Next Article in Journal
Which Assessment of Coach-Created Motivational Climate Better Predicts Young Athletes’ Engagement over a Season? Athletes’ Perceptions and Match Observations Do
Next Article in Special Issue
Insights into Opposite and Positive Effects of Biochar and Organic Fertilizer on Red Soil Properties and Growth of Pennisetum giganteum
Previous Article in Journal
The Role of Two Social Marketing Strategies and Communication Design in Chinese Households’ Waste-Sorting Intentions and Behavior: A Theory of Planned Behavior Approach
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 15
Issue 6
10.3390/su15065177
sustainability-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

Bacillus Thuringiensis Enhances the Ability of Ryegrass to Remediate Cadmium-Contaminated Soil

by
Jiyuan Jin
1,2,*,
Ruidong Mi
1,
Qiao Li
1,
Jian Lang
1,
Yushu Lan
3,
Na Huang
3 and
Gang Yang
3,*
1
Power China of Chengdu Engineering Corporation Limited, Chengdu 611130, China
2
College of Environment and Ecology, Chengdu University of Technology, Chengdu 610059, China
3
College of Environment Sciences, Sichuan Agricultural University, Chengdu 611130, China
*
Authors to whom correspondence should be addressed.
Sustainability 2023, 15(6), 5177; https://doi.org/10.3390/su15065177
Submission received: 8 January 2023 / Revised: 24 February 2023 / Accepted: 26 February 2023 / Published: 15 March 2023
(This article belongs to the Special Issue Advanced Methods and Technologies in Soil Metal Pollution Removal)
Browse Figures
Versions Notes

Abstract

:
Phytoremediation technology has been widely used for the remediation of heavy metals in soil due to its favorable environmental and ecological effects, but establishing a single phytoremediation technology can result in bottlenecks, such as a long cycle, low biomass, and difficulty in root absorption. At present, inoculation with microorganisms that could assist plants in their remediation of contaminated soils is attracting increasing attention. Therefore, in this study we selected ryegrass and Bacillus thuringiensis (SY) and analyzed the effects of SY inoculation on the growth of ryegrass, including the accumulation of Cd in ryegrass, changes in heavy metal forms, and the heavy metal content in rhizosphere soil, using pot experiments. The results indicate that SY inoculation promotes root growth and development of the ryegrass and the accumulation of cadmium in the plants. In addition, SY inoculation increased the levels of soil nutrients and the activities of soil urease, sucrase, and alkaline phosphatase. This study reveals that the use of SY improves the remediation efficiency of ryegrass for cadmium-contaminated soil, and supports the application potential of microorganisms in soil remediation technology.

1. Introduction

Cadmium (Cd) is a highly toxic pollutant, however, the Cd content in the vibrato of the soil is generally low. However, according to China’s “Pollution Bulletin”, cadmium is the number one heavy metal pollutant in Chinese farmland [1]. Based on the literature reports, farmland soil heavy metal Cd pollution is mainly caused by an unreasonable discharge of industry and agriculture [2,3]. Excess Cd in the soil can easily lead to a decline in the yield and the quality of agricultural products, which can be transmitted through the food chain, thus endangering human health [4]. Problems of high cost, soil destruction, and secondary pollution limit the development of traditional remediation methods for Cd pollution in soil [5]. Therefore, there is an increasing demand for environmentally friendly and low-cost restoration technologies.
Phytoremediation technology has broad prospects for application due to the advantages of good environmental, economic, and social benefits, and it has been widely used in the remediation of different types of Cd-contaminated soils [6]. At present, enrichment plants, such as sedum [7], ryegrass [8,9], and vetiver [10] have been found, and relevant research results have been obtained in soil heavy metal pollution remediation. Numerous studies have shown that phytoremediation techniques can reduce soil toxicity by extracting, transferring, absorbing, transforming, or stabilizing heavy metal pollutants in the soil through plant rhizosphere and microbial ecosystems [11]. As a typical type of hyperaccumulator, ryegrass has a strong ability to accumulate of Cd, which has the characteristics of fast growth, strong tillering ability and strong tolerance to heavy metals, and it has already been used in soil phytoremediation [12,13]. Li et al. [9] analyzed the remediation effect of different concentrations of ethylenediaminetetraacetic acid (EDTA) fortified ryegrass on heavy metals in sludge soil. However, the addition of EDTA-like chemicals might cause secondary soil pollution and potential ecological risks [13].
At present, the commonly used methods for assisting the phytoremediation of soil Cd pollution include agronomic measures, chemical methods, and biological methods [5]. Studies have shown that microorganisms play a crucial role in soil biogeochemical cycles and processes, and that plant-associated bacteria have the potential to promote plant growth and resistance under stress conditions. Thus the presence of certain microorganisms could improve soil fertility and productivity, and assist in the phytoremediation of soil [14]. Therefore, in recent years, the technology for microbial-enhanced phytoremediation of heavy metal-contaminated soil has come to the fore because of its advantages for economic and environmental protection. Through hydroponic experiments, Chen [15] verified that Sphingomonas SaMR12 inoculation could promote plant growth and increase the accumulation of Cd in plants. Following inoculation, the secretion of oxalic acid, citric acid, and succinic acid by the roots increased, which slowed down the toxicity of Cd to the plant. Bacillus sp. plays a key role in promoting plant growth and changing the uptake of heavy metals by plants, which is beneficial for improving the efficiency of plant remediation of soil [16]. Li [17] showed that Bacillus endophyte strains significantly increased the biomass (13–71%) and Cd uptake (41–160%) of hybrid Pennisetum. The experimental results of Deng [18] found that, after inoculation with Bacillus megaterium, the Cd content in the upper part of Sedum increased to 29.2–60.4%, which significantly improved the remediation efficiency for Cd-contaminated farmland soil. Both Bacillus thuringiensis and ryegrass have been widely used in the remediation of environmental pollution, but there are still some research gaps in the application of Bacillus thuringiensis in phytoremediation and the impact of Bacillus thuringiensis on the soil environment.
In this study, Bacillus thuringiensis and ryegrass were selected as the research objects, and the effect of Bacillus thuringiensis inoculation on the Cd content of the root soil of ryegrass, ryegrass growth, and the Cd absorption capacity was studied using a pot experiment, thus clarifying the effect of Bacillus thuringiensis in strengthening phytoremediation of Cd pollution. This study provides a theoretical reference for microbial-assisted phytoremediation of cadmium-contaminated soil and its practical application.

