Organic Materials Could Improve the Phytoremediation Efficiency of Soil Potentially Hazardous Metal by <i>Sedum alfredii</i> Hance

Peifan Wang; Shengting Rao; Jia Fang; Yongqiang Lv; Anying Zhao; Zhengqian Ye; Weijun Fu

doi:10.32604/phyton.2022.019368

Organic Materials Could Improve the Phytoremediation Efficiency of Soil Potentially Hazardous Metal by Sedum alfredii Hance

Peifan Wang1,#, Shengting Rao1,#, Jia Fang2, Yongqiang Lv2, Anying Zhao2, Zhengqian Ye2 and Weijun Fu1,*

1State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, 311300, China
2Key Laboratory of Soil Contamination Bioremediation of Zhejiang Province, Zhejiang A&F University, Hangzhou, 311300, China
*Corresponding Author: Weijun Fu. Email: fuweijun@zafu.edu.cn
#These two authors contributed equally to this work
Received: 19 September 2021; Accepted: 21 December 2021

Potentially hazardous metal (PHM) pollution of arable soils is attracting more and more attention worldwide due to the high toxicity, persistence and easy-bioaccumulation characteristics of PHMs [1]. It is urgent to find economic, efficient and feasible remediation technology for soil PHM pollution [2]. The general remediation methods of soil PHM pollution refer to physicochemical measures such as soil washing, surface capping and electro-kinetic extraction, bioremediation and phytoremediation [3,4]. However, the physicochemical methods cannot deal with large-scale soil pollution, which also can further lead to soil structure damage, biological activity decrease and soil quality degradation [5,6]. Compared with physicochemical remediation methods, phytoremediation has the advantage of in-situ treatment, low cost, simplicity of practice and compatibility with environmental aesthetics [7,8]. Because of its obvious advantages, phytoremediation has been received increasing attention and becomes one of the hot-spots in the environmental research field [9–11]. But the phytoremediation also has deficiencies such as lower remediation efficiency in highly polluted soil, slow remediation process, longer remediation cycle and is limited by practically environmental factors [12,13]. Therefore, it is important to take necessary measures to improve the efficiency of phytoremediation [14–19].

Applying organic fertilizer or organic material into soils is a practicable method, which could improve soil fertility and activate soil PHMs by dissolved organic matter (DOM) such as small molecule organic acids, leading to the availability change of PHMs for plants uptake [20]. Pan et al. found that organic fertilizer was beneficial to increase the content of exchangeable Cu and Cd in topsoils, which further promoted the uptake and accumulation of Cu and Cd by wheat [21]. In addition, Wei et al. [22] reported the remediation efficiency of hyperaccumulator (Rorippa globose) on Cd in contaminated soil was significantly improved, with the application of chicken manure. However, Wu et al. [23] reported that 2% humus combined with 2% lime application could immobilize the potentially hazardous metal in Cd- and Cu-polluted soil. While phytostabilized plant restrict the root uptake and translocation of toxic metals, resulting in a phytostailization effect [24]. Therefore, the organic material application has different effects on phytoremediation efficiency in different situations and how to apply organic materials for the remediation of PHMs-contaminated soils needs further study. Meanwhile, there is little research related to agricultural wastes application for the remediation efficiency of PHMs-contaminated soil by hyperaccumulators.

In China, a large number of organic wastes are produced in the process of agricultural production, including biogas residue (BR), mushroom residue (MS), bamboo shell (BS) and so on. The application of organic wastes as manure not only reduces their pollution to the environment, but also reduces the use of chemical fertilizer [17]. Biogas residue is a high-quality organic fertilizer which contains a large amount of organic matter and nutrients (e.g., N, P and K) for plant growth [23]. Mushroom residue is rich in cellulose, vitamins, mineral elements and other bioactive substances. It can be used as organic fertilizer or soil amendment in agricultural production [25]. As the processing waste of bamboo shoots, the bamboo-shoot shell also contains a large amount of amino acids, proteins, coarse fibers and other nutrients. High-quality compost can be obtained from bamboo shells [26,27].

Sedum alfredii (S. alfredii) Hance is a kind of Zn/Cd hyperaccumulators, which is found in a mine area in Southeast China [28]. It is one of the ideal remediation plants which can be applied to remove Cd and other PHMs from the contaminated soils [29]. In this study, a pot experiment was conducted to investigate the effects of three organic materials (biogas residue (BR), mushroom residue (MS) and bamboo shell (BS)) on phytoremediation by S. alfredii Hance. The objectives of our study were: (1) to investigate the effect of different organic materials on phytoremediation efficiency by S. alfredii Hance; (2) to select suitable ways of organic materials application on different polluted soils; and (3) to provide important information for practical field remediation of PHMs-contaminated soils.

