Next Article in Journal
Antiseizure and Neuroprotective Efficacy of Midazolam in Comparison with Tezampanel (LY293558) against Soman-Induced Status Epilepticus
Previous Article in Journal
Editorial for the Special Issue “Microplastics in Aquatic Environments: Occurrence, Distribution and Effects”
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Toxics
Volume 10
Issue 8
10.3390/toxics10080408
toxics-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effects of Amendments and Indigenous Microorganisms on the Growth and Cd and Pb Uptake of Coriander (Coriandrum sativum L.) in Heavy Metal-Contaminated Soils

by
Nana Mi
1,2,
Wenying Hao
1,2,
Zixin Zhou
1,2,
Longcheng Li
1,2,
Fayuan Wang
3,* and
Jingping Gai
1,2,*
1
Beijing Key Laboratory of Farmland Soil Pollution Prevention and Remediation, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
2
Key Laboratory of Plant-Soil Interactions, Chinese Ministry of Education, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
3
College of Environment and Safety Engineering, Qingdao University of Science and Technology, Qingdao 266042, China
*
Authors to whom correspondence should be addressed.
Toxics 2022, 10(8), 408; https://doi.org/10.3390/toxics10080408
Submission received: 28 June 2022 / Revised: 13 July 2022 / Accepted: 20 July 2022 / Published: 22 July 2022
(This article belongs to the Section Toxicity Reduction and Environmental Remediation)
Browse Figures
Versions Notes

Abstract

:
Heavy metal (HM) contamination of soils is a worldwide problem with adverse consequences to the environment and human health. For the safe production of vegetables in contaminated soil, efficient soil amendments need to be applied such as nano-hydroxyapatite (n-HAP) and poly γ-glutamic acid (γ-PGA), which can mitigate heavy metal uptake and enhance crop yield. However, the combined effects of soil amendments and indigenous microorganisms (IMOs) on HMs immobilisation and accumulation by crops have received little attention. We established a pot experiment to investigate the effects of IMOs combined with n-HAP and γ-PGA on coriander (Coriandrum sativum L.) growth and its Cd and Pb uptake in two acidic soils contaminated with HMs. The study demonstrated that applying n-HAP, with and without IMOs, significantly increased shoot dry biomass and reduced plant Cd and Pb uptake and diethylenetriaminepentaacetic acid (DTPA) extractable Cd and Pb concentrations in most cases. However, γ-PGA, with and without IMOs, only reduced soil DTPA-extractable Pb concentrations in slightly contaminated soil with 0.29 mg/kg Cd and 50.9 mg/kg Pb. Regardless of amendments, IMOs independently increased shoot dry biomass and soil DTPA-extractable Cd concentrations in moderately contaminated soil with 1.08 mg/kg Cd and 100.0 mg/kg Pb. A synergistic effect was observed with a combined IMOs and n-HAP treatment, where DTPA-extractable Cd and Pb concentrations decreased in slightly contaminated soil compared with the independent IMOs and n-HAP treatments. The combined treatment of γ-PGA and IMOs substantially increased shoot dry biomass in moderately contaminated soil. These results indicate that solo n-HAP enhanced plant growth and soil Cd and Pb immobilisation, and mitigated Cd and Pb accumulation in shoots. However, the combination of n-HAP and IMOs was optimal for stabilising and reducing HMs’ uptake and promoting plant growth in contaminated soil, suggesting its potential for safe crop production.

1. Introduction

Heavy metal (HM) pollution has long been a concern because of its limited biodegradability and toxicity to plants, animals, and humans [1,2,3]. The HMs, Pb and Cd, are ubiquitous pollutants in agricultural ecosystems owing to industrial practices, irrigation with sewage wastewater, application of livestock manure as fertiliser, and the use of agricultural chemicals [4,5]. Consequently, the remediation of HM-contaminated soils through soil replacement, chemical fixation, bioremediation, and plant stabilisation [6,7] is imperative for protecting the health and safety of the public and the environment [8].
Various in situ remediation techniques using various materials have been developed in recent decades [6,9]. Lime, phosphate, P-containing materials, clay minerals, metal oxides, and biochar have been widely used to decrease bioavailable HM in recent years [10,11]. Among them, apatite-based materials have been established to be effective in immobilising Pb, Cd, Cu, Zn, and other metals in soil [12]. Nanoscale phosphatic materials are particularly superior to their traditional bulk counterparts owing to their high adsorption capacity for HMs [13]. For example, nano-hydroxyapatite (n-HAP) is an ideal material for the disposal of contaminants because of its small particle size and increased surface area, which provide strong interactions with HMs [14,15,16]. For example, the concentration of Cd in potato tubers was reduced by 17.4% after applying n-HAP [17].
Poly γ-glutamic acid (γ-PGA) is a biological macromolecule formed from D-glutamic acid and L-glutamic acid monomers, which are joined via a gamma–glutamine bond [18,19,20]. The extracellular biopolymer, γ-PGA, is naturally occurring, being produced by microbes such as Bacillus subtilis and Bacillus lichenformis through fermentation [19]. Being a potential environment-friendly polymer with biodegradable, non-immunogenic, and non-toxic characteristics, γ-PGA can be used as a substrate to enhance the growth of microorganisms [19,21,22]. In recent years, γ-PGA has been widely applied in food processing [23], water treatment [24], agricultural industries [25], soil improvement, and the alleviation of abiotic stress in plants [26,27,28]. The numerous functional groups (–COOH) that γ-PGA contains can bind metal ions through a complex reaction. Previous studies have revealed that γ-PGA is effective for the adsorption of metal ions such as Ni2+, Cu2+, Zn2+, Cr3+, Hg2+, and U4+ during water treatment [29]. Several studies have reported the role of γ-PGA in alleviating HMs’ toxicity in plants. The effects of γ-PGA on cucumber seedlings were tested under Cd and Pb stress, demonstrating that γ-PGA effectively reduced the growth inhibitory effects of Cd and Pb on the plants, and the metal concentrations of the Cd + 1.2 g/L γ-PGA and Pb + 6 g/L γ-PGA groups were 38.65% and 74.13%, respectively, lower than those of the Cd and Pb only groups (i.e., the untreated groups) [30].
Compared with chemical sorbents, microorganisms are more environment-friendly because they attenuate the toxic influence of HMs on organisms without creating secondary pollution or destroying soil properties [31,32]. Microbial bioremediation can be achieved by utilising indigenous microorganisms (IMOs) in the soil environment to break down HMs into their benign components [33]. Compared with extraneous microbial communities, IMOs have greater adaptability and competitiveness within their specific soil environment [34]. Many studies have tested the natural remediation potential of IMOs on HM-polluted soils, and pronounced effects have been observed. For example, a study revealed that the total HM concentrations at several tailing sites decreased over 31 years of natural attenuation by IMOs, and the Cd and Zn concentrations decreased by 2.18 and 3.62 times, respectively [35].
Many studies have revealed that inoculation with microorganisms and amendments have synergistic effects in increasing soil fertility and plant performance in HM-contaminated soils [36,37]. The combination of biochar and arbuscular mycorrhizal fungi (AMF) inoculation could modify soil physicochemical properties, enhance AMF growth [38], and affect nutrient cycling [39]. Additionally, several studies have been conducted on the combined effects of n-HAP and microorganisms on the remediation of HM-polluted soils [10,40]. When combined with microorganisms, n-HAP improved the growth of plants and significantly decreased the uptake of HM. For example, Liu et al. revealed that, in Cd-contaminated soil, the combination of 0.5% (W/W) n-HAP with different concentrations of white rot fungi increased plant biomass by 17.95–23.93%, decreased plant Cd concentration by 38.16–40.94%, and significantly increased the activity of alkaline phosphatase and urease [41]. However, previous research has predominantly focused on a specific strain. ‘Soil ecological engineering’ has recently been proposed as an approach that combines management practices to enhance the overall biological diversity in human land-use systems with targeted manipulation of soil biota to improve agricultural sustainability [42]. Therefore, further confirmation is required to clarify whether IMOs combined with n-HAP and γ-PGA have a synergistic effect on HMs’ pollution remediation of agricultural land.
Some studies proved that people in Hunan and the other three provinces in southern China faced a high health risk of Pb and Cd when consuming vegetables [43]. Coriandrum sativum L. is an important vegetable crop that is widely used to flavour and garnish culinary dishes and is fundamental for supporting livelihoods [44]. In this study, we aimed to evaluate the independent and combined effects of IMOs with n-HAP and γ-PGA on plant growth, Pb and Cd uptake, and Pb and Cd immobilisation in soil. We hypothesised that the combined treatments would have an additive effect on soil alkalinisation and HMs’ stabilisation and modulate HMs’ uptake and coriander growth.