2. Materials and Methods

2.1. Test Materials

The strain Bacillus thuringiensis (SY) was provided by Tianjin Huanwei Biology Technology Limited Company. The test soil was collected in the Chengdu Plain of Sichuan Province, and the type of soil was paddy soil. The experimental plant ryegrass (perennial) was purchased from the Liucheng Seed Management Department of Wenjiang.
Bacillus was inoculated in LB liquid medium, incubated at 150 r Min−1 at 28 ℃ for 24 h, and the bacteria suspensions were centrifuged at 8000 r Min−1 for 5 min to collect the bacteria. The bacteria were cleaned twice with sterile high purity water, and then re-suspended in normal saline to adjust the OD600 value of the bacteria solution to about 1.0 for use. It was about 109 cfu/mL.

2.2. Test Design

Air-dried and screened contaminated soil (800 g) was placed in a bowl (165 mm × 130 mm) as a culture container. Seeds of ryegrass were disinfected, seeds were sown in matrix sand soil for culture, and seedlings with the same growth rate were selected and transplanted into pots of contaminated soil, with 15 plants in each pot. After transplantation, 15 mL the Bacillus thuringiensis suspension was added near the rhizosphere of the plants, and the same amount of sterilizing water was added to CK to replace SY. A total of 9 pots were set up for each treatment, with a total of 18 pots of ryegrass. Inoculation was completed within 2 h, and the growth time of the ryegrass after transplantation was calculated from the day of inoculation. The nutrient solution was the Hoagland nutrient solution, which was prepared in strict accordance with the instructions. The concentration of nutrients was Ca(NO3)2 = 945 mg/L, KNO3 = 607 mg/L, (NH4)3PO4 = 115 mg/L, MgSO4 = 493 mg/L, trace elements 5 mL/L, pH = 6. The fertilization frequency was 10 d/time. The tests were conducted in the greenhouse of the Chongzhou Modern Agriculture Research and Development Base of Sichuan Agricultural University. The field water capacity of the soil was kept at 60–70% during the testing process, and the nutrient solution was applied regularly.

2.3. Sample Collection and Processing

Following the different treatment regimes, the above-ground and underground (roots) parts of the plants were collected on days 0, 10, 20, and 30, and dried to constant weight after cleaning. At the same time, rhizosphere soil samples were collected and stored for later use after natural air drying, grinding, and screening.

2.4. Determination Methods

2.4.1. Determination of Metals in Plants

The HNO3-HClO4 wet digestion method was adopted and all elements were determined by inductively coupled plasma–mass spectroscopy (ICP–MS). GBW10044 (GBSB-22) was used for quality control to ensure data accuracy. A determination of the soil’s basic physical and chemical properties and available Cd was carried out as described in the section on “Soil agrochemical analysis” in Bao (2000). The heavy metal Cd in rhizosphere solid was digested using HNO3-HF-HClO4 and determined by ICP-optical emission spectroscopy (OES). GBW07428 (GSS-14) was used as quality control.

