11 ibuprofen metabolites were detected in plants and in the growth medium, suggesting that L. gibba metabolizes ibuprofen. Li et al. (2017) studied the removal of four selected emerging PPCP compounds using greater duckweed (S. polyrhiza) in a laboratory-scale constructed wetland ^[29]. Di Baccio et al. (2017) explored the removal and metabolism of ibuprofen by L. gibba at high (0.20 and 1 mg/L) and environmentally relevant (0.02 mg/L) ibuprofen concentrations ^[30]. Ibuprofen uptake increased with increasing concentration, but the relative accumulation of ibuprofen and generation of hydroxy-ibuprofen was higher in the lower ibuprofen treatments. The main oxidized ibuprofen metabolites in humans (hydroxy-ibuprofen and carboxy-ibuprofen) were identified in the intact plants and in the growth solutions. Apart from a mean physical-chemical degradation of 8.2%, the ibuprofen removal by plants was highly efficient (89–92.5%) in all conditions tested.

3. Other Industrial Organic Compounds

Because of the efficient removal of pesticides and PPCPs by duckweed, researchers have explored whether duckweed can effectively remove other organic pollutants. In a recent study, the potential of L. minor for decolorization and degradation of malachite green (a triarylmethane dye) was investigated. The decolorization ability of the plant species was as high as 88%, and eight metabolic intermediate compounds were identified by gas chromatography-mass spectrometry ^[31]. Can-Terzi et al. (2021) ^[32] studied the phytoremediation potential of L. minor using methylene blue and showed that L. minor could effectively remove methylene blue from wastewater with the highest removal efficiency (98%) within 24 h. Fourier transform infrared spectroscopy (FTIR) and scanning electron microscopy (SEM) analyses indicated that dye removal was mainly by biosorption. Torbati (2019) evaluated the ability of L. minor to decolorize the acid Bordeaux B (ABB, an aminoazo benzene dye) ^[33]. Increased temperature and enhancement of initial plant weight increased the dye removal efficiency, but raising the initial dye concentration and pH reduced it. In optimum conditions, L. minor exhibited a considerable potential (94% removal) for the phytoremediation of ABB. Seven intermediate ABB degradation products were identified using gas chromatography-mass spectrometry analysis, indicating biodegradation is one of the mechanisms of L. minor’s removal and detoxification of ABB.

In a study of the fate of five benzotriazoles (used to inhibit the corrosion of copper) in a continuous-flow L. minor system, benzotriazole removal ranged between 26% and 72%. Plant uptake seemed to be the major mechanism governing the removal of benzotriazoles. When Zhang and Liang (2021) investigated the removal efficiency of 8 perfluoroalkyl acids by L. minor under aeration ^[34], they found that the removal efficiency of L. minor for long-chain perfluoroalkanes exceeded 95%, while the removal efficiency for short-chain perfluoroalkanes was marginal. The accumulation of perfluorooctane sulfonate in L. minor cells reached 14.4% after 2 weeks of exposure. Subsequently, the researchers further investigated the absorption and accumulation effect of L. minor on several intermediates of perfluoroalkyl compounds. The results showed that, after 14 days of exposure, L. minor accumulated 86.7 μG kg⁻¹ and 1226 μG kg⁻¹ for perfluorooctyl sulfonamide and fluorotelomere sulfonate, respectively ^[34]. In related work, Ekperusi et al. (2020) tested the potential of Lemna paucicostata (Lemna aequinoctialis, according to current classification) for removing petroleum hydrocarbons from crude oil-contaminated waters in a constructed wetland over a period of 120 days ^[35]. They found that L. paucicostata significantly (F = 253.405, p < 0.05) removed petroleum hydrocarbons from the wetland, reaching nearly 98% after 120 days, and estimated that about 97% of the petroleum hydrocarbons were biodegraded, because less than 1% bioaccumulated.

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Yuzhen Zhou

Anton Stepanenko

Olena Kishchenko

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Nikolai Borisjuk

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Entry Collection: Wastewater Treatment

Update Date: 06 May 2023

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