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Article

Benefits of Ryegrass on Multicontaminated Soils Part 1: Effects of Fertilizers on Bioavailability and Accumulation of Metals

by
Christophe Waterlot
1,2,* and
Marie Hechelski
1
1
Laboratoire Génie Civil et géoEnvironnement (LGCgE), Yncréa Hauts-de-France, Institut Supérieur d’Agriculture, 48 Boulevard Vauban, 59046 Lille CEDEX, France
2
Equipe Biotechnologie et Gestion des Agents Pathogènes en agriculture (BIOGAP), Yncréa Hauts-de-France, Institut Supérieur d’Agriculture, 48 Boulevard Vauban, 59046 Lille CEDEX, France
*
Author to whom correspondence should be addressed.
Sustainability 2019, 11(18), 5093; https://doi.org/10.3390/su11185093
Submission received: 19 August 2019 / Revised: 9 September 2019 / Accepted: 15 September 2019 / Published: 18 September 2019
(This article belongs to the Special Issue Sustainable Development and Use of Plant Biomass for Marketable Resources)
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Abstract

:
Effects of three phosphorus fertilizers on the shoot biomass and on the accumulation of alkali, alkaline earth, and transition metals in the shoots and roots of ryegrass were studied with two contaminated garden soils. Phosphates were added in sustainable quantities in order to reduce the environmental availability of carcinogenic metals (e.g., Cd and Pb) and to enhance the bioavailability of alkali and alkaline earth metals as well as micronutrients needed by plants. Addition of Ca(H2PO4)2 was the most convenient way to (i) limit the concentration of Cd and Pb, (ii) keep constant the transfer of macro- and micronutrient from the soil to the ryegrass shoots, (iii) decrease the availability of metals, and (iv) increase the ratio values between potential Lewis acids and Cd or Pb in order to produce biosourced catalysis. For instance, the real phytoavailability was reduced by 27%–57% and 64.2%–94.8% for Cd and Pb, respectively. Interestingly, the real phytoavailability of Zn was the highest in the least contaminated soils. Even if soils were highly contaminated, no visual toxicity symptoms were recorded in the growing ryegrasses. This indicates that ryegrass is suitable for the revegetation of contaminated gardens. To promote the sustainable ryegrass production on contaminated soils for production of new organic fragrance and drugs in green processes according to REACH (Registration, Evaluation, Authorisation, and Restriction of Chemicals) regulation, two processes should be recommended: assisted phytostabilization of the elements, and then assisted phytoextraction by using chelators.

1. Introduction

Hyperaccumulators are mainly used in phytoextraction because they can contain up to 1%–2% of potentially toxic elements (PTEs). This advantage is combined with some drawbacks since there is no clear agronomic recommendation to produce hyperaccumulating plants. Consequently, the biomass of such plants is often low. The tolerant plants, in turn, do not accumulate PTEs as efficiently because they produce higher biomass yields as response to fertilizers or specific amendments. Thus, they are usually used in phytoremediation of soils contaminated by PTEs. Among the tolerant plants, ryegrass is currently used as green waste to make compost, to prevent the entrainment of windblown contaminated dust and the soil erosion, and to create public open space/parkland. It was selected for two mains reasons: its importance as a grazing crop and its preconization as a suitable plant for the revegetation of contaminated soils from metallurgical sites [1,2,3]. Among the 10 species of grass in the Poaceae family, the genus Lolium is one of the most known grasses used in the world as forage and lawn grasses. In France and in Europe, pasture and lawn seed are composed of annual ryegrass (Lolium multiflorum) and perennial ryegrass (Lolium perenne L.). Although defined as a non-hyperaccumulator plant, Lolium perenne L. has a strong resistance for PTEs. It was studied in assisted phytoextraction using biosurfactant (rhamnolipid), inorganic and organic chelatants (sulfates, citric acid, histidine, EDDS, EDTA, DTPA, NTA), chitosan or its derivatives, nanomaterials, hormones, and microbial agents with the aim at improving the translocation factor [4,5,6,7,8]. Lolium perenne L. has also been studied in rhizoremediation and in assisted phytostabilization [9,10,11]. The key of success of these technologies (used alone or in combination) lies also in its ability to reduce soil erosion, to enhance microbial activities in soils, and to improve soil fertility and carbon storage [12]. Remediation of contaminated soils by a combinational approach, using physical or chemical and biological technologies together with ryegrass [13,14,15] is used in phytoremediation of (i) soils contaminated by organic pollutants [16] and (ii) co-contaminated soils [17].
Emissions of dusts by two former smelters in the North of France have led to a significant increase of PTE concentrations in soils. Due to the accumulation of these pollutants in agricultural crops for foodstuffs, a high proportion of them did not comply with the European legislation [18,19]. Accumulation of PTEs in homegrown vegetables was demonstrated, and it was highlighted that most of the vegetables produced in kitchen gardens did not comply with the European foodstuff legislation [18]. This problem is not limited to northern France, but is present all over the world [20]. There are so challenges in assessing the health risks of consuming vegetables in metal-contaminated areas and, depending on the results, to make quick and good decisions about the management of these contaminated areas, including their reconversion.
Since phosphorus (P) amendments have been described as a promising technique to immobilize PTEs like Pb in contaminated soils, soluble, insoluble, and mixed phosphates were used to study their effects on mobility, bioavailability, and bioaccessibilty of PTEs [21,22,23,24]. Although H3PO4 was used as amendment, it is worth mentioning that it is never used as a P fertilizer. In fertilizers and in soil solution, P anion is typically either as H2PO4− or HPO42−, depending on soil pH. Also mineralization of organic P compounds produces phosphate anions that are prone to be (ad)sorbed, specifically onto the surface of poorly crystalline (hydr)oxides of Al or Fe according to a ligand-exchange mechanism. As for its counter-ions (e.g., K+, NH4+, Na+), they are important plant nutrients in soils because they are absolutely needed by plants. Utilization of phosphates has benefits in the long-term [25,26,27]. Nevertheless, soluble phosphates may be a potential source of eutrophication of groundwater and surface waters and mitigate out of the soil in runoff [28,29]. On the other hand, the use of insoluble phosphates is not a relevant option to maintain the soil productivity. The plant takes nutrients from the soil solution and not directly from the surface of solid material. However, it is noteworthy that P in the solution phase tends to be in equilibrium with P (ad)sorbed onto the surface of amorphous hydr(oxides) of Al and Fe. Depending on the P saturation degree of the sorbent surface, the concentration of soluble P is variable. Consequently, a relevant strategy consists of using moderately soluble phosphates like mono- and dicalcium phosphates (Ca(H2PO4)2 and CaHPO4), respectively named calcium dihydrogen phosphate and calcium hydrogen phosphate. The solubilization of these two crystalline phosphates in soil (Ca(H2PO4)2 ⇆ Ca2+ + 2H2PO4−; CaHPO4 ⇆ Ca2+ + HPO42−) are 18 g/100 g and 0.14 g/100 g, respectively, and the equilibrium constants are defined as log Ksp = −1.14 and log Ksp = −6.6 [30]. The current study was based on this strategy. Phosphates were added into the soil with a new approach in order to prevent the mobilization of carcinogenic compounds (e.g., Cd) and to limit their concentration in the aerial biomass of plants. The effects of Ca(H2PO4)2, CaHPO4, and the mixture of both phosphates on the accumulation of PTEs (Al, Cd, Cu, Mn, Pb, and Zn) and macro- and micronutrients (Fe, Na, K, Ca, Mg) in the shoots and roots of ryegrass (Lolium perenne L.) were reported. Three indicators were used to evaluate the phytoavailability of metals in order to define the strategy that can be used to manage contaminated soils, with the aim at using the biomass of ryegrass as a raw material in the manufacturing of biosourced catalyst to produce molecules of interest (pharmaceuticals, cosmetics).