2. Materials and Methods

2.1. Soil and Amendments

Two Pb- and Cd-contaminated soil samples were collected from the topsoil layer (0–20 cm depth) of typical agricultural land in Zhuzhou City (27°50′2.9″ N, 113°25′9.5″ E), Hunan Province, China. The soil under investigation has been contaminated with HMs by wastewater discharge from a nearby metallurgy plant since the early 1980s. The soil type is red earths. The clay content of the soil is 21.7%.  Fifty kilograms of soil was collected from two sites with different concentrations of heavy metal. According to China’s soil environmental quality for agricultural land standard (GB15618-2018), the total Cd and Pb concentration in the two soils was below the soil screening value and below the intervention value, respectively (Table 1), thus the soils were regarded as having slightly and moderately contaminated levels. For both soils, a subsample of fresh soil was passed through a 2 mm sieve and stored at 4 °C for preparing the IMOs’ inoculum. The remaining soil was air-dried at around 25 degrees Celsius, ground, and passed through a 2 mm sieve and stored at room temperature. A portion of the soil was used as the substrate in the pot experiment, and the remainder was used for analysing the selected soil parameters. The physicochemical attributions of the two soils are presented in Table 1.
n-HAP and γ-PGA were purchased from the Nanjing Emperor Nano Material Co., Ltd. (Nanjing, China) and Yantai Jinbang Biotechnology Co., Ltd. (Yantai, China), respectively. n-HAP is an ultra-fine powder with a pH of 10.8, Ca/P molar ratio of 1.70, total HM content ≤ 1 mg/kg, and average particle size ≤ 60 µm. The molecular weight of γ-PGA used in this study is 1.0 × 106 Da, and the density of aqueous solution is 1.11 g/mL. The mass concentration for the γ-PGA agents, which is produced from B. subtilis, is 4%. The Huoshan coriander (Coriandrum sativum L.) cultivar was selected for this experiment.

2.2. Pot Experiment

This experiment included three amendments, i.e., non-amendment control, n-HAP, and γ-PGA, and two microorganisms (non-inoculation control and IMOs). Two pollution levels were designed to represent slightly and moderately contaminated levels, respectively. A control treatment receiving no amendments was also included. Five replicates were performed for each treatment. The pots used in the experiment had a height of 18 cm and diameter of 16 cm and contained 1 kg of soil with or without amendments. The substrate soil was sterilized by γ-irradiation with 25 kGy 60Co. Two hundred grams of unsterilized IMOs and eight hundred grams of sterilized substrate soil were placed into the pot. n-HAP was added to the pots at a ratio of 1.5% each and homogeneously mixed according to the method of Zhu et al. (2019) [45], and the soil in each pot was then incubated for one week to equilibrate. γ-PGA was added to the pots at a ratio of 0.2% and homogeneously mixed, according to the method of Pang et al. (2018) [30], and the soils in each pot were then incubated for two weeks to equilibrate. Each pot was then sown with 20 pre-germinated seeds and thinned to six plants 15 days after emergence. The plants were grown in a glasshouse of China Agricultural University from April to July 2021, with a temperature of 20–25 °C, a relative humidity of 60–70%, and a light/darkness photoperiod of 14/10 h (light intensity, 240–350 μmol m−2 ·s−1). The pots were gravimetrically maintained at a water-holding capacity of approximately 60%, and the soil water holding capacity was determined by the ring knife method. No additional nutrients were applied in the experiments.

2.3. Harvest and Sample Analysis

2.3.1. Plant Analysis

The plants were harvested 60 days after transplantation. After transporting to the laboratory, each plant sample was washed with deionised water, oven-dried at 100 °C to an even weight, and separated into roots and shoots to determine the dry weight of each component for the biomass growth measurements; then, a 50–100 g dry sample was collected for chemical analysis. The dried samples were pulverised using a stainless-steel grinder and then stored at room temperature. Dry plant material (0.25 g) was digested in 8 mL of HNO3 in a microwave oven (Start 1500, MLS GmbH, Leutkirch im Allgäu, Germany) using a temperature step gradient (maximum of 210 °C). When necessary, digested solutions were diluted with 2% HNO3. The Cd and Pb concentrations in the extract solution were measured via inductively coupled plasma mass spectrometry (ICP-MS 7700, Agilent Technologies, Santa Clara, CA, USA). Blanks and a certified reference material, GBW10045 (GSB-23, rice flour), were also prepared by the digestion process for quality assurance. The recovery of the reference material was between 87% and 110%.

2.3.2. Soil Analysis

The soil from each pot was air-dried, ground by automatic agate mill, sieved into 2 mm, and mixed thoroughly; then, an around 200–300 g sample was collected for the analysis of metal availability and soil pH. The soil pH was measured in an aqueous soil suspension (1:2.5, w/v). The concentrations of available Cd and Pb were acquired by mechanically shaking each 3.0 g air-dried sample with 20 mL of 0.005 mol/L DTPA extract (0.005 mol/L DTPA + 0.01 mol/L CaCl2 + 0.1 mol/L triethanolamine, buffered to a pH of 7.30 using a hydrochloric acid solution or ammonia) [46]. After oscillation, the solution was centrifuged and immediately filtrated using a 0.45 μm filter membrane. Physical analysis of the filtrate was performed within 48 h via ICP-MS. Total Cd and Pb in substrate soil were digested with a solution of 3:1 HNO3/HClO4 (v/v), and the filtrate was also performed via ICP-MS.

2.4. Statistical Analysis

All data were tested for normality (Kolmogorov–Smirnov test) and homogeneity (Levene’s test) before statistical analysis. Data analyses were performed using the IBM SPSS statistical software package version 20 (IBM Corporation, New York, NY, USA) to obtain the significance and variance. The impact of three factors on plant growth, Cd and Pb concentration (in shoot and root), soil available HM concentration, and pH values was analysed by univariate analysis of variance (ANOVA) with the generalized linear model (GLM). Data were analysed using one-way ANOVA and Duncan’s multiple range test (p < 0.05) to compare the mean values for plant and soil data. All results are expressed as mean values and standard error (SE). All measurements were conducted in five replicates. Pearson correlation analysis was conducted to test the correlation among dry biomass; pH, Cd, and Pb concentration; and available Cd and Pb concentration at two contaminated levels.

