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Article

The Effects of Coexisting Elements (Zn and Ni) on Cd Accumulation and Rhizosphere Bacterial Community in the Soil-Tomato System

by
Yufeng Zhao
1,
Yuhui Wang
2,*,
Guojin Sun
1 and
Lu Feng
2
1
College of Water Conservancy and Environmental Engineering, Zhejiang University of Water Resources and Electric Power, Hangzhou 310018, China
2
State Environmental Protection Engineering Center for Pollution Treatment and Control in Textile Industry, College of Environmental Science and Engineering, Donghua University, Shanghai 201620, China
*
Author to whom correspondence should be addressed.
Processes 2023, 11(5), 1523; https://doi.org/10.3390/pr11051523
Submission received: 29 March 2023 / Revised: 26 April 2023 / Accepted: 15 May 2023 / Published: 16 May 2023
(This article belongs to the Special Issue Processes of Pollution Control and Resource Utilization)
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Abstract

:
The increasing cadmium (Cd) levels in agricultural soils have become a worldwide concern for food crop security. Cd accumulation in the soil-plant system is closely related to other coexisting factors. In this study, the effects of different levels of Zn or Ni on Cd accumulation in tomato plants and on the rhizosphere soil bacterial community structure were analyzed by coupling pot experiments with high-throughput sequencing. The results demonstrated that tomato plants (Lycopersicon esculentum) in Zn-Cd and Ni-Cd co-contaminated soils exhibited lower relative growth rates. Co-contamination at low levels tended to reduce the bioaccumulation of heavy metals in the roots of plants, whereas increased contaminant concentrations produced the opposite effect. In the presence of 200 mg/kg Zn or 20 mg/kg Ni, the biomass of plant roots increased by 4.95–23.16% and the Cd content of the plant roots decreased by 17.36–68.93% due to the antagonistic effects between Cd and Zn/Ni. In addition, the richness and diversity of the bacterial community were significantly altered under HMs co-contamination, and the number of special bacteria was positively correlated with the level of heavy metals in the rhizosphere soil. The relative abundance of Proteobacteria increased and that of Actinobacteria decreased in soils with low levels of heavy metals. This may improve the tolerance of plant roots to heavy metals and reduce the accumulation of Cd in plant roots. These findings highlight the important role of coexisting elements in the inhibition of Cd accumulation in tomatoes and offer important information for the production of safe crops.