2. Materials and Methods

2.1. Context of the Study and Soil Analysis

For more than a century, two lead and zinc smelters in northern France (Metaleurop Nord, Noyelles-Godault and Nyrstar, Auby) generated significant quantities of dust that have led to substantial contamination of the surrounding soils by PTEs like As, Cd, Co, Cr, Hg, In, Pb, and Sb [31]. Since the closure of Metaleurop Nord, most of the crops grown on these soils still present concentrations of Cd, Pb, and Zn higher than the maximum threshold allowed for food and feed [18,32]. In few cases, gardeners decided to change their cultural practices, while others took the decision to stop the gardening and to sow grass. In this context, two composite samples (0–25 cm) located not far from Metaleurop (Noyelles Godault, 3 km) and Nyrstar (Auby, 2 km) were sampled with a 6 cm diameter stainless steel auger and consisted of 10 cores, randomly taken in two kitchen garden soils (G1 and G2). Each composite sample was air-dried at a temperature below 40 °C and then crushed to pass through a 10 mm stainless steel sieve and crushed to pass through a 2 mm stainless steel sieve for the determination of physical and chemical parameters. Then, the composite samples were passed through a 250 µm sieve with an ultracentrifugal mill (ZM 200, Retsch, Hann, Germany) for the determination of total and extractable metal concentrations. After adding 5 g samples to 25 mL distilled water, the mixture was mechanically shaken for 5 min, allowed to settle for 2 h, and the pH of supernatant was measured in triplicates. The CaCO3 content was determined by measuring the volume of CO2 released by the reaction with HCl, handling a Bernard calcimeter [33]. The cation exchange capacity (CEC) was determined after percolation of 1.0 mol L−1 ammonium acetate solution at pH 7 [34]. The organic matter content was determined by dry combustion after burning 50 mg samples at 1000 °C in the presence of O2 [35]. Assimilable P (expressed in g P2O5 kg−1 of soil) was measured using an extraction by ammonium oxalate solution and spectrocolorimetric determination, according to the NF X 31–161 [36]. Particle size distribution was obtained through sedimentation and sieving, following the NF X 31–107 standard [37] by the INRA Soil Analysis Laboratory (Arras, France). Briefly, these soils had a clayey, sandy, loamy texture, although differed in the percentage of clay (Table 1). The pH of G1 and G2 was close to neutral, and the total carbonate content was 2.3-fold higher in G2 than in G1. This soil had the lowest cation-exchange capacity cmol+ kg−1 (24.1 vs. 12.5 cmol+ kg−1 for G1). The organic matter was slightly higher in the G2 topsoil than in G1, which presented 40% more P2O5 than in G2 (290 mg P2O5 kg−1 vs. 207 mg P2O5 kg−1).
Digestion of soil samples was performed using HNO3/H2O2/HCl hot-block (HotBlockTM Environmental Express®SC100, Charleston, SC, USA) digestion procedure, following the EPA 3050B method [38] with slight modifications. Briefly, 0.6 g of soil sample was acid-digested with nitric acid (HNO3, 70%, 6 mL) and heated at 90 ± 5 °C for 15 min. After cooling to less than 70 °C, 3 mL of HNO3 was added, and the mixture was heated to 90 ± 5 °C without boiling for 30 min. In absence of red vapor, the temperature was then maintained for 2 h. After cooling to less than 50 °C, 1.2 mL of water and 1.8 mL of H2O2 (30%) were slowly added. The solution was heated until effervescence subsided. After cooling, 6 mL of 12 M HCl was added, and the solution was heated at 90 ± 5 °C for 15 min. After cooling to room temperature, the volume was adjusted to 25 mL with ultra-pure water, and the digested-solutions were filtered over an acetate Millipore membrane (0.45 µm porosity) and were stored at 4 °C in acid-washed plastic bottles prior to analysis. Because the chemical procedure used to determine the total concentration of PTEs does not produce reliable information on the bioavailable reserves or on those becoming bioavailable in long run, bioavailable metals were determined according to the rhizosphere-based extraction protocol [39]. Briefly, soils samples (2 g) were mixed with 20 mL of 0.01 M low-molecular-weight organic acids in mixture (LMWOAs; acetic, lactic, citric, malic, formic acids with the following respective molar ratio 4:2:1:1:1). The soil suspension was shaken for 16 h, was centrifuged at 4530 rpm for 20 min, filtrated, and stored until analysis.