3. Results

3.1. Plant Growth Responses

Shoot dry biomass was significantly (p < 0.05) affected by amendments, IMOs, contaminated levels, amendments × IMOs, amendments × contaminated levels, IMOs × contaminated levels, and amendments × IMOs × contaminated levels in contaminated soil, and root biomass was significantly (p < 0.05) affected by IMOs, contaminated levels, and their interaction (Table 2). The effects of IMOs and amendments on shoot biomass are presented in Figure 1a,b. Compared with the control treatment, regardless of amendments, independent treatment of moderately contaminated soil with IMOs increased shoot and root dry biomass by 2.58 and 2.92 times, respectively. Compared with that of the control treatment, the shoot dry biomass of coriander treated with n-HAP only increased by 1.48 and 3.66 times in slightly and moderately contaminated soils, respectively. Compared with the control group, when combined with the IMOs, the increase was 1.29 and 3.56 times in slightly and moderately contaminated groups, respectively. In moderately contaminated soil, the combined effect of γ-PGA and IMOs inoculation significantly (p < 0.05) increased shoot (3.44-fold) and root (5.42-fold) dry biomass compared with the control treatment. However, shoot dry biomass showed a slight decrease in γ-PGA in the IMOs group in the slightly contaminated soil. The addition of n-HAP and γ-PGA had almost no influence on root dry biomass in either soil type (Table 3).

3.2. Cd and Pb Uptake by Coriander Tissues

The shoot Cd and Pb concentrations and root Cd concentration were significantly (p < 0.05) affected by amendments and contaminated levels, whereas shoot Cd concentration was also significantly (p < 0.05) affected by IMOs and the interaction of IMOs and amendments. Root Pb concentration was significantly (p < 0.05) affected by amendments and the interaction of amendments and contaminated levels (Table 2).
The effects of inoculation and amendments on shoot Cd concentrations are shown in Figure 2a,b, respectively, and the shoot Pb concentrations are shown in Figure 2c,d. The application of n-HAP with and without IMOs significantly (p < 0.05) reduced shoot Cd and Pb concentrations in both soils (Figure 2). With the addition of n-HAP, shoot Cd concentrations reduced by 1.89 and 1.44 times in the non-inoculation control and IMOs groups, respectively, as compared with those in the controls in moderately contaminated soil. Compared with that of the control treatment, the Cd concentrations of the shoots from slightly contaminated soil decreased by 4.38 and 3.25 times in the non-inoculation control and IMOs groups, respectively. With the addition of n-HAP, the shoot Pb concentrations reduced by 1.68 and 1.28 times and root Pb concentrations reduced by 3.22 and 2.50 times in the non-inoculation control and inoculation treatments, respectively, as compared with those in the control treatment in slightly contaminated soil. In moderately contaminated soil, shoot and root Pb concentrations of the n-HAP and IMOs combined group reduced by 2.57 and 2.30 times, respectively, as compared with those of plants grown in the control group. However, rather than decreasing the Cd and Pb concentrations, γ-PGA approximately doubled the root Cd and Pb concentrations in slightly contaminated soil.

3.3. Soil Analysis

3.3.1. Soil pH

Soil pH was significantly (p < 0.05) affected by amendment (Table 2). Compared with the control treatment in slightly contaminated soil, the addition of n-HAP significantly increased soil pH by 0.96 and 0.83 in the non-inoculation control and inoculation treatments, respectively, but had no effect in moderately contaminated soil (Figure 3b). The addition of γ-PGA and inoculation with IMOs had almost no influence on the pH values in all treatment groups.

3.3.2. Available Cd and Pb Concentrations

The available Cd and Pb concentration was significantly (p < 0.05) affected by amendments and contaminated levels. The available Cd concentration was also significantly (p < 0.05) affected by IMOs, IMOs × contaminated levels, and amendments × contaminated levels interactions (Table 2).
The effects of inoculation and amendments on the concentrations of available Cd are shown in Figure 4a. The available Pb concentrations are shown in Figure 4c. Regardless of amendments, IMOs independently increased the available Cd concentrations in moderately contaminated soil by 1.42 times compared with the control group. The application of n-HAP, with and without IMOs, significantly (p < 0.05) reduced the available Cd and Pb concentrations in both soils (Figure 4). Compared with the control group, when n-HAP was independently applied, available Cd concentrations reduced by 2.04 and 1.99 times and Pb concentrations reduced by 2.89 and 2.10 times in slightly and moderately contaminated soils, respectively. Compared with the control group, in the n-HAP and IMOs group combined, the available Cd concentrations decreased by 2.41 and 1.16 times and the available Pb concentrations decreased by 3.79 and 1.86 times in slightly and moderately contaminated soils, respectively. An additive effect was observed with n-HAP and IMOs reducing the available Cd and Pb concentrations in slightly contaminated soil to 0.08 mg/kg and 4.4 mg/kg, respectively. Compared with the control group, γ-PGA, with and without IMOs, exhibited inhibitory effects on available Pb concentrations in slightly contaminated soil, with a decrease of 1.13 and 1.21 times, respectively.

3.4. Correlation Analysis of Dry Biomass, Soil pH, Cd and Pb Concentrations, and Available Cd and Pb Concentrations

The correlation analysis results of shoot and root dry biomass, pH, Cd and Pb concentrations, and available Cd and Pb concentrations are shown in Figure 5. In the slightly contaminated soil, shoot dry biomass was negatively correlated with available Cd and shoot Pb concentrations, and Cd concentration was positively correlated with available Pb and Cd concentrations (p ≤ 0.05). Shoot Cd concentration was negatively correlated with soil pH. In moderately contaminated soil, shoot Cd concentration exhibited a positive correlation with available Pb and Cd concentrations, whereas shoot and root Pb concentrations were negatively correlated with soil pH.

4. Discussion

This study revealed a remarkable growth response and low Pb and Cd concentrations, which were beneficial to coriander, as a result of the (1) amendment with n-HAP, (2) amendment with γ-PGA, (3) inoculation with IMOs, (4) synergistic effect of IMOs and n-HAP in slightly contaminated soil, and (5) combined effect of γ-PGA and IMOs in moderately contaminated soil.

4.1. Effect of Pb and Cd Toxicity on Plant Growth

Shoot dry biomass was much higher in moderately contaminated soil than slightly contaminated soil, particularly in unsterilized treatments (Figure 1), which might imply the importance of IMOs in improving plant resistance to HM stress [47,48]. Previous research has also revealed that the stimulation of indigenous soil microbial activity is essential to enhance natural detoxification of contaminated environments [49].
In this study, growth inhibition of roots was observed in both soil treatment groups (Table 3). Growth inhibition in plants is a common physiological effect of HM stress. The toxicity varies between breeds and has an increased effect in sensitive plants [50]. Many key physiological processes, such as photosynthesis, respiration, reactive oxygen species (ROS) metabolism, and hormonal regulation, can be disrupted by HMs [51]; moreover, the life cycle of plants, from germination to final production, can be adversely affected [52,53]. The roots are the first components of a plant to be affected by stress conditions. Consequently, root length and viability are reduced, which eventually disrupt plant photosystems [54] and the absorption of essential nutrients [55]. In addition, root activity and biomass have been significantly decreased under soil acid stress [56].