The Cd-contaminated farmland soils were collected in two places (Wenzhou and Fuyang cities). Based on GB 15618-2018 in China [30] and single factor pollution index [31,32], Wenzhou soil was classified as “moderately-polluted soil”, which was collected from an experimental base in Wenzhou academy of agricultural science, Wenzhou City, Zhejiang Province; while Fuyang soil was named as ‘heavily-polluted soil’, which was taken from the surrounding area of a smelting plant in Huanshan Town, Fuyang City, Zhejiang Province. The basic physico-chemical properties are shown in Table 1. Soil samples were air-dried and sieved to pass a 5 mm nylon mesh.

The PHM hyperaccumulator S. alfredii Hance was taken from an ancient Pb/Zn mine in Quzhou City, Zhejiang Province, which could reproduce asexually. After artificial propagation through cuttage, all the homogeneous plants with a length of about 5 cm, uniform size, leaves and no terminal bud were selected as tested materials.

The biogas residue (BR) was collected from a pig manure digester in an organic farm of Yuhang County, Hangzhou City, Zhejiang Province. The mushroom residue was collected in a farm of Jiaxing City, Zhejiang Province, where the black fungus cultivation was carried out. The main raw material of fungus-stick was mulberry sawdust (about 80%). The auxiliary materials were wheat bran, cotton seed hull and lime. The bamboo-shoot shell was collected from an agricultural product processing factory in Lin’an County, Hangzhou City, Zhejiang Province. After mushroom residue (MR) and bamboo-shoot shell (BS) were fermented, three organic materials were air-dried and were ground for sieving through 2 mm nylon mesh. The basic properties are shown in Table 1.

Each organic material (BR, MR, BS) was mixed with the soil according to the organic material-soil ratio of 1% and 5%, respectively. Therefore, a total of 7 treatments were set up including a control (no organic material application) (Table 2). Each treatment had three replications. The size of the plastic pot was 305 mm × 210 mm × 110 mm (length × width × height) and 5 kg soil was filled in each pot. The S. alfredii Hance seedlings were transplanted into pots (row space: 5 cm, 35 plants per pot). When S. alfredii Hance was at the plant sealing line stage (average 45 days after planting), all the plants were harvested and soil samples were collected.

Plant samples were washed with deionized water and were measured their fresh weight. Then S. alfredii Hance samples were dried to a constant weight at 70°C and measured again. The dry samples were ground in an agate grinder for further analyses. The plant samples were digested with HNO3-H2O2, then the PHMs were determined by ICP-OES (Optima 7000 DV, PerkinElmer).

Soil samples were air-dried and sieved to pass a 5 mm nylon mesh. Soil pH was directly determined using a pH meter at a soil to water ratio of 1:2.5. (w/v) [33]. Soil organic matter was determined by concentrated sulphuric acid (H2SO4) and potassium dichromate (K2Cr2O7), and titration with ammonium sulfate iron (Fe(NH4)2(SO4)2·6H2O) solution [34]. Cation exchange capacity was determined by Ammonium acetate method [34]. Available nitrogen was determined by Alkali hydrolysis diffusion method; available phosphorus was determined by sodium bicarbonate-molybdenum-antimony resistance colorimetric method; available potassium was determined by Ammonium acetate extraction-flame photometer method [34].

The available PHMs of soil samples were extracted by HCl (0.1 mol L−1) and determined by ICP-OES (Optima 7000 DV, PerkinElmer) [34]. Total soil PHM contents were extracted using HNO3-HF-HClO4. Soil sample (0.1g) after passing through 0.149 mm nylon sieve, was taken in a 30 mL PTFE crucible, moistened the soil with deionized water, then added HF solution (7 ml) and concentrated HNO3 solution (1 ml), boiled and evaporated it on the hot plate and removed the crucible from the electric heating plate when it is nearly dry. After cooling, add HClO4 (2 ml), continue to boil until no white smoke and the residue in the crucible appears with light color. Then 1:1 HNO3 (1 ml), is added and heated until the solution is completely clear. The above solution is transferred to volumetric flask (25 ml) and determined by ICP-OES (Optima 7000 DV, PerkinElmer) [35]. Soil standard sample (GSS-4) was used for quality control.