2.2. Soil Amendment and Design of the Incubation Experiment

Phosphates (calcium dihydrogen phosphate (Ca(H2PO4)2; P1), calcium hydrogen phosphate ((CaHPO4); P2), and a mixture of these two compounds (75/25; P3) were added as reagent-grade. Each amendment was applied to soils in five replicates (n = 5) at a 3:5 molar ratio of P/metal, according to the recommendation of Ma et al. [40]. Amended and unamended soils were aged for 8 weeks prior to planting in a greenhouse and were maintained at 60% field capacity with tap water (electrical conductivity, 10 dS m−1; pH, 7; (Cd) = 0.8 µg L−1; (Pb) = 1.7 µg L−1). Eight weeks after the amendment, each soil was homogenized, and 0.225 g of ryegrass (Lolium perenne L.) was sown into each of the 40 pots (diameter: 12 cm; height: 12 cm; 2 soils × 4 treatments × 5 replicates), containing 400 g of soils. The plants were grown for 10 weeks in a greenhouse at 20–27 °C, and the soil moisture was maintained at 60% field capacity with tap water. The experimental design was randomized twice per week in order to be exposed to uniform environmental conditions. After 10 weeks of growth, the plants were harvested. In the same time, the roots of ryegrass were sampled, rinsed with distilled water to remove any soil particle or dust. Plant tissues were oven-dried at 40 °C and crushed with an oscillating crusher in order to sieve them below 315 µm. Digestion of plant tissues was performed using HNO3/H2O2 hot-block digestion procedure. In this procedure, 300 mg of plant tissues was transferred to a 50 mL digestion tube. Nitric acid (70%, 5 mL) was added, and the mixture was heated at 65 °C for 20 min and then, at 90 °C for 45 min. After cooling to less than 50 °C, 1.2 mL of water and 1.8 mL of H2O2 (30%) were slowly added. The solution was heated at 90 °C for 45 min. After cooling to room temperature, the volume was adjusted to 25 mL with ultra-pure water, filtered, and stored until analysis.

2.3. Phytoavailability of Metals

The plant’s ability to uptake metals was calculated from the concentration of metals in plant tissues and the concentration of metals in soils [41]. The real phytoavailability of metals was expressed as percentage of metal mass absorbed by the aboveground biomass of ryegrass with respect to the metal mass in soil per each pot [42]. The ability of ryegrass to transfer metals from the roots to its aboveground parts was defined as the ratio of the metal concentrations in shoots to roots [41]. Note that the concentration of metals was expressed in mg kg−1, biomass and soil mass were expressed in g pot−1 and kg pot−1, respectively.

2.4. Analytical Techniques and Quality Control

The metal concentrations in soil and plant digests were determined by a flame atomic absorption spectrometer (FAAS, AA-6800, Shimadzu, Tokyo, Japan). High-intensity boosted-discharge hollow-cathode lamps (Cd, Pb, and Zn; Hamamatsu, Iwata, Japan) were used to avoid spectral interferences [43,44,45]. The lamps were operated between 6 and 12 mA for Al, Ca, Cu, Fe, K, Mg, Mn, and Na, and a deuterium lamp was used for the background correction. The limits of detection (LOD) and quantification (LOQ), respectively based on three and ten times the standard deviation of the blank (n = 10), are presented in Table 2. The quality of the combined hot-block digestion procedure and analytical technique was evaluated by analyzing certified reference materials (CRM BCR 141 R, ERM® CC141 and PCRM CTA-VTL-2). Metal concentrations in the digestion solution are summarized in Table 3. The metal concentrations in the three reference materials were generally in good agreement with the certified or indicative aqua regia soluble concentrations. The precision and the trueness values were found to be less than 9%, except for Cd in the ERM® CC141 soil, in which the concentration was very low (0.22 ± 0.04 mg kg−1 instead of 0.25 ± 0.04 mg kg−1; Table 3).

2.5. Statistical Analysis

Significant differences between the treatments and the control were determined using a one-way ANOVA. Significance was reported at p < 0.05. All statistical tests were performed using the software program XLSTAT 2017 (Addinsoft, Paris, France).

3. Results and Discussion

3.1. Concentration of Transition, Alkali, and Alkaline Earth Metals and Aluminum in Soils

Metal transitions were chemically defined as metals in the d-block of the periodic table (Cd, Cu, Fe, Mn, Pb, Zn). Alkali (Na, K) and alkaline earth (Ca, Mg) metals are in the first and the second period of this table, respectively, whereas aluminum (Al) is in the boron group. Due to the close proximity of the smelters and gardens (G1 and G2), Al, Cd, Cu, Fe, Mn, Pb, and Zn were considered as PTEs, whereas Na, K, Ca, and Mg were defined as macronutrients. It is noteworthy to mention that concentrations of Cd, Pb, Zn, and Cu in G1 were 2.1-fold, 3.1-fold, 2.4-fold, and 1.9-fold higher than concentrations of these PTEs measured in the ploughed layer of contaminated cultivated soils around Nystar [31]. Concentrations of Cd, Pb, Zn, and Cu in G2 were 2.2-fold, 3.1-fold, 7.0-fold, and 3.9-fold higher than concentrations of these PTEs measured in the ploughed layer of contaminated cultivated soils around Metaleurop Nord [31]. These results were consistent with those obtained in previous studies, in which the authors showed that the contamination level of kitchen garden soils was greater than that in agricultural soils located in the same environmental context [46]. Pelfrêne et al. [47] reported that the mean concentrations of Mn, Fe, and Al in agricultural soils (n = 390) located in the studied area were 370 ± 140 mg kg−1, 22,090 ± 10,940 mg kg−1, and 9080 ± 6360 mg kg−1, respectively. Regarding these concentrations, it may be accepted that similar concentrations of Mn were obtained in soils G1 and G2, whereas the concentrations of Fe and Al were significantly highest and lowest. Although heterogeneous and variable concentrations were highlighted in garden soils from the studied area [48], no significant difference between the concentrations of Al, Cd, Cu, Fe, Mn Pb, Zn, Na, K, Ca, and Mg in soils before potting was highlighted. Note that concentrations of Cd, Pb, Zn, Cu, Ca, and Mg were higher in soil G2 than in soil G1 (1.24-fold, 3.21-fold, 1.94-fold, 2.39-fold, 3.45-fold, 1.93-fold, respectively), whereas Fe was the lowest in G2 (0.95-fold and 0.88-fold, respectively) and Al, Mn, Na, and K were rather similar in the two soils.