4.2. Effect of n-HAP with and without IMOs

Overall, n-HAP decreased soil Pb and Cd bioavailability and Pb and Cd concentrations in plant shoots, which led to positive effects on plant growth. Simultaneously, soil acidity was mitigated by n-HAP application. These results correspond with those of previous studies. For example, the addition of n-HAP significantly decreased Cu and Zn uptake by ryegrass and increased its biomass [57]. These findings suggest that n-HAP has potential for the remediation of contaminated soil and safe production of crops. The immobilisation of HMs by n-HAP is primarily due to the formation of phosphate precipitates with a considerably low solubility and bioaccessibility [57,58,59,60]. Amendments with P-containing materials generally decrease Cd and Pb mobility by precipitating pyromorphite-type minerals [58,61,62,63]. In this study, shoot Pb and Cd concentrations decreased with n-HAP application, which is consistent with the low DTPA-extracted Cd and Pb concentrations in the soil.
Soil pH generally influences the mobility and bioavailability of metallic contaminants and their absorption by plants [64,65]. A high soil pH generally facilitates the immobilisation of Cd and Pb, leading to low phytoavailability [58,66]. Our results demonstrate that n-HAP increased the soil pH, and the soil pH correlated positively with the plant biomass, but negatively (p < 0.05) with shoot Cd and Pb concentrations (Figure 5), confirming that soil pH is a key factor influencing plant growth and controlling HMs’ bioavailability and accumulation by plants in acidic soil. Furthermore, the liming effect facilitates the precipitation of HMs by forming insoluble oxyhydroxides and hydroxides [67]. Owing to its chemical composition, n-HAP can release OH− to increase soil pH, thereby inducing a liming effect [60]. Notably, in multiple-metal-contaminated soils, the presence of one metal can alleviate the immobilisation efficiency of the other because of adsorption site competition between them [67]. In this study, the available Pb concentration was positively related to shoot Cd concentration in both soils (Figure 5), thereby confirming this fact.
The combined application of IMOs and n-HAP exhibited synergistically decreased DTPA-extractable Cd and Pb concentrations in slightly contaminated soil; however, no synergistic effect was observed in moderately contaminated soil. Some studies have revealed that stabilising amendments in the heavy-metal-polluted soil aided the recovery of soil bacterial diversity and soil microbial metabolic activities related to Cd and Pb transformation and enriched genera related to nutrient activation, particularly at low metal concentrations [68,69,70,71]. Our results suggest that n-HAP, along with several taxa, may improve the immobilisation efficiencies of DTPA-extractable Cd and Pb in slightly contaminated soil, whereas IMOs from moderately contaminated soil developed many strains tolerant to HMs, thereby activating the available Cd in moderately contaminated soil.

4.3. Effect of γ-PGA with and without IMOs

In this study, growth inhibition was effectively alleviated in moderately contaminated soil and, in slightly contaminated soil, the available Pb was reduced when coriander was treated with γ-PGA. These results indicate that γ-PGA significantly alleviated the damage caused by HM stress. Similar results were obtained in previous studies, where the root and shoot biomass at Cd and Pb concentrations of exposed cucumber seedlings were significantly decreased, and growth inhibition was effectively alleviated following the addition of γ-PGA. This may be due to Cd2+ and Pb2+ adsorption by γ-PGA, whereby Cd and Pb transform from a free into a chelating state [30]. Several types of metal ions are effectively chelated by γ-PGA, and the reaction between γ-PGA and metals could change the helix–coil transition, which might affect the binding capacity of metals [72,73].
Previous research has revealed that HMs in soil reduce the amount of microbial biomass and change the community structure [74], and several studies have revealed that γ-PGA alleviates the toxic effects of Cd and Pb on soil microorganisms [30]. The effect of increasing shoot and root dry biomass in γ-PGA with IMO treatment in moderately contaminated soil was additive. Thus, γ-PGA can be used as a substrate to both improve the tolerance of some plant-growth-promoting microorganisms and increase the abundance of these microorganisms.

5. Conclusions

Applying n-HAP, with and without IMOs, significantly increased shoot dry biomass and reduced shoot Cd and Pb concentrations and DTPA-extracted Cd and Pb concentrations in both slightly and moderately contaminated soils in most cases. The application of γ-PGA, with and without IMOs, significantly reduced DTPA-extracted Pb in slightly contaminated soil. Irrespective of amendments, independently applied IMOs effectively increased shoot dry biomass and DTPA-extracted Cd in moderately contaminated soil. The combined application of IMOs with n-HAP synergistically decreased DTPA-extracted Cd and Pb in slightly contaminated soil, whereas the combination of γ-PGA and IMOs substantially increased shoot dry biomass in moderately contaminated soil. In conclusion, these results indicated that n-HAP can effectively improve crop production and decrease the Cd and Pb concentrations in coriander cultivated in soils contaminated by HMs, while the effect of γ-PGA was limited. However, the combination of n-HAP and IMOs only had a synergistically effect in reducing HMs’ availability at slightly contaminated levels, while γ-PGA with IMOs only showed an additive effect in promoting plant growth at moderately contaminated levels. Therefore, if microorganisms are properly controlled, soil amendments have a wide application potential for controlling HMs’ pollution of agricultural land, thereby improving crop growth. In addition, more appropriate soil amendments should be selected for safe crop production according to HMs’ pollution levels in the contaminated soil.