The one-way analysis of variance (ANOVA) was used to determine the significant differences among different treatments at the significant level of 0.05. The ANOVA was carried out using SPSS 20.0. All the plots were produced by origin software.

Compared with CK, pH values of most treatments decreased, except 5% MR treatment (Fig. 1). For example, the pH values of 5% BR and 1% BS treatments decreased by 0.3 unit in moderately-polluted soil (P < 0.05). The reason for such phenomenon was related to different compositions of organic materials, which were further decomposed into different soluble ions or small organic acids, leading to the pH variation in the soils [36]. In addition, pH values were also be affected by metabolic activities of S. Alfredii Hance roots such as root exudates, soil microorganisms and so on. The components of root exudates of the studied plant included some organic acid compounds (oxhydryl, carboxyl andamidogen), which could greatly decrease soil pH [37].

Figure 1: Effects of different treatments on pH in two soils (Different lowercases indicated significant differences between treatments (P < 0.05)). (a) Moderately-polluted soil. (b) Heavily-polluted soil

Adding 5% organic material had a marked increase in soil organic matter (SOM). However, adding 1% organic materials had no significant effect on SOM (P > 0.05), compared with the control (Fig. 2). This indicated that a higher concentration of organic materials had a better effect on the increase of soil organic matter. In moderately-polluted soil, the SOM contents of 5% BR, 5% MR and 5% BS treatments were 9.5%, 10.3% and 12.8% higher than control, respectively. In heavily-polluted soil, the SOM contents of 5% BR, 5% MR and 5% BS were 23.3%, 40.0% and 26.3% higher than the control, respectively (P < 0.05). The effects of organic material addition on SOM content were much obvious in heavily-polluted soil than that in moderately-polluted soil. The reasons might be as follows: (1) The organic matter content in Heavily-polluted soil was lower than Moderately-polluted soil. When the same dosage of organic material was applied, the increase of SOM in Heavily-polluted soil was obvious; (2) It was also possibly related to the heavy PHM pollution in Heavily-polluted soil, which inhibited the mineralization and decomposition of organic matter by soil microorganisms.

Figure 2: Soil organic matter content affected by different treatments (Different lower cases indicated significant differences between treatments (P < 0.05)). (a) Moderately-polluted soil. (b) Heavily-polluted soil

3.2 Effects of Organic Materials on the Concentration of Soil Available PHMs and Their Availability

For Moderately-polluted soil, compared to the control, most treatments (except the Cu and Zn in 5% BR treatment) decreased the available Cu, Zn, Pb and Cd concentration in the soil (Table 2), so did the availability of PHMs (Table 3).

The available concentration of PHMs varied depending on the types and dosages of organic materials in heavily-polluted soil (Table 2). In heavily-polluted soil, the concentrations of PHMs, significantly increased under 1% BS while significantly decreased under 5% BR, compared to the control (P < 0.05). For the available concentration of soil Cu, 5% organic material treatments had a lower concentration than the control, while 1% organic material treatments increased the content of soil available Cu. For available concentration of Zn, 1% BR and 1% BS significantly increased while 5% BR significantly decreased, compared to the control (P < 0.05). Low dosage (1%) treatments significantly (P < 0.05) increased the available Pb and high dosage (5%) decreased soil available Pb. For available Cd, 1% BS significantly increased while 5% BR significantly decreased, compared to the control (P < 0.05). Similar phenomena were found for the availability of PHMs in the heavily-polluted soil (Table 3).