3.2. Biomass, Concentrations of Transition, Alkali, and Alkaline Earth Metals and Aluminum in the Ryegrass Shoots

3.2.1. Shoot Biomass of Ryegrass

The shoots of ryegrass were cut ten weeks after sowing. The fresh weight biomass was from 23.5 g to 26.5 g for ryegrass grown on unamended and amended soils G1, whereas for soils G2, they were in the range 23–26.8 g. In view of the different water content in the aerial parts of ryegrass, shoots were dried at 40 °C (Figure 1). The dried shoot mass of ryegrass grown on G1 and G2 was on average 8.57 ± 052 mg and 8.68 ± 0.50 mg, respectively. In view of PTE concentrations in G1 and G2 soils (Table 4), these results revealed that the concentration of PTEs in the aerial parts of ryegrass did not only depend on the total concentration of PTEs in soils, but also on the bioavailable concentrations (soluble, labile, and exchangeable), as shown in other studies [6,9,49]. Moreover, due to the absence of visual toxicity symptoms (no noticeable wilting and slight leaf chlorosis), Lolium Perenne L. exhibited a metal tolerance when facing high PTE concentrations in soils. This finding correlated well with the fact that ryegrass was described as a suitable plant for the revegetation of contaminated soils from metallurgical sites [1]. The effects of phosphates on the biomass were the same for both soils, but were amendment-dependent (Figure 1). Calcium dihydrogen phosphate (P1) significantly increased the shoot biomass, whereas a significant decrease was observed with calcium hydrogen phosphate (P2). No significant effect was reported with the mixture of phosphates (P3). The chemical properties of P1 and P2 are very easy to distinguish since the ratio Ca/P values are 1.294 and 0.647, respectively. According to Chen et al. [50], calcium phosphate with a Ca/P ratio below 1.67 is considered as acid species. Consequently, the acidity of P2 is higher than that of P1. This theory was supported by the pH of the solution containing P1 and P2 for G1 (4.57 and 7.67, respectively) and G2 (4.11 and 8.05, respectively).

3.2.2. Concentrations of Transition, Alkali, and Alkaline Earth Metals and Aluminum in the Shoots of Ryegrass

Lolium perenne L. grew on G1 and G2, and metals, like PTEs (Al, Cd, Cu, Mn, Pb, and Zn), as well as macro- and micronutrients (Na, K, Ca, Mg, Fe) were measured in the shoots (Table 5). Although the concentrations of (i) Cd, Pb, Zn, Cu were higher in G2 than in G1 and (ii) Al and Mn were similar in the two soils (Table 4), the concentrations of these PTEs (except for Pb) were higher in the shoots of ryegrass grown on G1 than on G2 (Table 5). This result reflects a better stability of PTEs in the soil G2 than in G1, which may be explained by the highest organic matter and clays contents in G2 (Table 1). Indeed, common clays, such as kaolin and phyllosilicates (montmorillonite, bentonite, attapulgite, sepiolite, vermiculite) were used in many studies for ex-situ and in-situ immobilization of PTEs in soils and for the hazard limitation of these pollutants to plants [51,52]. As shown in Table 5, the best effects of fertilizers on the phytoavailability of PTEs were obtained in soil G1, suggesting that the soluble and labile pools of PTEs were the greatest in this soil. The three phosphorus amendments significantly decreased the PTEs concentrations (except Mn) and Fe in the shoots of ryegrass grown in G1. The best effects were obtained with P1 (Ca(H2PO4)2), which confirmed the successful ligand immobilization of divalent PTEs and so, the lowest accumulation of PTEs [25,53,54]. Moreover, Ca(H2PO4)2 is gradually transformed into more stable phosphates like octocalcium phosphates and apatites, which are known for their reactivity towards PTEs like Pb to form stable phosphates such as pyromorphite, unavailable for plants [30,42,55]. On the other hand, it can react with Fe, Al, and Ca to form secondary P minerals by precipitation [56]. This could explain the large decrease of Fe and Ca in the shoots of ryegrass grown on G1 and G2. The basic effects of Ca(H2PO4)2 may contribute to limit the concentration of macro- and microelements like Zn and Fe since it was the dominant species for pH between 4 and 5.5 [57].
Although the concentration of alkali and alkaline earth metals were in the following orders Ca > K > Mg > Na in G1 and Ca > Mg > K > Na in G2 (Table 4), those in the shoots of ryegrass grown on soils G1 and amended soil G2 were K > Ca > Na> Mg, but Ca > K > Na > Mg for ryegrass grown on the unamended soil G2. This result may be explained by the (i) decrease of Ca concentration in the shoots of ryegrass in presence of phosphates (up to 25%; Table 5) and (ii) the high concentration of Ca in G2 (Table 4). The immobilization of Ca using phosphates has been also observed for ryegrass grown on G1 (except for the mixture of phosphates), and the same trends were highlighted for Mg and Na. Note that the transfer of these cations from the soil to the ryegrass shoots was more limited using P1 than P2 and P3. In contrast, the phosphates did not have effects on the availability of K (Table 5). This is probably due to the fact that K is a primary nutrient and was defined as the most important element for plant nutrition [58,59]. Indeed, a minimum level of K in vacuole is necessary to maintain turgor and to avoid modifications of the metabolic processes and a decline in the growth of plants [60]. The ratio K/(Ca + Mg) is commonly used to define the risk of contracting grass tetany by cattle and to compare the assimilation of monovalent and divalent cations by plants [61,62]. This ratio ranged from 1.32 to 1.87 for G1, reflecting a higher absorption of monovalent over divalent cations, and was in the range 0.71–1.00 for G2, highlighting a higher absorption of divalent over monovalent cations. These ratio values help to understand why for each modality, the biomass of ryegrass grown on G1 and G2 was not statistically different. Except the pH, the organic matter, and the clay contents, everything suggests that the biomass of ryegrass is affected by the concentration of PTEs and the ratio K/(Ca + Mg), both parameters having antagonist effects. The highest shoots biomass, obtained for the two soils amended with P1 (Figure 1) could so be explained by the lowest concentration of PTEs in the aerial parts and the highest ratio values (1.71 ± 0.15 for G1P1 and 0.97 ± 0.07 for G2P1).