2.4.2. Determination of Soil Enzyme Activity

The activity of soil phosphatase was determined using the p-nitrophenyl phosphate disodium colorimetric method; the activity of soil catalase was determined using ultraviolet spectrophotometry; the activity of soil urease was determined by the phenol-sodium hypochlorite colorimetric method; and the activity of soil sucrase was determined using the 3, 5-dinitrosalicylic acid colorimetric method.

2.5. Data Analysis

Excel 2010 and SPSS 2.0 software were used for data analysis and Originpro (https://www.originlab.com/, accessed on 4 January 2023) software was used for the graphs. The significance of the differences was evaluated by one-way analysis of variance (ANOVA) with Duncan’s post hoc tests.

3. Results and Discussion

3.1. Changes in Soil Physical and Chemical Properties after Inoculation with SY

The physicochemical properties of the rhizosphere soil of ryegrass in the control group and the SY group were determined on days 0 and 30, and the results are shown in Table 1. On day 30, the pH under both treatment conditions decreased compared with day 0, which may be related to the small molecular organic acids secreted by SY during the growth process [18,19]. On day 30, the available potassium, phosphorus, alkali-hydrolyzed nitrogen, and organic matter in the SY group were 0.98%, 7.75%, 16.96%, and 18.94% higher than those in the control group. Thus inoculation with SY could improve available nitrogen and organic matter content. It is believed that Bacillus is an important phosphorus-solubilizing bacterium that can transform insoluble phosphate into soluble forms through the action of various enzymes of its own [20] and can solubilize phosphorus and potassium to provide essential nutrients for plant growth, as well as showing strong resistance to heavy metal pollution [21]. In this study, no significant increase in available phosphorus content was observed; the available potassium and phosphorus in the soil decreased on day 30 compared with the day 0, which may be due to the absorption of P and K for the soil during the growth and development of ryegrass.

3.2. Effects of SY Inoculation on Total and Available Cd Content in Root Soil

Figure 1 shows the changes in Cd and available Cd content in soil under the two treatment regimes. Many studies have found that Bacillus has a good activation effect on heavy metal Cd, promoting the migration and transformation of Cd in soil, with good applications for enhancing phytoremediation [22]. After inoculation with SY 20 d, inoculation with SY had the maximum activation effect on the available Cd in the soil. After the enrichment of heavy metals by ryegrass on days 20 and 30, the content of available Cd in the SY group was still 19.53% and 19.88% higher than that in the control group. It can be seen that inoculation of SY could activate Cd in the soil. A large number of studies have shown that heavy metal speciation in the soil is closely related to the pH level [23]. Studies have shown that a decrease in pH of only 0.2 units will increase Cd in the unstable state by 3–5 times [24]. In this study, inoculation with SY reduced the soil pH, which was an important factor leading to the activation of the Cd heavy metal.

3.3. Effects of SY on the Growth of Ryegrass

After inoculation with SY, the dry weight of the above-ground and underground parts of the plant, and the plant height, varied with inoculation time, as shown in Figure 2. Within 20 days of inoculation with SY, the growth of the above-ground part of ryegrass was not significantly improved. On day 30, the effect of SY on the improvement in growth of the above-ground part of ryegrass was more obvious, and the dry weight was 13.41% higher than that in the control group. On day 20, SY significantly promoted the growth of underground parts of the ryegrass, and the dry weight of the underground parts increased by 63.87%. After that, the growth trend for the underground parts in the SY group gradually slowed down, but was still 34.17% higher than that in the control group on day 30. Inoculation with SY showed some promoting effects on the change in plant height for the ryegrass, but the effect was not significant, and the plant height of the SY group was only 3.99%, 4.26%, and 6.19% higher than that of the control group on days 10, 20, and 30, respectively.
In conclusion, the inoculation SY liquid is mainly promoted to the growth of the grass roots of the ryegrass, and the differences in parts on the ground are not insignificant. As a rhizosphere growth-promoting bacterium, SY can improve soil fertility and promote plant growth by promoting the production of indole-3-acetic acid (IAA), siderophore production, phosphate solubilization, and enzyme activity [25,26]. Related studies have also confirmed that SY has a function in promoting plant growth [27].