Author Contributions

Conceptualization, N.M. and J.G.; Formal analysis, N.M., W.H. and Z.Z.; Methodology, N.M. and J.G.; Writing—original draft, N.M., W.H. and L.L.; Writing—review and editing, N.M., F.W. and J.G. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the China Agriculture Research System of Ministry of Finance (MOF) and Ministry of Agriculture and Rural Affairs (MARA) (CARS-23-B15).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Rai, P.K.; Lee, S.S.; Zhang, M.; Tsang, Y.F.; Kim, K.H. Heavy metals in food crops: Health risks, fate, mechanisms, and management. Environ. Int. 2019, 125, 365–385. [Google Scholar] [CrossRef] [PubMed]
  2. Liu, X.; Song, Q.; Tang, Y.; Li, W.; Xu, J.; Wu, J.; Wang, F.; Brookes, P.C. Human health risk assessment of heavy metals in soil-vegetable system: A multi-medium analysis. Sci. Total Environ. 2013, 463–464, 530–540. [Google Scholar] [CrossRef] [PubMed]
  3. Doabi, S.A.; Karami, M.; Afyuni, M.; Yeganeh, M. Pollution and health risk assessment of heavy metals in agricultural soil, atmospheric dust and major food crops in Kermanshah province, Iran. Ecotoxicol. Environ. Saf. 2018, 163, 153–164. [Google Scholar] [CrossRef] [PubMed]
  4. Peng, H.; Chen, Y.; Weng, L.; Ma, J.; Ma, Y.; Li, Y.; Islam, M.S. Comparisons of heavy metal input inventory in agricultural soils in North and South China: A review. Sci. Total Environ. 2019, 660, 776–786. [Google Scholar] [CrossRef]
  5. Nicholson, F.A.; Smith, S.R.; Alloway, B.J.; Carlton-Smith, C.; Chambers, B.J. An inventory of heavy metals inputs to agricultural soils in England and Wales. Sci. Total Environ. 2003, 311, 205–219. [Google Scholar] [CrossRef]
  6. Liu, L.; Li, W.; Song, W.; Guo, M. Remediation techniques for heavy metal-contaminated soils: Principles and applicability. Sci. Total Environ. 2018, 633, 206–219. [Google Scholar] [CrossRef]
  7. Shi, C.; Cui, Y.; Lu, J.; Zhang, B. Sulfur-based autotrophic biosystem for efficient vanadium (V) and chromium (VI) reductions in groundwater. Chem. Eng. J. 2020, 395, 124972. [Google Scholar] [CrossRef]
  8. Gu, P.; Zhang, Y.; Xie, H.; Wei, J.; Zhang, X.; Huang, X.; Wang, J.; Lou, X. Effect of cornstalk biochar on phytoremediation of Cd-contaminated soil by Beta vulgaris var. cicla L. Ecotoxicol. Environ. Saf. 2020, 205, 111144. [Google Scholar] [CrossRef]
  9. Khalid, S.; Shahid, M.; Niazi, N.K.; Murtaza, B.; Bibi, I.; Dumat, C. A comparison of technologies for remediation of heavy metal contaminated soils. J. Geochem. Explor. 2017, 182, 247–268. [Google Scholar] [CrossRef] [Green Version]
  10. Li, Y.; Wang, X.; Xu, H.; Xia, P.; Wang, H.; Jing, H.; Li, J.; Zhao, J. High zinc removal from water and soil using struvite-supported diatomite obtained by nitrogen and phosphate recovery from wastewater. Environ. Chem. Lett. 2017, 16, 569–573. [Google Scholar] [CrossRef]
  11. Seshadri, B.; Bolan, N.S.; Choppala, G.; Kunhikrishnan, A.; Sanderson, P.; Wang, H.; Currie, L.D.; Tsang, D.C.W.; Ok, Y.S.; Kim, G. Potential value of phosphate compounds in enhancing immobilization and reducing bioavailability of mixed heavy metal contaminants in shooting range soil. Chemosphere 2017, 184, 197–206. [Google Scholar] [CrossRef] [PubMed]
  12. Zhang, Z.; Li, M.; Chen, W.; Zhu, S.; Liu, N.; Zhu, L. Immobilization of lead and cadmium from aqueous solution and contaminated sediment using nano-hydroxyapatite. Environ. Pollut. 2010, 158, 514–519. [Google Scholar] [CrossRef] [PubMed]
  13. El-Nagar, D.A.; Massoud, S.A.; Ismail, S.H. Removal of some heavy metals and fungicides from aqueous solutions using nano-hydroxyapatite, nano-bentonite and nanocomposite. Arab. J. Chem. 2020, 13, 7695–7706. [Google Scholar] [CrossRef]
  14. Yan, Y.; Qi, F.; Zhao, S.; Luo, Y.; Gu, S.; Li, Q.; Zhang, L.; Zhou, S.; Bolan, N. A new low-cost hydroxyapatite for efficient immobilization of lead. J. Colloid Interface Sci. 2019, 553, 798–804. [Google Scholar] [CrossRef]
  15. Feng, Y.; Yang, J.; Liu, W.; Yan, Y.; Wang, Y. Hydroxyapatite as a passivator for safe wheat production and its impacts on soil microbial communities in a Cd-contaminated alkaline soil. J. Hazard. Mater. 2021, 404, 124005. [Google Scholar] [CrossRef]
  16. Shaheen, S.M.; Rinklebe, J. Impact of emerging and low cost alternative amendments on the (im)mobilization and phytoavailability of Cd and Pb in a contaminated floodplain soil. Ecol. Engin. 2015, 74, 319–326. [Google Scholar] [CrossRef]
  17. Liu, C.; Wang, L.; Yin, J.; Qi, L.P.; Feng, Y. Combined amendments of nano-hydroxyapatite immobilized cadmium in contaminated soil-potato (Solanum tuberosum L.) system. Bull. Environ. Contam. Toxicol. 2018, 100, 581–587. [Google Scholar] [CrossRef]
  18. Guo, Z.; Yang, N.; Zhu, C.; Gan, L. Exogenously applied poly-gamma-glutamic acid alleviates salt stress in wheat seedlings by modulating ion balance and the antioxidant system. Environ. Sci. Pollut. Res. 2017, 24, 6592–6598. [Google Scholar] [CrossRef]
  19. Yang, Z.H.; Dong, C.D.; Chen, C.W.; Sheu, Y.T.; Kao, C.M. Using poly-glutamic acid as soil-washing agent to remediate heavy metal-contaminated soils. Environ. Sci. Pollut. Res. 2018, 25, 5231–5242. [Google Scholar] [CrossRef]
  20. Xu, Z.; Lei, P.; Feng, X.; Li, S.; Xu, H. Analysis of the metabolic pathways affected by poly (gamma-glutamic acid) in Arabidopsis thaliana based on genechip microarray. J. Agric. Food Chem. 2016, 64, 6257–6266. [Google Scholar] [CrossRef]
  21. Sakamoto, S.; Kawase, Y. Adsorption capacities of poly-gamma-glutamic acid and its sodium salt for cesium removal from radioactive wastewaters. J. Environ. Radioact. 2016, 165, 151–158. [Google Scholar] [CrossRef] [PubMed]
  22. Liang, J.; Shi, W. Poly-γ-glutamic acid improves water-stable aggregates, nitrogen and phosphorus uptake efficiency, water-fertilizer productivity, and economic benefit in barren desertified soils of Northwest China. Agric. Water Manag. 2021, 245, 106551. [Google Scholar] [CrossRef]
  23. Bhat, A.R.; Irorere, V.U.; Bartlett, T.; Hill, D.; Kedia, G.; Morris, M.R.; Charalampopoulos, D.; Radecka, I. Bacillus subtilis natto: A non-toxic source of poly-γ-glutamic acid that could be used as a cryoprotectant for probiotic bacteria. AMB Express 2013, 3, 36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Hajdu, I.; Bodnár, M.; Csikós, Z.; Wei, S.; Daróczi, L.; Kovács, B.; Győri, Z.; Tamás, J.; Borbély, J. Combined nano-membrane technology for removal of lead ions. J. Memb. Sci. 2012, 409–410, 44–53. [Google Scholar] [CrossRef]