3.3. Concentrations of Transition, Alkali, and Alkaline Earth Metals And Aluminum in the Roots of Ryegrass

The PTEs, alkali and alkaline earth metals concentrations are summarized in Table 6. The concentrations of Cd, Pb, Fe, and Ca were significantly higher in the roots of ryegrass grown on the unamended soil G2 than those on the unamended soil G1. These results correlated well with the fact that the total concentrations of Cd, Pb, and Ca were higher in G2 than in G1. These trends were also observed for soils amended with P1, P2, or P3, since the most substantial increase of the concentration of Cd, Pb, Fe, and Ca by phosphates occurred in G2. The major effect was highlighted in G2 amended with P2, since the concentrations of Cd, Pb, Fe, and Ca were up to 55.4 mg kg−1, 238 mg kg−1, 2657 mg kg−1, and 4579 mg kg−1, respectively. Although the concentrations of Zn, Cu, and Mg were the highest in G2, their concentrations in the roots of ryegrass from G1 were higher than those from G2 (Table 6). The same trends were obtained after phosphates, except for Cu, even if its concentration remained at low level (from 20.4 to 38.5 mg kg−1 and from 13.2 to 38.9 mg kg−1 in amended soils G2 and G1, respectively). As it was observed for Cd, Pb, Fe, and Ca, the accumulation of Zn, Cu, and Mg was favored in amended soils G1 and G2 after amendment using P2. No significant differences between the concentrations of Al, Na, and K in soils G1 and G2 and in roots of ryegrass from both soils were highlighted (Table 6). Depending on phosphates and soils, significant increases of Al, Na, and K concentrations in the roots of ryegrass were observed, especially for amended soils G1 and G2 (except K) using P2.
It is well known that the bioavailability of metals depends on the radius, the ionic charge, and the first hydrolysis constant of metals [63,64,65]. In addition, the speciation of metals can be modified by the development of the physicochemical and biological processes (metal uptake, accumulation, sequestration, and metabolization) around the plant’s rhizosphere [66,67]. The variation in pH and organic carbon in the topsoil is due to the release of organic compounds from the plants and microbial activities. Among these organic compounds, flavonoids, lipids, sugars, amino acids, and LMWOAs such as acetic, citric, oxalic, propionic, butyric, malic, fumaric, malonic, and succinic acids have been widely found in the plant’s rhizosphere [68,69,70]. These organic compounds react with metals to form complexes, which are adsorbed by the roots and then translocated into the aboveground parts of plants, and have been recently used as environmental friendly remediation of contaminated soils [71,72]. For a better understanding of our results, chemical extraction was firstly performed on unamended and amended soils with a mixture of organic acids and then, the metal phytoavailability was studied using three indicators.

3.4. Evaluation of the Phytoavailability Using a Mixture of Organic Acids

Acetic and citric acids are the two main root exudates that have been widely used to assess the bioavailability of metals [73,74,75]. Their chemical actions on the soil solid phases are the solubilization of PTEs, resulting from the dissolution of carbonates/Fe oxides/hydroxides and the complexation of PTEs. Indeed, they were used to simulate the complexing behavior of the root exudates [39,76,77]. These acids were used in mixture with others like lactic, malic, and formic acids, and the resulting solution, currently called low-molecular-weight organic acids mixture, was described as a robust approach in different context to evaluate the bioavailability of PTEs in acidic, neutral, and slightly alkaline soils [39,78,79]. In this condition, the extractable metal may be associated to the short-term available pool of PTEs [80,81]. Whatever the conditions, the extractable PTEs concentrations in G1 were in the following decreasing order Zn > Fe > Al > Mn > Cd > Pb > Cu, whereas in unamended and amended soils G2, the order was Fe > Zn > Al > Mn > Cd > Pb > Cu (Table 7). As shown in the previous section, the total concentrations of PTEs in both G1 and G2 soils were ordered in the following sequence Fe > Zn > Al > Pb > Mn > Cu > Cd. This result demonstrates that the extractable metal was not only dependent on the total PTE concentrations, but also on their affinity with soil substrates (organic and mineral) to form stable chemical compounds. Moreover, note that the concentrations of extractable Cd, Cu, Mn, and Zn were the highest in unamended and amended soil G1. Once again, this result confirms there is no evident relation between extractable and total PTEs concentrations, since the total concentrations of these PTEs were the highest in soil G2.
Interesting findings were the relation between the total PTEs concentrations, their concentrations in the (i) LMWOAs extracting solutions, (ii) shoots of ryegrass, and (iii) root of ryegrass. Indeed, concentrations of major pollutants (Cd, Pb, Zn, and Cu), resulting mainly from the emission of dusts in the operating period of the Pb and Zn smelters, were highest in the roots of ryegrass grown on the most contaminated soil G2. The highest concentrations in the shoots of ryegrass were obtained from soil G1, in which the extractable PTEs concentrations were the highest. Acquisition of information about the chemical availability of PTEs before biomass production is so crucial. This becomes all the more important when optimizing a phytomanagement technique with the aim at (i) producing foodstuff and feedstuff, (ii) creating added value, like the production of biosourced catalysts to synthesize molecules of interest [82,83,84,85], and (iii) recovering Cd, Zn, and Ni used in many industrial applications [85,86,87].
Extractable concentrations of alkali (K and Na) and alkaline earth (Ca and Mg) metals correlated well with those measured in the roots of ryegrass from G1 (K > Na > Ca > Mg). This was not the case for roots of ryegrass from soil G2 (K > Ca > Mg > Na) due to the low extractable concentration of Na (from 22 to 31 mg kg−1; Table 7), a nonessential element for plants [88]. The concentration order of K, Ca, and Mg correlated well with the theory. Indeed, roots of plants are able to mobilize the nonexchangeable K from clays to avoid its depletion [89,90]. Although Ca and Mg are both divalent cations, their extractable concentrations were lower than that of K. This result is somewhat at odds with the theory, since the stability constant reflects a best stability of the complex resulting from the reaction between divalent cations with LMWOAs. However, it is well known that extractable concentration of cations also depends on their total concentration. It is worth mentioning the different orders between alkali and alkaline earth metals in the shoots of ryegrass and those measured in LMWOAs extracting solutions. This finding confirmed that artificial chemical solutions cannot (i) mimic the biological and physiological process and (ii) take into consideration the dynamic of the transformation in the rhizosphere environment. For instance, root exudates, like LMWOAs, are able to react with cations in order to produce soluble organometallic complexes in the microenvironment of the rhizosphere, particularly when these cations are nutrients [68,91,92]. Therefore, the phytoavailabillity of PTEs, alkali and alkali earth metals was studied using three mathematical indicators: uptake ability (BCF), real phytoavailability, and transfer (TF) for a better understanding.