The results from our pot experiment showed that organic material types and their application rates had different effects on the concentrations of available four PHMs in soils and their availability. Obviously, this was related to the complex reaction process in the soil system. The effects of organic materials on the bioavailability of PHMs depend on the properties of organic materials, the internal redox, the soil types and the characteristics of PHM ions [38]. Organic materials would be transformed and decomposed into low-molecular-weight organic acid and high-molecular-weight humic acid, after entering into soils. Lu et al. [39] and Garcia-Mina et al. reported that humic acid had different effects on PHMs under different conditions, which included activation or passivation of PHMs [40]. In this experiment, the properties of three organic materials were different. The BR was from the excretion of animals which was anaerobically fermented in biogas digester. The BS was aerobically fermented by the edible bamboo shoots leftover. And the MR was mainly produced in the fermentation of leftover from the cultivation of black fungus. Biogas residue contains a large amount of organic matter and nutrients (e.g., N, P and K) for plant growth [41]. Mushroom residue is rich in cellulose, vitamins, mineral elements and other bioactive substances. [42]. The bamboo-shoot shell contains a large amount of amino acids, proteins, coarse fibers and other nutrients [27]. Therefore, in terms of organic material compositions, BS had more simple-structure and easier-decomposition organic compositions (such as cellulose ((C6H10O5)n) and hemicellulose (arabinan, galactan and glucomannan)), compared with BR and MR [27,43]. Thus, BS can promote the available PHM contents in soils. Research indicated that the decreased pH values could improve the efficiency of Zn, Cd accumulation by plants [44]. Due to the high pH value of MR, which could lead to the pH increase in soils, the availability of soil PHMs significantly decreased [45]. The high pH affected the PHM uptake of plants. Therefore, the PHM accumulation in shoots of S. alfredii Hance under MR treatments was lower than the others and control. The decrease of soil pH could lead to the dissolution and release of carbonate-bound and hydroxide-bound PHMs. Therefore the acidic condition can increase the PHMs’ dissolution and release [46,47].

For Cu and Zn in moderately-polluted soil, 5% BR increased their contents, while 1% BR had no significant effect on their contents. However, the inverse phenomena were found in heavily-polluted soil. Both the nutrient contents and cation exchange capacity in moderately-polluted soil were higher than heavily-polluted soil, while the contents of PHMs were lower than heavily-polluted soil (Table 1). In such case, the activity or metabolic rate of microorganisms in moderately-polluted soil was much higher than that in heavily-polluted soil. The microorganism of rhizosphere is the benefit to plants’ uptake of PHMs [48], which might be a reason for the different results in the two soils.

For Cd, almost all treatments in this study restrained the available Cd to some extent. However, only the BS treatments had an activation effect on Cd in Heavily-polluted soil. Previous studies revealed that the root exudates and rhizosphere microorganisms (such as arbuscular mycorrhiza and endophytic mycorrhiza) of S. alfredii Hance had activation or inhibition effects on PHMs [49]. Therefore, PHMs would be activated or inhibited in different soil systems. This was influenced by a series of factors, such as the type and dosage of organic materials, root exudates, edaphon and soil organic matter [50]. The interaction between above factors determined the contents of available PHMs. In addition, with S. alfredii Hance absorbing PHMs from soil, the soil available PHMs reduced. Therefore, the mechanism of organic materials on the soil available PHMs during the growth of S. alfredii Hance was complicated.

Overall, the addition of organic materials enhanced the shoot dry weight of S. alfredii Hance. In Moderately-polluted soil, compared to the control, 5% MR, 1% BS and 5% BS treatment significantly (P < 0.05) enhanced the biomass production of S. alfredii Hance’s shoots (Fig. 3). In heavily-polluted soil, all treatments had an increase in biomass of the shoots. The 5% MR treatment had the highest biomass production for both soils. The addition of organic materials could promote the growth of S. alfredii Hance and increase the shoots biomass.

Figure 3: Biomass of S. alfredii Hance shoot dry weights affected by different treatments (Different lower cases in the above three tables indicated significant differences between treatments (P < 0.05)). (a) Moderately-polluted soil. (b) Heavily-polluted soil

3.3.2 Effects of Organic Materials on PHM Content in Shoots and Remediation Efficiency of S. alfredii Hance

Compared with control, the PHM contents in shoots of S. alfredii Hance showed a decreasing trend after organic materials application in two soils (Table 4). However, in moderately-polluted soil, the content of Zn in shoots had an inverse trend. Compared to the control, the treatments of 1% BR, 5% BR and 1% BS significantly (P < 0.05) increased the content of Zn in shoots of the plant. Generally speaking, the Zn concentration in plant shoots was high in this study. This was in line with other studies. Ni et al. [51] found that the accumulation of zinc reached more than 10 g kg−1, using S. alfredii Hance. In another study [52], the accumulation of zinc in above-ground part of S. alfredii Hance was more than 15 g kg−1.

Organic material reduced the content of Cd in plant shoots. The 5% MR treatment decreased by 57.6%, compared to the control. In heavily-polluted soil, Cu, Zn, Pb and Cd contents in shoots of S. alfredii Hance decreased after adding three organic materials. The effects of organic materials on PHM contents in shoots of S. alfredii Hance decreased more significantly with the increased application rates of organic materials.