  25. Yin, A.; Jia, Y.; Qiu, T.; Gao, M.; Cheng, S.; Wang, X.; Sun, Y. Poly-γ-glutamic acid improves the drought resistance of maize seedlings by adjusting the soil moisture and microbial community structure. Appl. Soil Ecol. 2018, 129, 128–135. [Google Scholar] [CrossRef]
  26. Xu, Z.; Lei, P.; Feng, X.; Xu, X.; Liang, J.; Chi, B.; Xu, H. Calcium involved in the poly (gamma-glutamic acid)-mediated promotion of Chinese cabbage nitrogen metabolism. Plant Physiol. Biochem. 2014, 80, 144–152. [Google Scholar] [CrossRef]
  27. Luo, Z.; Guo, Y.; Liu, J.; Qiu, H.; Zhao, M.; Zou, W.; Li, S. Microbial synthesis of poly-gamma-glutamic acid: Current progress, challenges, and future perspectives. Biotechnol. Biofuels 2016, 9, 134. [Google Scholar] [CrossRef] [Green Version]
  28. Lei, P.; Xu, Z.; Liang, J.; Luo, X.; Zhang, Y.; Feng, X.; Xu, H. Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant Growth Regul. 2015, 78, 233–241. [Google Scholar] [CrossRef]
  29. Inbaraj, B.S.; Wang, J.S.; Lu, J.F.; Siao, F.Y.; Chen, B.H. Adsorption of toxic mercury(II) by an extracellular biopolymer poly (gamma-glutamic acid). Bioresour. Technol. 2009, 100, 200–207. [Google Scholar] [CrossRef]
  30. Pang, X.; Lei, P.; Feng, X.; Xu, Z.; Xu, H.; Liu, K. Poly-gamma-glutamic acid, a bio-chelator, alleviates the toxicity of Cd and Pb in the soil and promotes the establishment of healthy Cucumis sativus L. seedling. Environ. Sci. Pollut. Res. 2018, 25, 19975–19988. [Google Scholar] [CrossRef]
  31. Ye, S.; Zhao, Z. Seismic response of prestressed anchors with frame structure. Math. Probl. Eng. 2020, 2020, 9029045. [Google Scholar] [CrossRef]
  32. Park, J.H.; Bolan, N.; Megharaj, M.; Naidu, R. Isolation of phosphate solubilizing bacteria and their potential for lead immobilization in soil. J. Hazard. Mater. 2011, 185, 829–836. [Google Scholar] [CrossRef] [PubMed]
  33. Oziegbe, O.; Oluduro, A.O.; Oziegbe, E.J.; Ahuekwe, E.F.; Olorunsola, S.J. Assessment of heavy metal bioremediation potential of bacterial isolates from landfill soils. Saudi J. Biol. Sci. 2021, 28, 3948–3956. [Google Scholar] [CrossRef] [PubMed]
  34. Griffiths, B.S.; Philippot, L. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol. Rev. 2013, 37, 112–129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Liu, J.L.; Yao, J.; Wang, F.; Min, N.; Gu, J.H.; Li, Z.F.; Sunahara, G.; Duran, R.; Solevic-Knudsen, T.; Hudson-Edwards, K.A.; et al. Bacterial diversity in typical abandoned multi-contaminated nonferrous metal(loid) tailings during natural attenuation. Environ. Pollut. 2019, 247, 98–107. [Google Scholar] [CrossRef]
  36. Kohler, J.; Caravaca, F.; Azcon, R.; Diaz, G.; Roldan, A. The combination of compost addition and arbuscular mycorrhizal inoculation produced positive and synergistic effects on the phytomanagement of a semiarid mine tailing. Sci. Total Environ. 2015, 514, 42–48. [Google Scholar] [CrossRef]
  37. Liu, L.; Li, J.W.; Yue, F.X.; Yan, X.; Wang, F.; Bloszies, S.; Wang, Y. Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere 2018, 194, 495–503. [Google Scholar] [CrossRef]
  38. Hammer, E.C.; Forstreuter, M.; Rillig, M.C.; Kohler, J. Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. Appl. Soil Ecol. 2015, 96, 114–121. [Google Scholar] [CrossRef]
  39. Hammer, E.C.; Balogh-Brunstad, Z.; Jakobsen, I.; Olsson, P.A.; Stipp, S.L.S.; Rillig, M.C. A mycorrhizal fungus grows on biochar and captures phosphorus from its surfaces. Soil Biol. Biochem. 2014, 77, 252–260. [Google Scholar] [CrossRef]
  40. Liu, W.; Zuo, Q.; Zhao, C.; Wang, S.; Shi, Y.; Liang, S.; Zhao, C.; Shen, S. Effects of Bacillus subtilis and nanohydroxyapatite on the metal accumulation and microbial diversity of rapeseed (Brassica campestris L.) for the remediation of cadmium-contaminated soil. Environ. Sci. Pollut. Res. 2018, 25, 25217–25226. [Google Scholar] [CrossRef]
  41. Liu, W.; Feng, Y.; Wu, X.W.; Li, Y.L.; Zhao, H.W.; Fang, Y.Y.; Wang, M.; Wang, S.T. Nanohydroxyapatite combined with white rot fungus can effectively reduce cadmium activity and change the soil microbial populations structure. Fresenius Environ. Bull. 2020, 29, 9644–9653. [Google Scholar]
  42. Bender, S.F.; Wagg, C.; van der Heijden, M.G.A. An Underground revolution: Biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 2016, 31, 440–452. [Google Scholar] [CrossRef] [PubMed]
  43. Zhong, T.Y.; Xue, D.W.; Zhao, L.M.; Zhang, X.Y. Concentration of heavy metals in vegetables and potential health risk assessment in China. Environ. Geochem. Health 2018, 40, 313–322. [Google Scholar] [CrossRef] [PubMed]
  44. Deepa, B.; Swathi, A.; Rajendra, H. Evaluation of antiarthritic activity of Coriander seed essential oil in Wistar albino rats. Res. J. Pharm. Technol. 2020, 13, 761–766. [Google Scholar] [CrossRef]
  45. Zhu, F.; He, S.Y.; Shang, Z.F. Effect of vegetables and nano-particle hydroxyapatite on the remediation of cadmium and phosphatase activity in rhizosphere soil through immobilization. Int. J. Phytorem. 2019, 21, 610–616. [Google Scholar] [CrossRef]
  46. Lu, R.K. Analytical Methods of Soil and Agricultural Chemistry; China Agricultural Science and Technology Press: Beijing, China, 2000. [Google Scholar]
  47. Carvalho, M.E.A.; Piotto, F.A.; Gaziola, S.A.; Jacomino, A.P.; Jozefczak, M.; Cuypers, A.; Azevedo, R.A. New insights about cadmium impacts on tomato: Plant acclimation, nutritional changes, fruit quality and yield. Food Energy Secur. 2018, 7, e00131. [Google Scholar] [CrossRef] [Green Version]
  48. Poschenrieder, C.; Cabot, C.; Martos, S.; Gallego, B.; Barcelo, J. Do toxic ions induce hormesis in plants? Plant Sci. 2013, 212, 15–25. [Google Scholar] [CrossRef]
  49. Vivas, A.; Vörös, A.; Biró, B.; Barea, J.M.; Ruiz-Lozano, J.M.; Azcón, R. Beneficial effects of indigenous Cd-tolerant and Cd-sensitive Glomus mosseae associated with a Cd-adapted strain of Brevibacillus sp. in improving plant tolerance to Cd contamination. Appl. Soil Ecol. 2003, 24, 177–186. [Google Scholar] [CrossRef]
  50. Metwally, A.; Safronova, V.I.; Belimov, A.A.; Dietz, K.J. Genotypic variation of the response to cadmium toxicity in Pisum sativum. J. Exp. Bot. 2005, 56, 167–178. [Google Scholar] [CrossRef]
  51. Hasan, M.K.; Cheng, Y.; Kanwar, M.K.; Chu, X.Y.; Ahammed, G.J.; Qi, Z.Y. Responses of plant proteins to heavy metal stress—A review. Front. Plant Sci. 2017, 8, 1492. [Google Scholar] [CrossRef] [Green Version]