3.4. Effects of SY Inoculation on the Content and Accumulation of Cd in Ryegrass

Figure 3a shows the changes in the Cd content of ryegrass after inoculation with SY. It can be seen that after the same time, the Cd content in the underground part of the ryegrass in the SY group was significantly higher than that in the control group. On the 10th day and the 20th day, the Cd content in the aerial part of the SY group was 39.83% and 18.80% higher than that in the control group, and the Cd content in the underground part was 9.22% and 18.37% higher than that in the control group, respectively. On the 30th day, the Cd content in the aerial and underground parts of the ryegrass in the SY group was 5.51% and 6.04% higher than that in the control group, respectively. In addition, according to the Cd accumulation of ryegrass at different stages demonstrated in Figure 3b, after 10 days, the accumulation of Cd in the roots of the SY group and the control group gradually began to show differences. On the 30th day, the accumulation of Cd in the SY group reached 13.45 μg pot−1, an increase of 23.38% compared with the control group. It can be seen from the comparison that Cd is mainly enriched in the underground part of ryegrass, and the root system shows a strong ability to absorb Cd, and SY enhances the enrichment of Cd in the root system of ryegrass.
Some scholars believe that plant growth-promoting bacteria contribute to the absorption of Cd by plants, mainly because growth-promoting bacteria induce the formation of plant lateral roots and thus increase the absorption of Cd [28]. In the early stages of treatment, the growth-promotion effect of SY on the underground parts of ryegrass was not obvious, thus the change in Cd uptake in ryegrass roots was not obvious, and the difference in Cd accumulation between the SY group and the control group was not significant. On day 20, there was a significant difference in the growth of ryegrass roots, and the amount of Cd absorption and Cd accumulation in the roots also showed differences at this time. The results indicate that SY promoted the absorption and accumulation of Cd in ryegrass by promoting the growth and development of ryegrass roots.

3.5. Effects of SY Inoculation on Trace Elements in Ryegrass

Figure 4 shows the content of trace elements in the above-ground and underground parts of ryegrass. On day 0, there was no significant difference in the trace element content between the control group and SY treatment groups. With the passage of time after inoculation, the content of trace elements in the SY group was higher than that in the control group, indicating that SY had a promotion effect on the absorption of trace elements in ryegrass. Compared with the control group, Cu content in the above-ground and underground parts of the SY group increased by 1.97–3.93% and 2.18–16.88%, respectively, and the Cu content in ryegrass reached a maximum at about day 10. On day 20, the content of Mn in ryegrass in the SY group had changed the most, compared with the control group, and the above-ground and underground parts increased by 42.79% and 42.66%, respectively. Zn content only showed a significant change on day 30, with the Zn content in the underground part of ryegrass increasing by 13.87% compared with the control group. Inoculation with SY greatly affected the Fe content, especially in the underground part. On day 10, the Fe content in the underground part of ryegrass had increased significantly, and on day 30 the Fe content in the SY group was 78.53% higher than that in the control group, indicating that SY had a much greater promoting effect on Fe absorption in ryegrass. The trace element, Fe, is considered an important factor affecting plant growth [29]. In this study, the growth of underground parts of ryegrass started to be heterogenous from day 10 when the Fe element content started to differ between the two treatment groups. It may be that SY increases the absorption of Fe in ryegrass and promotes root growth [30]. It has been found that inoculation with SY has a significant promotion effect on radish growth in heavy metal-contaminated soil [31].

3.6. Changes in Soil Enzyme Activity after Inoculation with SY

Soil enzyme activity is an important index for evaluating of soil quality, and plays an important role in maintaining soil fertility and responding quickly to environmental changes [32,33]. Soil enzymes actively participate in the decomposition of organic matter and the nutrient cycle, and high enzyme activity also indicates that soil quality is relatively good, with enzymes playing an important role in plant growth and development [34]. Changes in the soil enzymes after inoculation are shown in Figure 5. The trend in the change in soil urease activity (URE) in the control group and the SY group was consistent (Figure 5a). Urease activity increased gradually at the beginning of the treatment and decreased gradually after day 20. There was no significant difference in urease activity between the SY group and the control group at the initial stage, but a significant difference began to occur on day 10. Subsequently, the urease activity of the SY group was always higher than that of the control group, and the urease activity of the SY group was 4.24% higher than that of the control group at day 20 following SY inoculation. Soil phosphatase activity (PHO) was relatively stable in the early stages, but increased with the change in the ryegrass growth cycle after day 10 (Figure 5b). The activity of phosphatase in the SY group was higher than that in the control group during the whole growth stage, with an increase of 1.02–3.27%, indicating that SY could promote phosphatase activity.
Soil sucrase activity (SUC) in the control group increased within 0–20 days, but decreased after 20 days (Figure 5c). Soil sucrase activity in the SY group increased rapidly in the first 10 days, with the highest increase of 21.03%, and began to decrease after day 10. The activity of sucrase in the SY group was higher than in the control group during the whole growth period of ryegrass, and there was a significant difference between the two treatment groups in the first 20 days. The trend in the change of soil catalase activity (CAT) in the two treatment groups was similar (Figure 5d). Catalase activity increased from days 0 to 10, and reached a maximum in both treatment groups on day 10. At this time, catalase activity in the control group was 18.65% higher than that in the SY group. After day 10, the catalase activity in the two treatment groups continued to decrease, but on day 20 the catalase activity of the control group was still 16.80% higher than that of the SY group.
These results show that SY inoculation can increase the activities of various enzymes (urease, phosphatase, and sucrase) in soil, with urease, sucrase, and phosphatase all being important enzymes for transforming the various nutrients required for plant growth [35]. This may be one of the reasons for the rapid plant growth observed in the SY group after 10 days. Soil catalase could be used as an indicator of heavy metal stress in plants, as heavy metal stress induces excessive production of catalase [36]. The results of this study show that inoculation with SY reduced catalase activity, which meant that oxidative stress in the soil was improved, and the toxic effect of heavy metals on ryegrass was reduced.