3.5. Phytoavailability of PTEs, Alkali and Alkaline Earth Metals in Unamended and Amended Soils

The set of data related to the three indicators of the phytoavailability is presented in Figure 2. The first ratio used to evaluate the effects of phosphates on the phytoavailability of PTEs, alkali and alkaline earth metals was the plant/substrate ratio. This ratio is usually used to assess the plant’s ability to uptake metals. It was calculated considering metals in the plant parts (roots and shoots) and the concentration of metals in the soil on which the ryegrass grow. As shown in Figure 2, this indicator, commonly named bioconcentration factor (BCF; [34]) differed according to the metals and the soils. The BCF values of monovalent cations (Na and K) were the highest, ranging from 35.7 to 80.4 and from 10.1 to 16.7 for Na and K, respectively. For alkaline earth metals (Ca and Mg), the BCF values were in the range 1.8–3.0 for Ca and 2.3–4.5 for Mg on unamended and amended soils G1, whereas they were reduced by half on the unamended and amended soils G2. Note that BCF values of Ca and Mg were slightly the lowest in presence of P1. This trend was also observed for Cd and correlated well with the fact that competition between Ca and Cd may exist since the ionic radius of Cd2+ (0.097 nm) is very close to that of Ca2+ (0.094 nm) and the valence of both cations is the same. The physicochemical characteristics of Cd and Ca ions can contribute to explain the highest BCF value for Cd among the studied PTEs, the BCF order being Cd > Zn > Mn > Cu > Al > Pb > Fe (Figure 2). This order highlights the high phytoavailability of Cd in the soil studied, the BCF value being in the range 1.7–3.4. This result is consistent with the fact that Cd ions move through the plant tissues using Ca channels by active transport, since Ca ion is an essential nutrient for plants [93].
Some studies reported interesting discussions about the potential utilization of plants for phytoextraction or phytostabilizatation [41]. According to Yoon et al. [94], BCF and TF (translocation factor) may be used to establish if a plant is a good candidate or not for phytoremediation purposes. When BCF and TF are greater than one, plants have the potential to be used for phytoextraction; when BCF is higher and TF is less than one, the plant is defined as a metal-tolerant plant; when BCF and TF are less than one, plants have the potential to be used for phytostabilization. In view of the TF values, the second ratio studied in the current study, three evident metal groups may be established. The first is composed of Cd, Cu, Fe, Pb, and Zn, for which TF was below 1, the second was formed by alkali and alkaline earth metals for which TF was higher than one, and in the third group, Al and Mn, for which the BCF values depended on the soil studied and the modality. For instance, the BCF values for Mn were higher than one for ryegrass grown in unamended and amended soil G1, whereas they were below one for ryegrass grown on unamended and amended soil G2. In contrast, P1 and P2 slowed down the ability of ryegrass to uptake Al in soil G1 (BCF < 1), whereas BCF values were less than one in unamended and amended soil G2. There is so no doubt on the ryegrass capabilities of extracting Na and K, which may improve the aggregation of soil particles over the long-term. On the other hand, as regards the BCF and TF values and under the experimental conditions, ryegrass may be defined as a metal-tolerant plant that can be used for phytostabilization. This point ties up the findings of many authors that selected ryegrass as a suitable plant for the revegetation of contaminated soils from metallurgical sites [1], able to remove Cd from soils [95].
The third ratio was related to the real phytoavailability of PTEs, alkali, and alkaline earth metals and takes into account the concentration of metals in plant and soil, the above-ground biomass, and the soil mass. As shown in Figure 2, the real phytoavailability was higher in the less contaminated soil G1 than in soil G2. This result correlated well with the extractable metal concentration measured in the LMWOAs solution for Cd, Zn, Ca, Mn, Na, and K. Recently, similarities between the real phytoavailability of Pb, Cu, and Zn and their water extractability have been found [42]. The real phytoavailability order was Na > K > Mg > Ca > Cd > Mn > Zn > Cu > Al > Pb > Fe. The main effects of phosphates on the real phytoavailability of PTEs, alkali, and alkaline earth metals were obtained using DCP on soil G1, in which the availability of metals were the highest. With this amendment, the phytoavailability of Cd, Pb, Cu, and Al was reduced by 27%–57%, 64.2%–94.8%, 18.3%–43.1%, and 50.1%–89.4%, respectively. Interestingly, the real phytoavailability of Zn was higher in soil G1 than in soil G2 for all modalities. This result is consistent with the findings of Sarret et al. [96]. The authors highlighted the highest lability of Zn in soil located around the Auby’s smelter (Nyrstar) in comparison with those around the former smelter Metaleurop Nord. In a same way, we can assume that the lability of Cd, Cu, Mn, Ca, Mg, Na, and K is the highest in the soils located in the surrounding of the Nyrstar smelter. Recent studies demonstrated the importance of the isotopic signature in the phytoavailability of few metals like Pb, Cu, Zn, and Mg [97,98]. According to the authors, heavy Zn isotopes are mainly present in the roots, whereas light Zn isotopes are transferred in the aerial parts. Consequently, the difference in the isotopic fractionation of Zn in the soils around the former smelter Metaleurop Nord and Nystar could explain the difference between the TF values of Zn in ryegrass grown on G1 and G2 [97]. Further studies are so necessary to define the isotopic fractionation of PTEs like Cd, Pb, Cu, and Al around these two Pb and Zn smelters for a better understanding of the PTEs transfer from the soil to the different plant tissues.

3.6. Potential Application of the Aerial Parts of Ryegrass

Based on recent studies described by Hechelski et al. [82], the aerial parts of ryegrass may have potential interest in organic chemistry and polymer science. Indeed, recent studies reported the use of metals from hyperaccumulating plants biomass to produce ecocatalysts. Among them, Al, Cu, Fe, Mn, and Zn are of great interest since they were transformed into Lewis acids (LA), an important class of catalysts used in many organic transformations [82,83,84,85]. It is well accepted that the metal concentration in the aerial parts of plants has to be higher than 1000 mg kg−1 DW (Dry Weight) for the conception of ecocatalysts [99,100]. In view of the results described in Table 5, the aerial parts of ryegrass should be interesting for this application, the concentration of potential LA (Al, Cu, Fe, Mn, and Zn) ranging from 792 to 1280 mg kg−1 DW. However, the presence of Cd and Pb in the plant biomass may pose a problem for human health since both metal are defined as carcinogenic, mutagenic, and reprotoxic substances. It is worth noting that in the present study, Cd and Pb were in small amounts in the plant biomass in comparison with potential LA, the ratios LA/Cd ranging from 104 to 193, and LA/Pb being in the range 41–1534.