  52. Shekari, L.; Aroiee, H.; Mirshekari, A.; Nemati, H. Protective role of selenium on cucumber (Cucumis sativus L.) exposed to cadmium and lead stress during reproductive stage role of selenium on heavy metals stress. J. Plant Nutr. 2019, 42, 529–542. [Google Scholar] [CrossRef]
  53. Hoque, M.N.; Tahjib-Ul-Arif, M.; Hannan, A.; Sultana, N.; Akhter, S.; Hasanuzzaman, M.; Akter, F.; Hossain, M.S.; Abu Sayed, M.; Hasan, M.T.; et al. Melatonin modulates plant tolerance to heavy metal stress: Morphological responses to molecular mechanisms. Int. J. Mol. Sci. 2021, 22, 11445. [Google Scholar] [CrossRef] [PubMed]
  54. Farid, M.; Ali, S.; Rizwan, M.; Ali, Q.; Abbas, F.; Bukhari, S.A.H.; Saeed, R.; Wu, L.H. Citric acid assisted phytoextraction of chromium by sunflower; morpho-physiological and biochemical alterations in plants. Ecotoxicol. Environ. Saf. 2017, 145, 90–102. [Google Scholar] [CrossRef]
  55. Zhang, H.H.; Xu, Z.S.; Guo, K.W.; Huo, Y.Z.; He, G.Q.; Sun, H.W.; Guan, Y.P.; Xu, N.; Yang, W.; Sun, G.Y. Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicol. Environ. Saf. 2020, 202, 110856. [Google Scholar] [CrossRef] [PubMed]
  56. Tachibana, N.; Yoshikawa, S.; Ikeda, K. Influences of heavy application of nitrogen on soil acidification and root growth in tea fields. Jpn. J. Crop. Sci. 1995, 64, 516–522. [Google Scholar] [CrossRef] [Green Version]
  57. Sun, R.J.; Chen, J.H.; Fan, T.T.; Zhou, D.M.; Wang, Y.J. Effect of nanoparticle hydroxyapatite on the immobilization of Cu and Zn in polluted soil. Environ. Sci. Pollut. Res. 2018, 25, 73–80. [Google Scholar] [CrossRef] [PubMed]
  58. Wang, F.Y.; Zhang, S.Q.; Cheng, P.; Zhang, S.W.; Sun, Y.H. Effects of Soil amendments on heavy metal immobilization and accumulation by maize grown in a multiple-metal-contaminated soil and their potential for safe crop production. Toxics 2020, 8, 102. [Google Scholar] [CrossRef]
  59. Lee, H.H.; Owens, V.N.; Park, S.; Kim, J.; Hong, C.O. Adsorption and precipitation of cadmium affected by chemical form and addition rate of phosphate in soils having different levels of cadmium. Chemosphere 2018, 206, 369–375. [Google Scholar] [CrossRef]
  60. Zeng, G.M.; Wan, J.; Huang, D.L.; Hu, L.; Huang, C.; Cheng, M.; Xue, W.J.; Gong, X.M.; Wang, R.Z.; Jiang, D.N. Precipitation, adsorption and rhizosphere effect: The mechanisms for phosphate-induced Pb immobilization in soils—A review. J. Hazard. Mater. 2017, 339, 354–367. [Google Scholar] [CrossRef]
  61. Cao, X.D.; Wahbi, A.; Ma, L.N.; Li, B.; Yang, Y.L. Immobilization of Zn, Cu, and Pb in contaminated soils using phosphate rock and phosphoric acid. J. Hazard. Mater. 2009, 164, 555–564. [Google Scholar] [CrossRef]
  62. Xu, Y.P.; Schwartz, F.W.; Traina, S.J. Sorption of Zn2+ and Cd2+ on hydroxyapatite surface. Environ. Sci. Technol. 1994, 28, 1472–1480. [Google Scholar] [CrossRef] [PubMed]
  63. Ryan, J.A.; Zhang, P.C.; Hesterberg, D.; Chou, J.; Sayers, D.E. Formation of chloropyromorphite in a lead-contaminated soil amended with hydroxyapatite. Environ. Sci. Technol. 2001, 35, 3798–3803. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Zeng, F.R.; Ali, S.; Zhang, H.T.; Ouyang, Y.B.; Qiu, B.Y.; Wu, F.B.; Zhang, G.P. The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ. Pollut. 2011, 159, 84–91. [Google Scholar] [CrossRef]
  65. Collins, C. Uptake of organic pollutants and potentially toxic elements (PTEs) by crops. In Persistent Organic Pollutants and Toxic Metals in Foods; Rose, M., Fernandes, A., Eds.; Woodhead Publishing Limited: Cambridge, UK, 2013; pp. 129–144. [Google Scholar]
  66. Lim, J.E.; Ahmad, M.; Lee, S.S.; Shope, C.L.; Hashimoto, Y.; Kim, K.R.; Usman, A.R.A.; Yang, J.E.; Ok, Y.S. Effects of lime-based waste materials on immobilization and phytoavailability of cadmium and lead in contaminated soil. Clean-Soil Air Water 2013, 41, 1235–1241. [Google Scholar] [CrossRef]
  67. Kumpiene, J.; Lagerkvist, A.; Maurice, C. Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments—A review. Waste Manag. 2008, 28, 215–225. [Google Scholar] [CrossRef]
  68. Cui, H.B.; Shi, Y.; Zhou, J.; Chu, H.Y.; Cang, L.; Zhou, D.M. Effect of different grain sizes of hydroxyapatite on soil heavy metal bioavailability and microbial community composition. Agric. Ecosys. Environ. 2018, 267, 165–173. [Google Scholar] [CrossRef]
  69. Li, H.; Liu, L.M.; Luo, L.; Liu, Y.; Wei, J.H.; Zhang, J.C.; Yang, Y.; Chen, A.W.; Mao, Q.M.; Zhou, Y.Y. Response of soil microbial communities to red mud-based stabilizer remediation of cadmium-contaminated farmland. Environ. Sci. Pollut. Res. 2018, 25, 11661–11669. [Google Scholar] [CrossRef]
  70. Chen, Y.; Chen, F.F.; Xie, M.D.; Jiang, Q.Q.; Chen, W.Q.; Ao, T.Q. The impact of stabilizing amendments on the microbial community and metabolism in cadmium-contaminated paddy soils. Chem. Eng. J. 2020, 395, 125132. [Google Scholar] [CrossRef]
  71. Yin, K.; Wang, Q.; Lv, M.; Chen, L. Microorganism remediation strategies towards heavy metals. Chem. Eng. J. 2019, 360, 1553–1563. [Google Scholar] [CrossRef]
  72. Sierra, C.; Martinez-Blanco, D.; Blanco, J.A.; Gallego, J.R. Optimisation of magnetic separation: A case study for soil washing at a heavy metals polluted site. Chemosphere 2014, 107, 290–296. [Google Scholar] [CrossRef]
  73. Panczuk-Figura, I.; Kolodynska, D. Biodegradable chelating agent for heavy metal ions removal. Separat. Sci. Technol. 2016, 51, 2576–2585. [Google Scholar] [CrossRef]
  74. Knight, B.P.; McGrath, S.P.; Chaudri, A.M. Biomass carbon measurements and substrate utilization patterns of microbial populations from soils amended with cadmium, copper, or zinc. Appl. Environ. Microbiol. 1997, 63, 39–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Toxics 10 00408 g001 550
Figure 1. Shoot dry biomass of coriander (Coriandrum sativum L.) grown in slightly contaminated soil (a) and moderately contaminated soil (b). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b, c, d).
Figure 1. Shoot dry biomass of coriander (Coriandrum sativum L.) grown in slightly contaminated soil (a) and moderately contaminated soil (b). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b, c, d).
Toxics 10 00408 g001
Toxics 10 00408 g002 550
Figure 2. Shoot Cd concentrations (a,b) and Pb concentrations (c,d) of coriander in slightly contaminated soil (a,c) and moderately contaminated soil (b,d). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b, c).