4. Conclusions

In this study, inoculation of SY improved the available state of cadmium in soil and promoted the growth and uptake of ryegrass roots. The existence of SY may increase the content of available nitrogen and organic matter. In addition, the inoculation of SY assisted the uptake of trace elements (Fe) during the ryegrass remediation process, slightly increased the activities of soil urease, phosphate and invertase, decreased the activity of dioxygenase, and promoted the growth and development of ryegrass roots. accumulation of cadmium. This study verified that SY enhanced the ability of ryegrass to absorb Cd in soil, and clarified the application potential of SY in soil remediation.

Author Contributions

Conceptualization, R.M. and G.Y.; Methodology, J.J., R.M., Y.L. and N.H.; Software, J.L.; Validation, J.L.; Formal analysis, Q.L.; Investigation, R.M. and Q.L.; Resources, G.Y.; Data curation, J.J. and N.H.; Writing—original draft, J.J., N.H. and G.Y.; Supervision, Y.L.; Project administration, Q.L.; Funding acquisition, G.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Power Construction of China grant number (P42819, DJ-ZDXM-2019-42).

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.

References

  1. Wei, L.; Huang, Y.; Huang, L.; Huang, Q.; Li, Y.; Li, X.; Yang, S.; Liu, C.; Liu, Z. Combined biochar and soda residues increases maize yields and decreases grain Cd/Pb in a highly Cd/Pb-polluted acid Udults soil. Agric. Ecosyst. Environ. 2021, 306, 107198. [Google Scholar] [CrossRef]
  2. Hu, B.; Shao, S.; Ni, H.; Fu, Z.; Huang, M.; Chen, Q.; Shi, Z. Assessment of potentially toxic element pollution in soils and related health risks in 271 cities across China. Envrion. Pollut. 2021, 270, 116196. [Google Scholar] [CrossRef]
  3. Zhang, P.; Qin, C.; Hong, X.; Kang, G.; Qin, M.; Yang, D.; Pang, B.; Li, Y.; He, J.; Dick, R. Risk assessment and source analysis of soil heavy metal pollution from lower reaches of Yellow River irrigation in China. Sci. Total Envrion. 2018, 633, 1136–1147. [Google Scholar] [CrossRef]
  4. Zhang, H.; Jin, Q.; Huang, R. Characteristics of Heavy Metal Pollution in Agricultural Soils and Bioaccumulation in Plants of Dabaoshan Mine. Soils 2017, 49, 141–149. [Google Scholar]
  5. Shen, X.; Dai, M.; Yang, J.; Sun, L.; Tan, X.; Peng, C.; Ali, I.; Naz, I. A critical review on the phytoremediation of heavy metals from environment: Performance and challenges. Chemosphere 2022, 291, 132979. [Google Scholar] [CrossRef] [PubMed]
  6. Saxena, G.; Purchase, D.; Mulla, S.; Saratale, G.; Bharagava, R. Phytoremediation of heavy metal-contaminated sites: Eco-environmental concerns, field studies, sustainability issues, and future prospects. Rev. Environ. Contam. Toxicol. Vol. 2019, 249, 71–131. [Google Scholar]
  7. Huang, Y.; Huang, Y.; Hou, J.; Wu, L.; Christie, P.; Liu, W. Microbial community assembly of the hyperaccumulator plant Sedum plumbizincicola in two contrasting soil types with three levels of cadmium contamination. Sci. Total Environ. 2023, 863, 160917. [Google Scholar] [CrossRef]
  8. Xie, H.; Ma, Y.; Wang, Y.; Sun, F.; Liu, R.; Liu, X.; Xu, Y. Biological response and phytoremediation of perennial ryegrass to halogenated flame retardants and Cd in contaminated soils. J. Environ. Chem. Eng. 2021, 9, 106526. [Google Scholar] [CrossRef]
  9. Li, F.; Qiu, Y.; Xu, X.; Yang, F.; Wang, Z.; Feng, J.; Wang, J. EDTA-enhanced phytoremediation of heavy metals from sludge soil by Italian ryegrass (Lolium perenne L.). Ecotoxicol. Environ. Saf. 2020, 191, 110185. [Google Scholar] [CrossRef] [PubMed]