4. Conclusions

Calcium dihydrogen phosphate (Ca(H2PO4)2), calcium hydrogen phosphate (CaHPO4), and a mixture of both phosphates were added in sustainable amounts to contaminated garden soils in order to drop the carcinogenic, mutagenic, and reprotoxic metals (e.g., Cd, Pb) and to rise up the transfer of nutrients. Despite the concentration of PTEs (Al, Cd, Cu, Mn, Pb, and Zn) in soils (up to 10.03 g kg−1), no visual toxicity symptoms was recorded, making this plant suitable for the revegetation of contaminated gardens. The concentrations of PTEs in the ryegrass shoots were not dependent on their concentrations in soils, suggesting a relation between the phytoavailability of PTEs and their stability in soils, mainly explained by the organic matter and clay contents. In contrast, the concentrations of metals in the roots of ryegrass depended on the concentrations of metals in soils and increased in amended soils.
The shoot biomass of ryegrass significantly increased with the application of Ca(H2PO4)2, a negative effect was highlighted using CaHPO4, whereas no effect on the biomass was observed using the mixture of phosphates. Among the three studied amendments, Ca(H2PO4)2 was the most appropriate to our objectives: (i) limitation of the concentration of Cd and Pb in the ryegrass shoots, especially from soil G1, (ii) ability to maintain the transfer of macro- and micronutrients, (iii) limitation of the availability of PTEs in soil where they were the highest, (iv) improving the ratio values between potential Lewis acids and Cd or Pb, in order to use transformed shoot biomass of ryegrass as biosourced catalysts. This is the main objective of the second part of the current study.

Author Contributions

Formal analysis, Investigation, Methodology, Writing—original draft and editing, C.W.; Writing—review, M.H.

Funding

This research was funded by YNCREA Hauts-de-France—ISA

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Effects of P fertilizers in the fresh biomass of ryegrass shoots from G1 and G2 soils. Vertical bars indicate standard deviation (n = 5). Letters refer to significant differences (p < 0.05).
Figure 1. Effects of P fertilizers in the fresh biomass of ryegrass shoots from G1 and G2 soils. Vertical bars indicate standard deviation (n = 5). Letters refer to significant differences (p < 0.05).
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Figure 2. Translocation factors, uptake ability, and phytoavailability of PTEs, alkali, and alkaline earth metals (mean ± standard deviation; n = 5).
Figure 2. Translocation factors, uptake ability, and phytoavailability of PTEs, alkali, and alkaline earth metals (mean ± standard deviation; n = 5).
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Table
Table 1. Physicochemical parameters of G1 and G2 soils.
Table 1. Physicochemical parameters of G1 and G2 soils.
SoilClay aCoarse Silt aFine Silt aCoarse Sand aFine Sand apHCaCO3 aCECOMP2O5 b
G11893151901101967.39 ± 0.037.2 ± 0.123.8 ± 1.271.2 ± 1.3290 ± 2
G2288324196451477.21 ± 0.0216.2 ± 0.212.5 ± 1.295.8 ± 2.0207 ± 2
a g kg−1; b mg kg−1; CEC: Cation-exchange capacity in cmol+ kg−1; OM: Organic matter. pH, CaCO3, CEC, OM and P2O5 were expressed as mean and standard deviation (n = 3).
Table
Table 2. Limits of detection (LOD) and quantification (LOQ) in µg L−1.
Table 2. Limits of detection (LOD) and quantification (LOQ) in µg L−1.
ElementCdPbZnAlCaCuFeKMgMnNa
LOD2.141.01.5156.032.249.041.95.012.04.15.0
LOQ7.0136.75.0520.0107.3163.3139.716.740.013.716.7
Table
Table 3. Certified and measured concentrations of PTEs (mg kg−1) in reference materials—statistic indicators of the analytical quality.
Table 3. Certified and measured concentrations of PTEs (mg kg−1) in reference materials—statistic indicators of the analytical quality.
MetalCRM BCR 141 RERM® CC141PCRM CTA-VTL-2
Certified ValueObtained Value (n = 3)Precision (%)Trueness (%)Certified Value Obtained Value (n = 3)Precision (%)Trueness (%)Certified ValueObtained Value (n = 3)Precision (%)Trueness (%)
Al32,200 ± 600 a32,412 ± 1350.41−0.66----1682 b1614 ± 503.014.04
Cd13.96 ± 0.4613.31 ± 0.090.67−4.660.25 ± 0.040.22 ± 0.0418.20−13.601.52 ± 0.171.50 ± 0.138.70−1.31
Cu46.9 ± 1.844.6 ± 1.63.59−4.9012.4 ± 0.912.7 ± 0.32.360.2418.2 ± 0.919.8 ± 0.21.018.79
Fe25,850 ± 40024,955 ± 16056.43−3.46-11901 ± 780.66-1083 ± 331088 ± 353.210.46
Mn653 ± 20664 ± 71.051.68387 ± 17400 ± 41.003.3679.7 ± 2.683.4 ± 3.54.204.60
Pb51.3 ± 2.050.0 ± 1.22.40−2.5332.2 ± 1.430.6 ± 1.75.55−4.9722.1 ± 1.221.8 ± 1.25.50−1.35
Zn270 ± 8277 ± 1.60.572.5950 ± 447 ± 12.12−6.0043.0 ± 2.142.9 ± 2.25.13−0.23
a indicative value; b only one value.
Table
Table 4. Concentration (mg kg−1; n = 5) of metal transition, alkali, and alkaline earth metals in soils G1 and G2 before the addition of phosphates.
Table 4. Concentration (mg kg−1; n = 5) of metal transition, alkali, and alkaline earth metals in soils G1 and G2 before the addition of phosphates.
MetalSoil G1Soil G1 + P1Soil G1 + P2Soil G1 + P3Soil G2Soil G2 + P1Soil G2 + P2Soil G2 + P3
Cd17.2±1.617.6±0.817.9±0.716.9±1.021.7±1.021.3±1.221.3±2.021.9±1.1
Pb503±47478±50515±26537±191656±1631573±1541607±1341748±92
Zn2459±3262274±1592221±1612359±1424651±5534512±5564162±5554821±332
Cu45±145±346±245±1108±9105±9102±9116±5
Mn404±59402±41391±45390±34402±24357±35371±47391±14
Fe36,565±346535,691±103632,824±382535,753±177232,124±194830,593±213129,694±238931,118±776
Al2464±2972637±2902746±4712572±1612205±2802132±1682133±4912537±163
Ca7783±6558403±11777988±16897226±107126,685±716526,440±380725,352±377626,492±3614
Mg1789±1061767±1191682±1721568±2043434±4333332±3393129±1933269±145
Na363±48356±16292±14390±110382±62373±65317±49390±27
K2184±1002168±1522127±1492259±1622293±1452281±1752106±1452138±103
P1: calcium dihydrogen phosphate; P2: calcium hydrogen phosphate; P3: mixture of P1 and P2 (75/25).
Table
Table 5. Concentration (mg kg−1; n = 5) of metal transition, alkali, and alkaline earth metals measured in the shoots of ryegrass, grown in unamended and amended soils G1 and G2.
Table 5. Concentration (mg kg−1; n = 5) of metal transition, alkali, and alkaline earth metals measured in the shoots of ryegrass, grown in unamended and amended soils G1 and G2.
MetalSoil G1Soil G1 + P1Soil G1 + P2Soil G1 + P3Soil G2Soil G2 + P1Soil G2 + P2Soil G2 + P3
Cd11.0±0.17.1±0.37.7±0.99.0±0.23.3±0.03.6±0.13.5±0.72.8±0.1
Pb7.0±0.51.4±0.83.8±1.07.2±0.612.7±0.611.3±2.26.8±1.27.1±0.6
Zn737±5566±28587±11624±10273±2295±13297±16271±3
Cu4.5±0.33.5±0.13.2±0.24.3±0.23.3±0.12.3±0.72.0±0.32.7±0.1
Mn164±1167±12144±19199±360±053±674±941±0
Fe184±137±256±40210±3116±172±2024±520±2
Al172±855±2375±32152±5106±7106±46125±3228±1
Ca13,390±35410,466±134010,642±97613,936±35219,027±614,408±112817,919±39814,656±278
Mg4416±183632±703761±3574485±914162±243502±3253903±3793343±115
Na12,105±9710306±18812,114±111711,793±37015,181±30611,854±100913,907±255610,404±122
K24,533±12923916±26920,392±387124,430±52316,625±6817,315±45716,832±118017,686±91
P1: calcium dihydrogen phosphate; P2: calcium hydrogen phosphate; P3: mixture of P1 and P2 (75/25).
Table
Table 6. Concentration (mg kg−1; n = 5) of metal transition, alkali, and alkaline earth metals measured in the roots of ryegrass, grown in unamended and amended soils G1 and G2.
Table 6. Concentration (mg kg−1; n = 5) of metal transition, alkali, and alkaline earth metals measured in the roots of ryegrass, grown in unamended and amended soils G1 and G2.
MetalSoil G1Soil G1 + P1Soil G1 + P2Soil G1 + P3Soil G2Soil G2 + P1Soil G2 + P2Soil G2 + P3
Cd19.7±0.919.2±1.925.0±3.421.1±2.243.7±6.351.0±10.755.4±6.149.6±4.6
Pb33.9±4.232.4±5.634.3±1.633.9±4.6122.4±26.9222.8±46.7240.1±15.1200.7±50.2
Zn1610±1571409±2071973±6401545±148954±241105±3161366±781009±155
Cu23.4±3.125.8±7.419.1±4.619.0±4.321.7±2.034.9±2.129.4±3.926.9±5.0
Mn104±6118±30117±9146±4470±1371±6105±2172±6
Fe1114±1901100±1671267±1381234±2482302±1372541±1702657±472506±180
Al185±51234±81281±60232±75213±52320±64381±58300±76
Ca2666±712676±4403664±7822761±3183633±3684129±6504579±4214481±660
Mg954±27833±1201179±207936±75980±48947±2501033±58915±57
Na5220±7434688±8886340±8634724±6604630±3883582±5696221±3375415±1458
K7317±6378011±135410,303±22908239±11438992±12077647±10737672±8077778±1187
P1: calcium dihydrogen phosphate; P2: calcium hydrogen phosphate; P3: mixture of P1 and P2 (75/25).
Table
Table 7. Extractable concentration of metal transition, alkali, and alkali earth metals (mg kg−1; n = 5) using low-molecular-weight organic acids in mixture.
Table 7. Extractable concentration of metal transition, alkali, and alkali earth metals (mg kg−1; n = 5) using low-molecular-weight organic acids in mixture.
MetalSoil G1Soil G1 + P1Soil G1 + P2Soil G1 + P3Soil G2Soil G2 + P1Soil G2 + P2Soil G2 + P3
Cd1.6±0.01.5±0.11.6±0.11.6±0.00.2±0.00.2±0.10.2±0.00.2±0.0
Pb1.3±0.11.3±0.11.3±0.11.4±0.12.2±0.12.2±0.12.1±0.12.2±0.2
Zn319±5291±34288±45328±1265±2759±1959±1561±2
Cu0.8±0.10.8±0.10.8±0.10.8±0.00.5±0.00.6±0.20.5±0.00.5±0.0
Mn26±127±824±426±222±122±121±222±1
Fe115±9117±27113±17108±2142±13153±24131±24142±23
Ca135±27153±20158±23152±11214±13199±14218±28198±10
Mg82±585±680±679±1121±7121±7125±4124±4
Na170±3156±17165±26172±125±228±424±224±1
K364±9363±8372±7375±3256±9259±4256±5251±6
P1: calcium dihydrogen phosphate; P2: calcium hydrogen phosphate; P3: mixture of P1 and P2 (75/25).

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Waterlot, C.; Hechelski, M. Benefits of Ryegrass on Multicontaminated Soils Part 1: Effects of Fertilizers on Bioavailability and Accumulation of Metals. Sustainability 2019, 11, 5093. https://doi.org/10.3390/su11185093

AMA Style

Waterlot C, Hechelski M. Benefits of Ryegrass on Multicontaminated Soils Part 1: Effects of Fertilizers on Bioavailability and Accumulation of Metals. Sustainability. 2019; 11(18):5093. https://doi.org/10.3390/su11185093

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Waterlot, Christophe, and Marie Hechelski. 2019. "Benefits of Ryegrass on Multicontaminated Soils Part 1: Effects of Fertilizers on Bioavailability and Accumulation of Metals" Sustainability 11, no. 18: 5093. https://doi.org/10.3390/su11185093

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