To evaluate the efficiency of S. alfredii Hance in remediation of PHM-contaminated soil, not only the improvement of soil structure, fertility, and transport rate [2], but also the total amount of PHMs removed from the soil per unit time should be considered. The total amount of PHMs uptaken by S. alfredii Hance was related to two factors. One was the biomass of shoots, the other was the PHM contents in S. alfredii Hance. The PHM accumulation was the product of biomass and content, which could directly reflect the effect of organic materials on the PHM remediation efficiency of S. alfredii Hance. In this experiment, all three types of organic materials addition enhanced the biomass production in moderately-polluted and heavily-polluted soils, especially for the MR treatments (Fig. 3). The MR application was helpful for the better nutritional condition of S. alfredii Hance, which was mainly attributed to the fact that the sticks had much more glucose, amino acids and beneficial microorganisms for the growth of target plants [53]. Unlike biomass production, three organic materials had different effects on the uptake and accumulation of PHMs in shoots of S. alfredii Hance. This finding was in line with the results of other studies [54,55], revealing that the effect of organic materials on PHMs removal was also related to soil properties and PHMs. The MR treatments inhibited the accumulation of PHMs in moderately-polluted soil, and the Cu, Pb, Cd accumulation in heavily-polluted soil (Table 5). BR and BS treatments mainly promoted Cu and Zn accumulation but inhibited Pb accumulation in both two soils. For Cd, only 1% BS treatment significantly promoted its accumulation in shoots in Moderately-polluted soil; both 1% BR and 5% BS treatments significantly promoted Cd accumulation in Heavily-polluted soil. The inhibition effect on the PHMs might be due to the increase of soil pH, the complexation and fixation of PHM by macromolecules complex organic matters such as humic substances during the decaying organic materials process, which resulted in the decrease of PHM activity in soil and the restraint of their uptake by plant roots [20]. On the other hand, the promotion effect on the PHMs of the shoots was related to the similar effect of organic materials on the growth of S. alfredii Hance, and the activation of soil PHMs by micro-molecular organics, which were generated from organic materials’ mineralization and decomposition process [21,34,56]. Therefore, although the same organic material treatment enhanced the biomass product in shoots of S. alfredii Hance, it could also reduce the accumulation of PHMs in shoots.

The properties of organic materials, as well as their application rates can influence the soil PHMs’ availability. Therefore, more attention should be paid to the availability of soil PHMs and the growth of S. alfredii Hance. In such a case, the phytoremediation efficiency of S. alfredii Hance under the application of the organic material could be effectively evaluated. Among the tested three organic materials, BS and BR applications were better choices for phytoremediation to soil PHMs pollution. If an appropriate rate of BS and BR was added to soil, the remediation efficiency for Zn/Cd contaminated soils by S. alfredii Hance could be promoted. While the MR addition inhibited the absorption of Cu, Zn, Pb and Cd by S. alfredii Hance, reducing the PHM uptake in shoots of the plant.

The BR, MR and BS application could decrease the pH in two soils (moderately-polluted soil and heavily-polluted soil) except the 5% MR treatment. The contents of soil organic matter with 5% organic materials application were significantly higher than that with 1% organic materials. For the available PHM concentrations in soil, 5% BR treatment had the best activation effect on Cu and Zn in moderately-polluted soil, while 1% BS has the best effect on Cu, Zn, Pb and Cd in heavily-polluted soil.

Based on the biomass production and PHM contents in shoots of S. alfredii Hance, 1% BS treatment had the best effect on Cd uptake and accumulation in shoots of S. alfredii Hance in moderately-polluted soil. In heavily-polluted soil, the remediation effect on Zn was as follows: 5% BS > 5% BR > 5% MR while for Cd, 1% BR and 5% BS treatments were better than the control.

The proper addition of BR and BS could promote the phytoremediation efficiency of soil PHMs by S. alfredii Hance. The MR had no significant effect due to its higher pH. The degree of soil pollution and the types of organic materials could both influence the phytoremediation efficiency. These indicated that the application of organic materials to improve phytoremediation efficiency should both consider physico-chemical properties of organic materials and soils.

Acknowledgement: We thank Chunying Dou for his help in the laboratory analysis and Ying He for her help in the figure production.

Funding Statement: This work was financially supported by the National College Students’ Innovation and Entrepreneurship Training Program (202110341014).

Conflicts of Interest: The authors declare that they have no conflicts of interest to report regarding the present study.

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