  10. Basant, K.N.; Singh, J.; Kumari, B.; Sinam, G.; Gautam, A.; Singh, G.; Swapnil; Mishra, K.; Mallick, S. Nickel and cadmium phytoextraction efficiencies of vetiver and lemongrass grown on Ni-Cd battery waste contaminated soil: A comparative study of linear and nonlinear models. J. Environ. Manag. 2021, 295, 113144. [Google Scholar]
  11. Dixit, R.; Malaviya, D.; Pandiyan, K.; Singh, U.; Sahu, A.; Shukla, R.; Singh, B.; Rai, J.; Sharma, P.; Lade, H. Bioremediation of heavy metals from soil and aquatic environment: An overview of principles and criteria of fundamental processes. Sustainability 2015, 7, 2189–2212. [Google Scholar] [CrossRef] [Green Version]
  12. Feng, D.; Huang, C.; Xu, W.; Qin, Y.; Li, Y.; Li, T.; Yang, M.; He, Z. Difference of cadmium bioaccumulation and transportation in two ryegrass varieties and the correlation between plant cadmium concentration and soil cadmium chemical forms. Wirel. Pers. Commun. 2020, 110, 291–307. [Google Scholar] [CrossRef]
  13. Zhao, R.; Huang, L.; Peng, X.; Fan, L.; Chen, S.; Qin, P.; Zhang, J.; Chen, A.; Huang, H. Effect of different amounts of fruit peel-based activator combined with phosphate-solubilizing bacteria on enhancing phytoextraction of Cd from farmland soil by ryegrass. Environ. Pollut. 2023, 316, 120602. [Google Scholar] [CrossRef]
  14. Kumar, A.; Vandana, R.; Singh, M.; Pandey, K. Plant growth promoting rhizobacteria (PGPR). A promising approach for disease management. In Microbes and Environmental Management; Studium Press: New Delhi, India, 2015; pp. 195–209. [Google Scholar]
  15. Chen, B.; Zhang, Y.; Rafiq, M.; Khan, K.; Pan, F.; Yang, X.; Feng, Y. Improvement of cadmium uptake and accumulation in Sedum alfredii by endophytic bacteria Sphingomonas SaMR12: Effects on plant growth and root exudates. Chemosphere 2014, 117, 367–373. [Google Scholar] [CrossRef]
  16. El-Meihy, R.; Abou-Aly, H.; Youssef, A.; Tewfike, T.; El-Alkshar, E. Efficiency of heavy metals-tolerant plant growth promoting bacteria for alleviating heavy metals toxicity on sorghum. Environ. Exp. Bot. 2019, 162, 295–301. [Google Scholar] [CrossRef]
  17. Li, Y.; Han, H.; He, L.; Wang, Q.; Sheng, X. Inoculation with endophytic Bacillus megaterium H3 increases Cd phytostabilization and alleviates Cd toxicity to hybrid pennisetum in Cd-contaminated aquatic environments. Environ. Sci. Pollut. Res. 2017, 24, 1416–1423. [Google Scholar] [CrossRef]
  18. Deng, Y.-Q.; Cao, X.-Y.; Tan, C.-Y.; Sun, L.-J.; Peng, X.; Bai, J.; Huang, S.-P. Strengthening the effect of Bacillus megaterium on remediation of Cd-contaminated farmland soil by Sedum plumbizincicola. J. Appl. Ecol. 2020, 31, 3111–3118. [Google Scholar]
  19. Wu, J.; Kamal, N.; Hao, H.; Qian, C.; Liu, Z.; Shao, Y.; Zhong, X.; Xu, B. Endophytic Bacillus megaterium BM18-2 mutated for cadmium accumulation and improving plant growth in Hybrid Pennisetum. Biotechnol. Rep. 2019, 24, e00374. [Google Scholar] [CrossRef]
  20. Abdallah, D.; Frikha-Gargouri, O.; Tounsi, S. Rizhospheric competence, plant growth promotion and biocontrol efficacy of Bacillus amyloliquefaciens subsp. plantarum strain 32a. Biol. Control 2018, 124, 61–67. [Google Scholar] [CrossRef]
  21. Delfim, J.; Gerding, M.; Zagal, E. Phosphorus fractions in Andisol and Ultisol inoculated with Bacillus thuringiensis and phosphorus uptake by wheat. J. Plant Nutr. 2020, 43, 2728–2739. [Google Scholar] [CrossRef]
  22. Din, B.; Rafique, M.; Javed, M.; Kamran, M.; Mehmood, S.; Khan, M.; Sultan, T.; Munis, M.; Chaudhary, H. Assisted phytoremediation of chromium spiked soils by Sesbania Sesban in association with Bacillus xiamenensis PM14: A biochemical analysis. Plant Physiol. Biochem. 2020, 146, 249–258. [Google Scholar] [CrossRef] [PubMed]
  23. Bashir, S.; Shaaban, M.; Hussain, Q.; Mehmood, S.; Zhu, J.; Fu, Q.; Aziz, O.; Hu, H. Influence of organic and inorganic passivators on Cd and Pb stabilization and microbial biomass in a contaminated paddy soil. J. Soils Sediments 2018, 18, 2948–2959. [Google Scholar] [CrossRef]
  24. Zhu, H.; Chen, C.; Xu, C.; Zhu, Q.; Huang, D. Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China. Environ. Pollut. 2016, 219, 99–106. [Google Scholar] [CrossRef]
  25. Khan, N.; Bano, A.; Rahman, M.; Guo, J.; Kang, Z.; Babar, M. Comparative physiological and metabolic analysis reveals a complex mechanism involved in drought tolerance in chickpea (Cicer arietinum L.) induced by PGPR and PGRs. Sci. Rep. 2019, 9, 1–19. [Google Scholar] [CrossRef] [Green Version]
  26. Singh, S.; Kumar, V.; Sidhu, G.; Datta, S.; Dhanjal, D.; Koul, B.; Janeja, H.; Singh, J. Plant growth promoting rhizobacteria from heavy metal contaminated soil promote growth attributes of Pisum sativum L. Biocatal. Agric. Biotechnol. 2019, 17, 665–671. [Google Scholar] [CrossRef]
  27. Jo, H.; Tagele, S.; Pham, H.; Kim, M.-C.; Choi, S.-D.; Kim, M.-J.; Park, Y.-J.; Ibal, J.; Park, G.-S.; Shin, J.-H. Response of soil bacterial community and pepper plant growth to application of Bacillus thuringiensis KNU-07. Agronomy 2020, 10, 551. [Google Scholar] [CrossRef]
  28. Wu, Y.; Ma, L.; Liu, Q.; Vestergård, M.; Topalovic, O.; Wang, Q.; Zhou, Q.; Huang, L.; Yang, X.; Feng, Y. The plant-growth promoting bacteria promote cadmium uptake by inducing a hormonal crosstalk and lateral root formation in a hyperaccumulator plant Sedum alfredii. J. Hazard. Mater. 2020, 395, 122661. [Google Scholar] [CrossRef]
  29. Rout, G.; Sahoo, S. Role of iron in plant growth and metabolism. Rev. Agric. Sci. 2015, 3, 1–24. [Google Scholar] [CrossRef] [Green Version]
  30. Huang, H.; Zhao, Y.; Fan, L.; Jin, Q.; Yang, G.; Xu, Z. Improvement of manganese phytoremediation by Broussonetia papyrifera with two plant growth promoting (PGP) Bacillus species. Chemosphere 2020, 260, 127614. [Google Scholar] [CrossRef] [PubMed]
  31. Han, H.; Sheng, X.; Hu, J.; He, L.; Wang, Q. Metal-immobilizing Serratia liquefaciens CL-1 and Bacillus thuringiensis X30 increase biomass and reduce heavy metal accumulation of radish under field conditions. Ecotoxicol. Environ. Saf. 2018, 161, 526–533. [Google Scholar] [CrossRef]
  32. Liu, Y.-N.; Guo, Z.-H.; Xiao, X.-Y.; Wang, S.; Jiang, Z.-C.; Zeng, P. Phytostabilisation potential of giant reed for metals contaminated soil modified with complex organic fertiliser and fly ash: A field experiment. Sci. Total Environ. 2017, 576, 292–302. [Google Scholar] [CrossRef] [PubMed]
  33. Mierzwa-Hersztek, M.; Gondek, K.; Baran, A. Effect of poultry litter biochar on soil enzymatic activity, ecotoxicity and plant growth. Appl. Soil Ecol. 2016, 105, 144–150. [Google Scholar] [CrossRef]
  34. Ma, Y.-H.; Fu, S.-L.; Zhang, X.-P.; Zhao, K.; Chen, H. Intercropping improves soil nutrient availability, soil enzyme activity and tea quantity and quality. Appl. Soil Ecol. 2017, 119, 171–178. [Google Scholar] [CrossRef]
  35. Dubey, S.; Shri, M.; Gupta, A.; Rani, V.; Chakrabarty, D. Toxicity and detoxification of heavy metals during plant growth and metabolism. Environ. Chem. Lett. 2018, 16, 1169–1192. [Google Scholar] [CrossRef]
  36. Nascimento, F.; Hernandez, A.; Glick, B.; Rossi, M. Plant growth-promoting activities and genomic analysis of the stress-resistant Bacillus megaterium STB1, a bacterium of agricultural and biotechnological interest. Biotechnol. Rep. 2020, 25, e00406. [Google Scholar] [CrossRef]
Sustainability 15 05177 g001 550
Figure 1. Changes in (a) soil Cd, (b) Cd removal rate, and (c) available Cd content after different periods. Letters (a, b, c, d, e and f) indicate significant difference between treatments.
Figure 1. Changes in (a) soil Cd, (b) Cd removal rate, and (c) available Cd content after different periods. Letters (a, b, c, d, e and f) indicate significant difference between treatments.
Sustainability 15 05177 g001
Sustainability 15 05177 g002 550
Figure 2. Changes in (a) dry weight and (b) plant height of ryegrass. Letters (a, b, c, d and e) indicate significant difference between treatments.
Figure 2. Changes in (a) dry weight and (b) plant height of ryegrass. Letters (a, b, c, d and e) indicate significant difference between treatments.
Sustainability 15 05177 g002
Sustainability 15 05177 g003 550
Figure 3. (a) Content of Cd in the shoot and root. (b) Cd accumulation of ryegrass at different stages. Letters (a, b, c, d, e and f) indicate significant difference between treatments.
Figure 3. (a) Content of Cd in the shoot and root. (b) Cd accumulation of ryegrass at different stages. Letters (a, b, c, d, e and f) indicate significant difference between treatments.
Sustainability 15 05177 g003
Sustainability 15 05177 g004 550
Figure 4. The absorption of trace elements in ryegrass: (a) Cu, (b) Fe, (c) Mn, and (d) Zn. Letters (a, b and c) indicate significant difference between treatments.
Figure 4. The absorption of trace elements in ryegrass: (a) Cu, (b) Fe, (c) Mn, and (d) Zn. Letters (a, b and c) indicate significant difference between treatments.
Sustainability 15 05177 g004
Sustainability 15 05177 g005 550
Figure 5. Changes in soil enzyme activities: (a) URE, (b) PHO, (c) SUC, and (d) CAT. Letters (a, b, c and d) indicate significant difference between treatments.
Figure 5. Changes in soil enzyme activities: (a) URE, (b) PHO, (c) SUC, and (d) CAT. Letters (a, b, c and d) indicate significant difference between treatments.
Sustainability 15 05177 g005
Table
Table 1. Physical and chemical properties of the soil.
Table 1. Physical and chemical properties of the soil.
TreatmentpHAvailable K (mg kg−1)Available P (mg kg−1)Available N (mg kg−1)Organic Matter (g kg−1)
CK-07.68 ± 0.02 a55.28 ± 1.70 a7.75 ± 1.08 a88.45 ± 2.45 a29.20 ± 1.03 a
SY-07.65 ± 0.01 a69.91 ± 1.22 b7.98 ± 0.76 a89.98 ± 0.51 a29.71 ± 0.61 a
CK-307.51 ± 0.01 b34.64 ± 2.48 c5.42 ± 1.03 b87.43 ± 6.34 a26.08 ± 0.78 a
SY-307.46 ± 0.01 c34.98 ± 0.01 c5.84 ± 0.16 b102.26 ± 6.43 b31.02 ± 1.10 b
Letters (a, b and c) indicate significant differences between treatments.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Jin, J.; Mi, R.; Li, Q.; Lang, J.; Lan, Y.; Huang, N.; Yang, G. Bacillus Thuringiensis Enhances the Ability of Ryegrass to Remediate Cadmium-Contaminated Soil. Sustainability 2023, 15, 5177. https://doi.org/10.3390/su15065177

AMA Style

Jin J, Mi R, Li Q, Lang J, Lan Y, Huang N, Yang G. Bacillus Thuringiensis Enhances the Ability of Ryegrass to Remediate Cadmium-Contaminated Soil. Sustainability. 2023; 15(6):5177. https://doi.org/10.3390/su15065177

Chicago/Turabian Style

Jin, Jiyuan, Ruidong Mi, Qiao Li, Jian Lang, Yushu Lan, Na Huang, and Gang Yang. 2023. "Bacillus Thuringiensis Enhances the Ability of Ryegrass to Remediate Cadmium-Contaminated Soil" Sustainability 15, no. 6: 5177. https://doi.org/10.3390/su15065177

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