Figure 2. Shoot Cd concentrations (a,b) and Pb concentrations (c,d) of coriander in slightly contaminated soil (a,c) and moderately contaminated soil (b,d). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b, c).
Toxics 10 00408 g002
Toxics 10 00408 g003 550
Figure 3. Soil pH following plant harvesting in slightly contaminated soil (a) and moderately contaminated soil (b). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b).
Figure 3. Soil pH following plant harvesting in slightly contaminated soil (a) and moderately contaminated soil (b). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b).
Toxics 10 00408 g003
Toxics 10 00408 g004 550
Figure 4. Available Cd concentration (a,b) and available Pb concentration (c,d) in slightly contaminated soil (a,c) and moderately contaminated soil (b,d). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b, c, d).
Figure 4. Available Cd concentration (a,b) and available Pb concentration (c,d) in slightly contaminated soil (a,c) and moderately contaminated soil (b,d). Non-inoculated control and indigenous microorganism (IMO) inoculation are represented by NM and M, respectively. Non-amendment control, nano-hydroxyapatite (n-HAP), and poly-γ-glutamic acid (γ-PGA) treatments are represented by CK, n-HAP, and γ-PGA, respectively. Data are represented as ±SE of five replicates. The significant differences between different treatments calculated using Duncan’s multiple range test following significant one-way ANOVA (p < 0.05) are indicated by different lowercase letters (a, b, c, d).
Toxics 10 00408 g004
Toxics 10 00408 g005 550
Figure 5. Correlation analysis among dry biomass, pH, Cd and Pb concentration, and available Cd and Pb concentration in slightly (a) and moderately (b) contaminated soils.
Figure 5. Correlation analysis among dry biomass, pH, Cd and Pb concentration, and available Cd and Pb concentration in slightly (a) and moderately (b) contaminated soils.
Toxics 10 00408 g005
Table
Table 1. Major physicochemical attributions of the contaminated soil.
Table 1. Major physicochemical attributions of the contaminated soil.
SoilspHECTPOlsen-PSOCAvailable CdTotal CdAvailable PbTotal Pb
(ds/cm)(g/kg)(mg/kg)(g/kg)(mg/kg)(mg/kg)(mg/kg)(mg/kg)
Slightly contaminated4.56 ± 0.25376 ± 70.50 ± 0.1017.9 ± 0.526.5 ± 1.10.21 ± 0.010.29 ± 0.01 (0.30) 113.8 ± 0.550.9 ± 3.0 (70.0) 1
Moderately contaminated3.85 ± 0.13271 ± 40.82 ± 0.0360.0 ± 2.917.0 ± 0.30.66 ± 0.061.08± 0.05 (1.50) 229.4 ± 1.0100.0 ± 1.8 (400.0) 2
Note: 1, 2 Data are from the “Soil Environmental Quality—Risk control standard for soil contamination of agricultural land (GB 15618-2018)”. 1 “Screening value” means potential risks for agricultural food security, crop growth, or soil quality if pollutant concentrations exceed this value. 2 “Intervention value” means the soil should be strictly controlled for agricultural production if pollutant concentrations exceed this value. Abbreviations: EC, electrical conductivity; TP, total phosphorous; Olsen-P, available phosphorous; SOC, soil organic carbon. Data are mean ± SE (n = 3).
Table
Table 2. Significance levels (F value) of indigenous microorganism, amendments, contaminated levels and their second- and third-order interactions in shoot biomass, shoot Cd and Pb concentration, root biomass, root Cd and Pb concentration, available Cd and Pb concentration, and pH values according to a three-way ANOVA.
Table 2. Significance levels (F value) of indigenous microorganism, amendments, contaminated levels and their second- and third-order interactions in shoot biomass, shoot Cd and Pb concentration, root biomass, root Cd and Pb concentration, available Cd and Pb concentration, and pH values according to a three-way ANOVA.
ParameterMACLM × AM × CLA × CLM × A × CL
Shoot biomass13.3 ***56.8 ***5.9 *9.1 ***37.1 ***11.1 ***6.0 **
Shoot Cd concentration7.0 *54.1 ***63.1 ***4.2 *0.91.00.7
Shoot Pb concentration2.412.5 ***22.6 ***0.16.1 *2.90.5
Root biomass6.1 *0.420.0 ***1.45.5*1.71.7
Root Cd concentration4.04.1 *30.8 ***2.52.11.62.1
Root Pb concentration0.620.6 ***0.82.71.36.0 **1.2
pH values1.05.0 *0.70.10.00.00.5
Available Cd concentration98.2 ***128.0 ***804.0 ***1.899.7 ***12.6 ***0.3
Available Pb concentration0.1107.0 ***310.0 ***2.20.41.51.8
Note: M represents the two inocula (non-inoculated control and indigenous microorganism); A represents the amendments (CK, n-HAP, and γ-PGA); and CL represents the contaminated levels (slightly and moderately contaminated). The significance of the effect is indicated by * p < 0.05, ** p < 0.01, and *** p < 0.001.
Table
Table 3. Dry biomass, Cd concentration, and Pb concentration in the root of coriander (Coriandrum sativum L.).
Table 3. Dry biomass, Cd concentration, and Pb concentration in the root of coriander (Coriandrum sativum L.).
TreatmentsDry Biomass (g/pot)Cd Concentration (mg/kg)Pb Concentration (mg/kg)
NMMNMMNMM
Slightly contaminated
CK0.064 a0.082 a3.18 cd4.69 bc23.8 b38.9 a
n-HAP0.040 a0.042 a2.47 d3.25 cd7.4 c9.51 c
γ-PGA0.050 a0.042 a6.04 ab6.73 a47.1 a49.8 a
Moderately contaminated
CK0.065 b0.190 ab9.62 b86.0 a34.5 ab40.7 a
n-HAP0.200 ab0.225 ab10.2 b7.6 b33.4 ab15.0 b
γ-PGA0.078 b0.353 a11.0 ab18.7 ab31.7 ab40.0 a
Note: NM, non-inoculated control; M, indigenous microorganisms; CK, non-amendment control; n-HAP, nano-hydroxyapatite; γ-PGA, poly-γ-glutamic acid. Data are represented as mean of five replicates; different letters indicate significant differences between six treatments at p < 0.05.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Mi, N.; Hao, W.; Zhou, Z.; Li, L.; Wang, F.; Gai, J. Effects of Amendments and Indigenous Microorganisms on the Growth and Cd and Pb Uptake of Coriander (Coriandrum sativum L.) in Heavy Metal-Contaminated Soils. Toxics 2022, 10, 408. https://doi.org/10.3390/toxics10080408

AMA Style

Mi N, Hao W, Zhou Z, Li L, Wang F, Gai J. Effects of Amendments and Indigenous Microorganisms on the Growth and Cd and Pb Uptake of Coriander (Coriandrum sativum L.) in Heavy Metal-Contaminated Soils. Toxics. 2022; 10(8):408. https://doi.org/10.3390/toxics10080408

Chicago/Turabian Style

Mi, Nana, Wenying Hao, Zixin Zhou, Longcheng Li, Fayuan Wang, and Jingping Gai. 2022. "Effects of Amendments and Indigenous Microorganisms on the Growth and Cd and Pb Uptake of Coriander (Coriandrum sativum L.) in Heavy Metal-Contaminated Soils" Toxics 10, no. 8: 408. https://doi.org/10.3390/toxics10080408

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop