Selenium improved the combined remediation efficiency of Pseudomonas aeruginosa and ryegrass on cadmium-nonylphenol co-contaminated soil
Graphical abstract
Introduction
Nonylphenol polyethoxylates (NPEOs) are widely used as surfactants and commonly used in the industrial production and commercial supplies, such as detergents, emulsifiers, wetting and dispersing agents, etc (Soares et al., 2008). Nonylphenol (NP) is a degradation intermediate of NPEOs, and as an endocrine-disrupting chemical, it can disrupt the human endocrine system and also induce breast cancer (Sakai, 2001; Kudo et al., 2004; Ding et al., 2019). NP is mainly found in the wastewater of factories that produce chemical demulsifiers, pesticides, and plastics with nonylphenols as additive (Singh et al., 2007; Hermabessiere et al., 2017; Kim et al., 2019). NP in wastewater is inevitably redistributed into the soil, and its concentration in U.S. soil ranges from 68 to 8834 μg kg−1, and up to 2720 μg kg−1 in parts of Canada (Kwak et al., 2017). NP in the environment posed a serious threat to plants. When C. vulgaris and S. capricornutum were cultured in NP contaminated water (NP 0.25–4.0 mg L−1) for 96 h, NP exerted toxic effects by reducing chlorophyll a concentration, inhibiting photosynthesis, and inhibiting antioxidant enzyme activity (Gao and Tam, 2011). However, most of the research on NP has focused on water sludge, and NP pollution in farmland soil has not yet attracted enough attention.
Cd contamination has long been a subject of widespread concern and poses the highest potential ecological risk (He et al., 2019). Besides natural factors, it mainly comes from the mining, atmospheric deposition after combustion emissions, and the application of Cd containing fertilizers and pesticides (Kubier et al., 2019). These factors lead to the aggravation of Cd pollution in farmland soil, and an increasing number of agricultural products contain excessive levels of Cd (Meharg et al., 2013). After Cd enters human body through the food chain, it will cause diseases such as cancer and injury of the central nervous system (Rehman et al., 2017).
It is worth noting that heavy metals and organic contaminants do not usually exist alone. Take China's major watersheds as an example, the content of NP and Cd in the residual sludge from sewage treatment plants in the Pearl River Delta region was up to 65.17 mg kg−1 and 2.72 mg kg−1 respectively (Liu et al., 2016b). The NP-Cd co-contamination area also exists in Lanzhou section of the Yellow River. NP concentration in the water is 34.2–599 ng L−1, and the NP concentration in the sediment is as high as 863.0 μg kg−1, while Cd content in the soil of sewage irrigation area is as high as 0.9 mg kg−1 (Xu et al., 2006; Chen et al., 2009). Long time irrigation with wastewater containing pollutants might lead to co-contamination in soils. For example, after irrigated with wastewater for about 40 years, the Cd content of the soil in XiaoDian was as high as 2.58 mg kg−1, and meanwhile the naphthalene content was 546 μg kg−1 (Khan et al., 2008). When heavy metals and organic pollutants were occurring in soil together, the pollutants may interact with each other. Studies of Sun et al. (2011) indicated that Cd (20 or 50 mg kg−1) in soil reduced the uptake of B[a]P by Tagetes patula by inhibiting it's growth after 4 weeks of incubation, the same is ture for Cu (100 or 500 mg kg−1) and Pb (1000 or 3000 mg kg−1). However, there are differences in the impact of different types and concentrations of heavy metals on PAH, which makes pollution remediation more difficult. Studies of soil culture experiments indicated that the inhibition effect of Pb (339 mg kg−1) on PAH degradation rate is greater than that of Cd at low concentration (134 mg kg−1), but it is opposite at high concentration (Pb 782 mg kg−1, Cd 620 mg kg−1) (Deary et al., 2018).
Lots of approaches had been implemented to control the organic-heavy metals co-contamination. A 40-day potting experiment discovered that 0.1 μM 24-epibrassinolide (EBR) alleviated the toxic effect of Cd (100 μM) and phenanthrene (100 μM) on tomatoes (Ahammed et al., 2013). In the potted experiment of sunflower, the degradation rate of phenanthrene was 96% and pore water Cd2+ reduced by 66% after 120 days of treatment with modified rice straw (5.56 g kg−1 soil) (Elyamine et al., 2019). However, researchers found that there were many disadvantages in these methods, such as secondary pollution, high technical requirements, high cost, and difficult to popularize. It is important to explore more cost-effective and environmentally friendly methods of contamination soil remediation. Phytoremediation, as an efficient way to clean organic-heavy metals co-contaminated soil, is reported (Steliga and Kluk, 2020). It's eco-friendly and doesn't cause secondary pollution, the harvested biomass of phytoremediation materials could be processed by pyrolysis, liquid extraction (Lu et al., 2014; Cui et al., 2018).
Previous studies showed that Festuca arundinacea could be used for heavy metals-petroleum hydrocarbons co-contamination soil remediation. After 6 months of pot experiment with Festuca arundinacea, the removal rates of Pb, Ni, Cd, and petroleum hydrocarbons in the soil were 25.1%, 23.84%, 42.3% and 56%, respectively (Steliga and Kluk, 2020). Furthermore, the results of Fire Phoenix pot experiment proved that it could facilitated the remediation of PAH-Cd co-contamination (PAHs 104.79–144.87 mg kg−1, Cd 15 mg kg−1). After 150 days of planting, the removal rates of PAHs and Cd reached 64.57% and 40.93%, respectively (Dai et al., 2020). Although phytoremediation has its advantages, most of the plant biomass used for pollution remediation is small and the remediation efficiency is limited. Assitant measures for phytoremediation to improve the remediation efficiency should be developed. Microorganisms play important roles in the soil, nitrogen-fixing bacteria, mycorrhizal fungi, and rhizosphere growth-promoting bacteria in rhizosphere soil are closely related to the supply of nutrients such as N, P, Fe, Cu (Chen et al., 2019a). Microorganisms are also essential for the efficient removal of many pollutants such as As, Sb, Cd and methylmercury, no matter it is direct degradation or the joint action of microbial communities (Sun et al., 2020; Zhou et al., 2020).
In terms of P. aeruginosa, it still had high activity even in the medium containing 100 μM Cd2+, and showed strong resistance to Cd (Tang et al., 2018). After 84 h of P. aeruginosa treatment, the degradation rate of NP in water reached about 70% (Shi et al., 2017). Selenium (Se), as one of the essential micronutrients of human body and beneficial elements of plants, can not only improve human health (adequate intake of 15–70 μg·day−1), but also enhance the phytoremediation efficiency in soil contaminated with heavy metals (Zhao et al., 2020; Hamilton, 2004). After applying 5 μM Se to the Pteris vittata L. hydroponic system and cultured for two weeks, the As concentration in the plant increased by 7–45%, compared to the treatment without Se (Srivastava et al., 2009). It might promote the removal of pollutants in soil by facilitating the growth of the plant, relieving oxidative stress, and even combining with heavy metals to form complexes (Lin et al., 2012; Alves et al., 2020). In a 60-day pot experiment, the application of Na2SeO3 (0.5 mg kg−1 or 1.5 mg kg−1) significantly decreased H2O2 and MDA in Alternanthera philoxeroides grown in diesel-contaminated soil, and the reduction efficiency of diesel in the rhizosphere soil increased by about 15% with Se application (Huang et al., 2019).
The effects of Se on plant and microbial communities, as well as the effects of P. aeruginosa on heavy metals and organic pollutants were considered. In this study, we expected to verify the enhanced effect of Se and P. aeruginosa on phytoremediation of Cd-NP co-contaminated soil through pot experiment. Ryegrass was selected as the test plant because it is a wide range of forage grass and has a certain accumulation capacity of heavy metals (Feng et al., 2020). The objectives of the present study were to (1) assess the role of Se and P. aeruginosa on NP and Cd removal, (2) analyze the differences of soil enzyme activity and functional groups, (3) monitor the dynamic process of the whole microbial community, (4) explore different species in different environments and their roles in pollution remediation.
Section snippets
Media, chemicals, and strain
Cd contaminated soil was collected from an vegetable field in Wuhan city (30°60′N,114°33′E), Hubei, China. The soil was air-dried and sieved to remove impurities such as stones and organic residues. And the soil presented the following properties: pH 5.99, organic matter 9.39 g kg−1, alkali-hydrolyzable nitrogen 41.07 mg kg−1, available phosphorus 22.28 mg kg−1, available potassium 160 mg kg−1, and total Cd 1.48 mg kg−1.
Nonylphenol (4-n-nonylphenol, CAS No.84852-15-3) in liquid form was
Plant growth and Cd uptake
Excess concentration of Cd in plant tissues would bring potential risk to human beings, furthermore, translocate into the food chain. The biomass and Cd accumulation in the shoots and roots of ryegrass after 60 days' exposure are shown in Fig. S1 and Fig. 1, respectively. The shoots' biomass of CN5 (p < 0.05) and CN50 (p < 0.01) was significantly lower than that of C, but there was no significant difference in their roots’ biomass (Fig. S1). CN5pSe(Ⅵ) determined an increase of root biomass of
P. aeruginosa and Se in soil promoted plant growth and phytoremediation efficiency
In the present study, the Cd-NP co-contamination inhibited the growth of ryegrass, P. aeruginosa inoculation alleviated this inhibiting effect, and compared with P. aeruginosa inoculated alone, simultaneous application of P. aeruginosa and Se has a stronger effect on the growth of ryegrass (Fig. S1). Studies have shown that a certain concentration of heavy metals combined with organic pollutants inhibited the growth of plants (Chen et al., 2019b; Chen et al., 2020). After 70 days of growing in
Conclusions
This study proved that P. aeruginosa inoculation could promote the phytoremediation of Cd-NP co-contaminated soil, and the application of Se can further improve the efficiency of the micro-phyto combined remediation. The applied P. aeruginosa and Se mainly promoted the removal of pollutants through the following ways: (ⅰ) limit soil adsorption of NP, so as to promote its degradation, (ⅱ) change soil enzyme activity, thereby regulating soil detoxification function and nutrient cycle, (ⅲ) enrich
Credit author statement
Gang Ni: Conceptualization, Methodology, Formal analysis, Investigation, Writing - Original Draft, Writing - Review & Editing, Visualization. Guangyu Shi: Conceptualization, Resources. Chengxiao Hu: Resources. Xu Wang: Resources. Min Nie: Formal analysis, Investigation, Visualization. Miaomiao Cai: Formal analysis, Investigation, Visualization. Qin Cheng: Formal analysis, Investigation, Visualization. Xiaohu Zhao: Conceptualization, Methodology, Writing - Original Draft, Resources, Writing -
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (41807142, 41571321), the Opening Project of Fujian Universities and Colleges Engineering Research Center of Modern Facility Agriculture (G2-KF2007), the Opening Project of Key Laboratory of Testing and Evaluation for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs (NK202101), the Fundamental Research Funds for the Central Universities (BC2021102, BC2021106).
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