1. Introduction

The accumulation of heavy metals (HMs) in soil has become a significant environmental problem with rapid urbanization and industrialization [1]. The latest nationwide survey on the status of soil contamination in China revealed that 16.1% of all samples analyzed exceeded the environmental quality standards [2,3], with HMs being the main pollutants (82.4%). The pollution status of HMs in soils from China between 1977 and 2020 was investigated by Shi et al. [4], with the results indicating that cadmium (Cd) was the most widespread pollutant in agricultural soils. The mean concentration of Cd was 5.73 times higher than the limit for agricultural soils when comparing the metal concentration relative to the standard limit [5]. Importantly, Cd is one of the most toxic and dangerous HMs for living organisms, even at low concentrations [6]. Moreover, increasing Cd pollution seriously affects the yield of crops [7]. Cd can also be transferred from contaminated soil to crops and plants and accumulate in organisms through the food chain, posing severe threats to human health [8]. Tomatoes (Lycopersicon esculentum, L. esculentum), a vital vegetable crop worldwide, provide numerous health benefits to humans [9].
Therefore, a better understanding of the fate of Cd in the soil-tomato system and the influencing factors is critical for protecting food security.
Many studies have examined the mechanisms underlying Cd toxicity and the uptake, translocation, and accumulation of Cd in crops [10,11,12]. The toxicity of Cd inhibits plant growth, disturbs photosynthesis and transpiration, and reduces the synthesis of carbohydrates and nucleic acids [13,14,15]. The uptake and accumulation of Cd in crops are influenced by many factors, including plant type, Cd concentration, soil pH, and organic matter [12]. Moreover, coexisting elements in the soil may significantly influence the uptake and transport of Cd in the crop through antagonistic, additive, and synergistic effects between HMs [16,17]. While zinc (Zn) and nickel (Ni) are essential micronutrients that are required for many structural and biochemical functions in plants, they are toxic at high concentrations [18,19]. Ni in the soil can reduce the absorption of Cd in the roots of maize and rice [20,21]. Moreover, the presence of Zn can significantly reduce Cd accumulation and toxicity in many crops (such as wheat, rice, maize, and leaf vegetables) because Cd and Zn have similar absorption systems and ion competition exists [22,23,24]. However, several studies have demonstrated that the application of Zn or Ni does not inhibit Cd accumulation in some crops [22,25]. Although the influences of coexisting mineral factors on Cd accumulation in different crops have been widely investigated, the existing research on the interactions between HMs in the same crop is conflicting. In addition, there is a scarcity of studies on the interactive effects of Ni combined with Cd treatment on tomato plants.
As an important medium for the exchange of plant and soil resources, the rhizosphere microbiota plays an important role in crop growth [26]. Generally, HM pollution has negative effects on the rhizosphere microbial community [27]. As a toxic element in soil, Cd can affect the microbial distribution, and the diversity of the bacterial community decreases with increasing levels of Cd [28]. High HMs levels can also result in the enrichment of some microbial species that are tolerant to very high concentrations of HMs [29]. For crops, changes in the soil microbial community composition and structure can affect the absorption of Cd and micronutrients (such as Fe, Zn, Mg, and Ca) [30]. Recently, several studies have explored the impact of changes in the structure of rhizosphere microbial communities on the accumulation of heavy metals in plants through inoculation with specific bacterial strains or the application of substances to the soil [24,31,32]. Nonetheless, our understanding of how the whole indigenous soil microbiome affects Cd accumulation in crop plants remains limited, especially when considering the complex interactions between Cd and other HMs in soil-plant systems.
In this study, a pot experiment was conducted, and tomatoes were exposed to different levels of contamination with Cd, Zn, Ni, and various combinations of these HMs. The plant growth and HMs concentrations of the tomato plant tissues were determined at the end of the treatment. Pyrosequencing of the 16S rRNA genes was conducted to detect differences in the bacterial communities of the rhizosphere soil under the different treatments. The aims of this study were to (I) explore the growth characteristics of tomatoes under Cd, Zn, and Ni stress; (II) determine the fates of Cd, Zn, and Ni in soil-tomato systems under single/combined contamination; and (III) investigate the interaction effects between the rhizosphere microbial community structure and the HMs uptake and accumulation processes in tomato plants. It was hypothesized that the coexistence of Cd and other HMs in tomato-soil systems would significantly affect the migration and accumulation of Cd in tomato plants through complex interactions between the plant and the rhizosphere microbial community. These findings can inform the development of strategies for the safe cultivation of tomato crops in areas contaminated with Cd, Zn, and Ni.

2. Materials and Methods

2.1. Material Preparation

Cherry tomatoes (Lycopersicon esculentum var. cerasiforme) are a high Cd-accumulating fruit and typically contain two to three times the recommended Cd concentration for fruits and vegetables [13,33]. In this study, a commonly cultivated type of cherry tomato (Meiwei, a high Cd accumulation cultivar) was selected based on the findings of Xu et al. [34]. The cherry tomato seedlings were obtained from a registered retailer in Songjiang, Shanghai, China. The seedlings were propagated in a half-strength modified Hoagland’s nutrient solution in order to maintain suitable seedling development and were grown in a growth chamber (SGZ1000A, China) under cool white fluorescent lights (450 μmol photons·m−2 s−1) at 25 ± 2 °C with a 12-h light/dark photoperiod. The modified Hoagland nutrient solution was composed of Ca(NO3)2·4H2O2 (0.473 g/L), KNO3 (0.253 g/L), NH4NO3(0.40 g/L), KH2PO4 (0.068 g/L), MgSO4 (0.12 g/L), and microelements. The cultured tomato seedlings with a similar growth status (plant height: 8 ± 2 cm) were randomly assigned to the treatment groups.
The pot experiment was conducted at the Donghua University Songjiang Campus (31°02′52.92″ N, 121°13′37.44″ E). The soil samples were collected from an agricultural field located near Songjiang, Shanghai, at a depth of 0–20 cm. The method of topsoil sampling was as described in the Technical Specification for Soil Environmental Monitoring [35]. The soil samples were transported to the laboratory, air-dried at room temperature, and passed through a 2-mm nylon sieve before use in the experiments. Following the method described by Jiang et al. [36], the pH value of the soil samples was measured at a soil:water ratio of 1:2.5 using a multi-parameter tester (HQ40d, Hach Water Quality Analytical Instruments (Shanghai) Co., Ltd., Shanghai, China). The soil texture was determined by a combination of sieving and sedimentation (ISO 11277). The soil organic matter was determined using wet digestion by the potassium dichromate method. The content of total nitrogen was measured according to the micro-Kjeldahl method, and the total phosphorus content was colorimetrically determined by wet digestion with HF–HClO4. The contents of available nitrogen and phosphorus were measured by the micro-diffusion technique and the Olsen method, respectively. For the total Cd, Zn, and Ni concentrations in the soil, 0.2 g of soil samples were digested with a mixture of nitric acid (HNO3), hydrofluoric acid (HF), and perchloric acid (HClO4) in Teflon crucibles on a hot plate (GDANA-HT10, China). The physicochemical properties of the initial soil samples were as follows: heavy loam; pH, 7.63; 15.90 g·kg−1 organic matter; 16.96 mg·kg−1 available phosphorus (P); 125.67 mg·kg−1 available nitrogen (N); 307.26 mg·kg−1 total P; 660.05 mg·kg−1 total N; total Cd, Zn, and Ni concentrations of 0.10, 2.96, and 0.13 mg·kg−1, respectively.

2.2. Experimental Design

Three experimental treatment groups were examined in this study: 1. the effect of Cd treatment on tomato seedlings; 2. the effect of Cd with Zn co-treatment on tomato seedlings; 3. the effect of Cd with Ni co-treatment on tomato seedlings. In this experiment, CdCl2·2.5H2O solution, ZnSO4·7H2O solution, and Ni(NO4)2·6H2O solution were used as the sources of Cd, Zn, and Ni, respectively. The selection of Cd, Zn, and Ni contamination levels was mainly based on extreme pollution situations that have been reported earlier [37,38,39]. As shown in Table 1, the three experimental treatment groups comprised sub-treatments, as follows: (1) the Cd treatment group included four levels of Cd contamination (0, 1, 20, 50 mg kg−1 soil); (2) the Cd with Zn co-treatment group included four levels of Cd contamination (0, 1, 20, 50 mg kg−1) which were respectively supplemented with 1, 20, 50 mg Zn kg−1 soil; (3) the Cd with Ni co-treatment group included four levels of Cd contamination (0, 1, 20, 50 mg kg−1) which were respectively supplemented with 20, 80, 160 mg Ni kg−1 soil. The treated soils were transferred into plastic pots (16 cm × 14 cm), and all soil samples were cultured at room temperature for 30 days in the dark. In total, the study comprised 28 experimental treatment combinations, which were replicated three times in a completely randomized block design.

2.3. Plant Culture

Each pot contained 0.85 kg of treated soil and one pre-germinated tomato seedling. Plant culture was conducted in a phytotron (SGZ-1000 A, Hangzhou Shuolian Instrument Co., Ltd., Hangzhou, China) at 25–30 °C under a 12-hour light/dark photoperiod with a relative humidity of 80%. During the 65 days of culture, the soil in each treatment was maintained at a water-holding capacity of 65–70% by adding deionized water. The plant growth conditions remained the same, and the plots were rotated weekly to eliminate spatial variability in the growth chamber.

2.4. Determination of Plant Growth

All tomato plants were harvested for analysis at the end of the seedling period and before the fruiting period [38]. At the end of the 65-day treatment, the fresh weight and length of the plants were measured to evaluate the plant growth response. The relative growth rate (RGR, g·d−1) of the different treatments was calculated as follows: RGR = (lnW2—lnW1)/t, where W1 and W2 are the initial fresh weight and final fresh weight (g), respectively, after 65 days of treatment, and t represents the treatment time (days).

2.5. Determination of HM Contents

After 65 days of treatment, the plants were removed from the pots and rinsed in deionized water. After harvesting, they were divided into roots, stems, and leaves for analysis of the HMs concentrations. Before analysis, the harvested plants were washed with distilled water and blotted with tissue paper. The roots, stems, and leaves were dried at 75 °C for 48 h. After drying, the ground plant samples were passed through 149 μm nylon sieves to obtain a uniform particle size. The ground samples of the roots and shoots were analyzed for HMs accumulation by the wet digestion method, as described by Miller [40]. A 1 g plant sample, 10 mL of HNO3, and 5 mL of HClO4 were added to a glass flask, and digestion was performed to obtain the HMs solution. After complete digestion, the resulting solution was transferred to a volumetric flask and diluted to 25 mL. The total Cd, Zn, and Ni concentrations of all samples were determined by an atomic absorption spectrophotometer (TAS-986, USA).

2.6. Microbial Analysis of the Soil Samples

When the plants were harvested, rhizosphere soil samples from the CK, Cd1, Cd3, minimum and maximum Zn-Cd co-contamination treatments, and Ni-Cd co-contamination treatments were also collected for soil bacterial community analysis. The genomic DNA in the rhizosphere soil was extracted using an Invitrogen kit (Thermo Fisher Scientific, USA), according to the manufacturer’s instructions. Polymerase chain reaction (PCR) amplification of the V4-V5 regions of the bacterial 16S rRNA gene was performed with the primers 515F (5′-GTGCCAGCMGCCGCGG-3′) and 907R (5′-CCGTCAATTCMTTTRAG TTT-3′). PCR reactions were performed, and the PCR products were purified, as described in a previous study [41]. Furthermore, all PCR products were sequenced on an Illumina Miseq system (Mayo Biotechnology Co., Ltd., Shanghai, China).

2.7. Data Analysis

Three replicates were performed for each experiment, and the experimental data are expressed as the mean ± SE. The Cd, Zn, and Ni concentrations in the tomato plants were expressed on a plant dry weight basis (mg kg−1 DW). All figures were plotted using Prism. Heat maps were generated by Heml to reflect the differences in the abundance distributions of species between the different groups. All statistical analyses were performed in SPSS. One-way analysis of variance (ANOVA) with Tukey’s test (p < 0.05) was used to evaluate significant differences in the plant growth rate and HMs contents of the plant, with the Cd, Zn, and Ni contamination levels as single factors.

3. Results and Discussion

3.1. Effects of Cd, Zn, and Ni on Plant Growth

After 65 days of treatment, the results revealed that plant growth was significantly affected by the concentrations of Cd, Zn, and Ni. As shown in Figure 1, under the single Cd contamination treatment, the RGR of L. esculentum was negatively correlated with the soil Cd level. Studies have confirmed the negative impact of Cd on the growth of tomato plants [42,43]. As shown in Table S1, the weight of the tomato plant in the 1 mg kg−1 Cd treatment significantly increased by 8.45% compared to the control (13.73 g·plant−1), but in the 20–100 mg kg−1 Cd treatments, the plant weight decreased by 6.26–61.83% compared to the control (13.73 g·plant−1). This may be because metal ions may activate the enzymes involved in cytokinin metabolism, which accelerates plant growth [44]. However, Cd has toxic effects on plant cells when the Cd concentration exceeds a certain level [45]. Similar observations were reported by Valencia-Hernandez et al. [46].
For the Zn-Cd and Ni-Cd co-contamination treatments, the RGR values of the plants were lower than those of the Cd alone treatment. Zn, as an enzyme co-factor, participates in the physiological processes of plants and has an important effect on plant growth [47]. The results indicated that the application of Cd supplemented with Ni or Zn further caused a significant reduction in the fresh weight of the plant (reduction of 23.90–82.18%) as compared to the Cd alone treatment (Table S1). It has been reported that Zn might be the dominant factor underlying reduced plant growth at higher levels of Zn-Cd treatment than at lower levels [48]. Thus, the reduced biomass of the plants treated with Zn or Zn-Cd might be due to the toxic effect of excess Zn and the impact of the excess Zn on the homeostasis of metal ions in tomato plants [23]. Compared with other HMs, Ni has the highest toxicity, mainly due to the low Ni requirement of crops [14]. Further, plant cells might have greater respiration rates under Cd and Ni stress, which significantly affect cell elongation and meristematic activity [49]. The lower biomass of plants exposed to Ni and Zn is also related to the inhibitory effects of Ni and Zn on the activities of enzymes involved in the photosynthetic carbon reduction cycle [50,51]. In summary, the relative growth rate and biomass of tomato plants were reduced with exposure to Zn-Cd and Ni-Cd co-contaminated soil, and these effects are likely attributed to alterations in numerous physiological processes as a result of HM exposure.
In contrast, the application of certain concentrations of Zn (200 mg·kg−1) or Ni (20 mg·kg−1) with 1–20 mg·kg−1 Cd increased the root fresh weight by 77.13% and 50.95%, respectively, in comparison to the Cd treatment alone (Table S1). It has been claimed that Cd has a harmful impact on tomato roots, greatly impairing cell elongation and resulting in cell death [52]. The increase in the root fresh weight might be due to the reduced accumulation of Cd in the plant roots as a result of competition between Cd and Zn/Ni [21,53,54]. However, the high Zn/Ni levels with Cd treatment led to a significant reduction in the fresh weight of the plants (Table S1). It has been reported that higher Zn levels combined with Cd can increase the Cd concentration in plants; meanwhile, higher Zn treatment (300 mg·kg−1) significantly reduced the plant weight and caused oxidative stress in plants [48].

3.2. Accumulation and Transformation of Cd, Zn, and Ni in Tomato Plants

The concentrations of Cd, Zn, and Ni in the shoots and roots of L. esculentum are shown in Figure 2. Overall, the Cd, Zn, and Ni concentrations in the plant increased with increasing HMs contamination of the soil. The average HMs content of the different parts of the plant for all treatments was as follows: root > stem > leaf. The HMs concentration in the shoots of L. esculentum was 2–3 times lower than that in the roots. Previous studies indicated that more than 70% of Cd accumulates in the tomato roots under Cd stress [52,55]. This may serve as a defense mechanism against Cd stress to reduce the toxic effect of Cd on the aboveground parts of the tomato plant.
The impact of co-pollution on the accumulation and migration of HMs in the soil-plant system is related to the degree of pollution. Compared with the single Cd treatment, the 200 mg kg−1 Zn with Cd treatment resulted in a decrease in Cd accumulation in the roots (17.36–22.12%). There is no special transport protein for Cd in plants; Cd enters the roots of the plant through essential element transport proteins [56]. Cd and Zn have similar chemical properties and absorption transporters (such as OsIRT1, OsHMA2, and OsZIP7), and this may be the reason for the antagonistic effect between Cd and Zn [57,58]. Cd might be extruded from the roots by Zn application due to the specific up-regulation of Cd-transporting ATPase; this could contribute to the lower Cd accumulation in the roots under the Cd + Zn treatment compared to the Cd only treatment. Additionally, Zn supplementation could activate metallothionein expression and increase the content of phenolic compounds in the roots, which could chelate HMs or remove free radicals, attenuating oxidative damage under Cd stress [59,60]. However, higher concentrations of Zn can not only aggravate the toxic effects of Cd on plants but can also facilitate the translocation of Cd [61,62]. Therefore, high supplementation of Zn in the Cd treatment resulted in a slight increase in Cd accumulation in the roots and shoots as compared with the single Cd treatment.
The effects of Zn-Cd co-contamination on the Zn content of plants are shown in Figure 3. The combination of Cd+Zn produced a 5.97–37.74% reduction in Zn accumulation in the roots and a 36.80–123.07% increase in Zn accumulation in the shoots, as compared to the Zn only treatment. Moreover, the Zn contents of the roots and shoots significantly decreased with increasing Cd supply. Increased Cd accumulation in the plant is likely to negatively affect Zn accumulation because Cd and Zn compete for the same transporter and binding compounds. This is in accordance with the results observed in Cd-hyperaccumulators (Cosmos bipinnatus and Catharanthus roseus) [61,63] and other crops (wheat, rice, and maize) [22,23,64]. In addition, under excessive Cd and Zn stress, more Zn is transported to the shoots and more Cd is trapped in the roots due to the important role of Zn in enzyme reactions and gene expression to maintain shoot growth and photosynthesis.
Unlike the Zn-Cd treatment, the Cd and Ni co-contamination treatment successively decreased the Cd concentration in the roots of L. esculentum by 15.74–56.08% compared with the individual Cd treatment (Figure 2b). For the Ni-Cd treatments, increasing the Ni contamination level from 0 to 20 mg/kg increased the total Cd accumulation in plant shoots from 0.28 to 12.42 mg/kg dry weight of plant, while further increases in the contamination level to 160 mg/kg did not cause further increases in Cd accumulation. Under the same concentrations of Cd and Ni in the culture medium, the Cd absorption capacity of the plant is more than twice that of Ni due to the different binding affinities of metal transporters in plants [65]. This may be the reason for the high accumulation of Cd in the plant shoots under the combined contamination of low-concentration (20 mg kg−1) Ni and 20 mg kg−1 Cd.
In the current study, the Ni content of the roots of L. esculentum was dependent on the Ni level. Compared to the Ni-only treatment, the Ni-Cd treatment at lower levels decreased the Ni concentration of the tomato roots by 20.39–31.14% and the Ni concentration of the tomato shoots by 28.96–39.68% (Figure 4). These results suggest that the interaction pattern between Cd and Ni in tomato plants is antagonistic. As shown in Figure 2, Ni contamination at higher levels inhibited Cd enrichment in the plant roots and reduced Cd transport to the shoots. Previous research has revealed that the concentration of Cd in the roots of rice decreases with increasing Ni addition, and Cd is mainly distributed in the root cell walls and soluble fractions [21]. The polysaccharides and proteins contained in the plant cell wall can provide polar substances such as hydroxyl or carboxyl groups that bind to HM ions, thereby inhibiting the further transport of HM ions. This is consistent with the results of Zhang et al. [21], but contrary to the results of Khaliq et al. [66], where the addition of Cd enhanced the uptake of Ni by the roots.
In general, Cd-Zn and Cd-Ni co-contamination at low levels tended to reduce the bioaccumulation of HMs in the roots of tomato plants. However, according to the maximum allowable value specified in the Chinese food standard [67], the Cd contents in the aboveground parts of the plant greatly exceeded the threshold for cereal food security (0.05 mg/kg for Cd), at least for the present growth stage. This indicates that these levels of contamination will pose serious threats to human health if humans consume foods derived from crops grown in these Cd-contaminated soils. Therefore, proactive measures are still needed to prevent human exposure to crops grown on Cd-contaminated agricultural soils in the future.

3.3. Effects of Cd, Zn, and Ni on the Community Diversity of the Soil Microorganisms

The microbial richness and diversity of the rhizosphere soil under the different HM treatments are shown in Table 2. The Chao, Ace, and Shannon indices in the soils contaminated with Cd alone were much smaller than those of the uncontaminated soil, indicating that community diversity in these contaminated soils decreased. As some microorganisms are highly sensitive to HM toxicity, they will become extinct after exposure to high concentrations of HM [68]. However, compared to the single Cd treatment (Cd1 and Cd3), the Zn-Cd and Ni-Cd co-treatments increased the diversity and richness of the soil bacterial community. The findings revealed that certain concentrations of Zn or Ni tended to enhance the microbial diversity of the rhizosphere soil in the co-contamination treatments.

3.4. Effects of Cd, Zn, and Ni on the Community Structure of the Soil Microorganisms

3.4.1. Microbial Community at the Phylum Level

Figure 5 below shows the bacterial community composition at the phylum level. In all soil samples, Proteobacteria (27.9–52.0%) was the most dominant phylum, followed by Actinobacteria (6.6–21.1%), Bacteroidetes (4.2–26.9%), Acidobacteria (4.6–18.6%), and Chloroflexi (3.6–12.5%). Among these, Proteobacteria are ubiquitous in the rhizosphere environments of different plant species; they have good tolerance to HM contamination [69,70,71]. Wang et al. also found that Proteobacteria, Bacteroidetes, Acidobacteria, and Actinobacteria are the most dominant phyla in Cd-contaminated wheat rhizosphere soil [72].
Microorganisms will accumulate richness by interacting with HMs; this leads to the evolution of some HM-tolerant groups that are more adapted to the current environment. As shown in Figure 5a, the relative abundance of Proteobacteria decreased with increasing Cd concentration. Proteobacteria play an important role in soil C and N cycling, and their relative abundance is positively correlated with several C and N cycling enzyme activities [73]. Thus, the current results indicate that high Cd levels may influence soil nutrient cycling, thus inhibiting the root growth of L. esculentum. Compared with the soil contaminated with Cd alone, the relative abundance of Proteobacteria in the Zn-Cd and Ni-Cd co-contaminated soils increased with increasing Cd levels. High concentrations of HMs and toxic substances serve as a source of energy and nutrition for Proteobacteria [74]. Thus, an increase in the relative abundance of Proteobacteria in contaminated soil might be helpful in maintaining a stable nutritional level for the growth of L. esculentum and may improve the ability of L. esculentum to resist Cd toxicity [75].
In addition, the phyla Actinobacteria, Bacteroidetes, and Acidobacteria were more enriched in the Cd-treated rhizosphere soil in comparison to the uncontaminated soil. Acidobacteria and Bacteroidetes are reported to resist HM toxicity due to their complexation and adsorption capacities [76]. However, the relative abundances of these microorganisms (Actinobacteria, Bacteroidetes, and Acidobacteria) were significantly lower in the Zn-Cd and Ni-Cd co-polluted soils than in the soils polluted with the same concentrations of Cd. Moreover, Actinobacteria were positively associated with the available Cd in the contaminated soils [77], indicating that the significant reduction in Cd accumulation in the roots in the presence of Zn or Ni might be related to a decrease in the available Cd concentration in the rhizosphere soil.
In principal component analysis (PCA), a shorter distance between the microbial samples represents higher structural similarity. The current PCA revealed that the bacterial communities in the different soils were clustered according to their HMs concentrations. As shown in Figure 5b, the samples with severe HMs concentrations were closely packed on the negative axis of PC2, while the samples with lower HMs concentrations were clustered together on the positive axis of PC2. Meanwhile, the bacterial communities of the Cd1, Ni1Cd1, and Zn1Cd1 treatments exhibited similar structures. Together, these findings demonstrate that the microbial community compositions of the rhizosphere soil were significantly influenced by the different concentrations of Cd contamination, with greater effects in the case of a high concentration of Cd combined with other HM pollution.

3.4.2. Microbial Community at the Genus Level

The heat map in Figure 6 highlights the top 30 genera that accounted for the most sequences. The right side of the figure shows the meaning of the color gradient. The higher the abundance, the more red the color, and the lower the abundance, the more blue the color [77,78]. The rhizosphere of the Cd-contaminated soil exhibited higher abundances of unclassified_Acidobacteria and unclassified_Cytophagaceae as compared to the uncontaminated soil. Unclassified_Acidobacteria and unclassified_Cytophagaceae are affiliated with the phyla Acidobacteria and Bacteroidetes, respectively. Acidobacteria and Bacteroidetes are more tolerant of HMs contamination [79], and when the Cd concentration is high, Bacteroides can promote the transformation of nutrients. On the contrary, the depletion of Acidobacteria and Bacteroidetes in the rhizosphere soil of the Zn-Cd and Ni-Cd co-pollution treatments might be an indirect effect due to increases in the relative abundances of other microbial taxa [80]. The highest abundance of Sphingomonas, which belongs to Alphaproteobacteria at the class level and Proteobacteria at the phylum level, was observed in the uncontaminated rhizosphere soil (8.43%). Sphingomonas can promote the growth of host plants by stimulating the root secretion of plant auxins and cytokinins [81,82] and immobilizing HMs [83]. The current results indicate that single and combined HMs pollution of soils may have a negative influence on the enrichment of the Sphingomonas genera, thus inhibiting the root growth of the plant.
Additionally, the relative abundances of Pseudomonas (belonging to the Proteobacteria phylum) and Leptolyngbya (belonging to the Cyanobacteria phylum) in the Ni1Cd1, Ni3Cd3, Zn1Cd1, and Zn3Cd3 treatments were higher than those in the Cd1 and Cd3 treatments. The abundance of the bacterial genus Pseudomonas was inhibited in soil treated with Cd [84], whereas it was enriched in the Zn-Cd and Ni-Cd co-polluted rhizosphere soil, and this could affect plant growth and HMs absorption. A previous study found that Pseudomonas, a well-known plant growth-promoting bacteria (PGPR), reduced metal-induced stress in plants [70,82], and thus, the enrichment of some special species of Pseudomonas (such as Pseudomonas sp. TCd-1) might form a natural barrier to decrease Cd uptake by plants [85]. Thus, it can be assumed that the changes in the relative abundances of Proteobacteria and Actinobacteria at the phylum level and Pseudomonas at the genus level in HMs-co-polluted soil may enhance the Cd tolerance of plants and reduce the Cd accumulation in plants.

4. Conclusions

The absorption and transport behaviors of Cd in a soil-tomato system under different pollution conditions were studied in a pot experiment. The results demonstrated that exposure to multiple contamination (Zn-Cd and Ni-Cd) stresses significantly alters the microbial diversity of the rhizosphere soils, which indirectly affects the absorption and accumulation processes of Cd in the roots of tomato plants. Furthermore, several bacterial groups are stimulated by Cd-Zn or Cd-Ni co-stress, likely contributing to the tolerance and bioaccumulation behavior of Cd in plants. These findings improve our empirical and theoretical understanding of the interaction effects between Cd, Zn, and Ni in soil-crop systems. Although the accumulation of pollutants in the growth stage of the tomato plant was preliminarily discussed in this study, the effects in other stages of the plant cycle require further investigation. In future studies, the uptake and accumulation of Cd in the tomato fructification stage should be investigated in order to evaluate the risk of Cd exposure in the food chain.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/pr11051523/s1, Table S1: The growth attributes of L. esculentum plants after treatment with single element (Cd, Zn, or Ni) or co-contaminated conditions for 65d. Data are shown as mean ± SD, n = 3.

Author Contributions

Conceptualization, Y.W.; methodology, Y.W.; software, L.F.; validation, Y.Z., and L.F.; formal analysis, Y.Z.; investigation, L.F.; resources, L.F.; data curation, Y.W.; writing—original draft preparation, Y.Z.; writing—review and editing, Y.W.; supervision, G.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Scientific Research Foundation of Zhejiang University of Water Resources and Electric Power (grant number X20220028) and the Key Technology Research and Development Program of Zhejiang (grant number 2021C03196).

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Acknowledgments

The authors appreciate the support of Scientific Research Foundation of Zhejiang University of Water Resources and Electric Power and the Key Technology Research and Development Program of Zhejiang.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. RGR of plants after 65 days of growth under single (a), Zn-Cd co-contamination conditions (b), and Ni-Cd co-contamination conditions (c). The error bars represent the mean ± S.E. (n = 3). The different letters within the different treatments indicate the significant difference at the p < 0.05.
Figure 1. RGR of plants after 65 days of growth under single (a), Zn-Cd co-contamination conditions (b), and Ni-Cd co-contamination conditions (c). The error bars represent the mean ± S.E. (n = 3). The different letters within the different treatments indicate the significant difference at the p < 0.05.
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Figure 2. Concentrations of Cd in the shoots (a,b) and roots (c,d) of L. esculentum under single or co-contamination conditions. The error bars represent the mean ± S.E. (n = 3). The different letters within the different treatments indicate the significant difference at the p < 0.05.
Figure 2. Concentrations of Cd in the shoots (a,b) and roots (c,d) of L. esculentum under single or co-contamination conditions. The error bars represent the mean ± S.E. (n = 3). The different letters within the different treatments indicate the significant difference at the p < 0.05.
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Figure 3. Concentrations of Zn in the shoots (a) and roots (b) of L. esculentum under single or co-contamination conditions. The error bars represent the mean ± S.E. (n = 3).
Figure 3. Concentrations of Zn in the shoots (a) and roots (b) of L. esculentum under single or co-contamination conditions. The error bars represent the mean ± S.E. (n = 3).
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Figure 4. Concentrations of Ni in the shoots (a) and roots (b) of L. esculentum under single or co-contamination conditions. The error bars represent the mean ± S.E. (n = 3).
Figure 4. Concentrations of Ni in the shoots (a) and roots (b) of L. esculentum under single or co-contamination conditions. The error bars represent the mean ± S.E. (n = 3).
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Figure 5. (a) The compositions (b) and principal components analysis (PCA) of the bacterial communities at the phylum level of different soils contaminated with heavy metals. Note: Only phyla with a relative abundance higher than 1.0% are shown in (a).
Figure 5. (a) The compositions (b) and principal components analysis (PCA) of the bacterial communities at the phylum level of different soils contaminated with heavy metals. Note: Only phyla with a relative abundance higher than 1.0% are shown in (a).
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Figure 6. A genus-level heat map of different soils treated with HMs.
Figure 6. A genus-level heat map of different soils treated with HMs.
Processes 11 01523 g006
Table
Table 1. Concentrations (mg·kg−1 DW soil) of heavy metals added to the soil.
Table 1. Concentrations (mg·kg−1 DW soil) of heavy metals added to the soil.
Treatment GroupsCd ConcentrationZn ConcentrationNi ConcentrationNomenclature
Cd single treatment000Cd0(CK)
100Cd1
2000Cd2
5000Cd3
Cd combined with Zn treatments02000Zn1Cd0
12000Zn1Cd1
202000Zn1Cd2
50200–Zn1Cd3
05000Zn2Cd0
15000Zn2Cd1
20500–Zn2Cd2
50500–Zn2Cd3
010000Zn3Cd0
110000Zn3Cd1
2010000Zn3Cd2
5010000Zn3Cd3
Cd combined with Ni treatments0020Ni1Cd0
1020Ni1Cd1
20020Ni1Cd2
50020Ni1Cd3
0080Ni2Cd0
1080Ni2Cd1
20080Ni2Cd2
50080Ni2Cd3
00160Ni3Cd0
10160Ni3Cd1
200160Ni3Cd2
500160Ni3Cd3
Table
Table 2. Microbial diversity indices in the soil under different heavy metal treatments.
Table 2. Microbial diversity indices in the soil under different heavy metal treatments.
SystemShannonSimpsonAceChaoCoverage
CK6.9916450.0044944196.9074198.9660.982454
Cd16.0724210.0068592857.1502846.4190.984998
Cd35.8233610.0208383063.7353014.9420.984634
Zn1Cd16.0708200.0079312932.6632938.1720.985992
Zn3Cd36.7575060.0045574106.0774030.0480.985002
Ni1Cd15.7064930.0114932876.452862.2770.986712
Ni3Cd36.0661910.0125573875.3973810.7850.979581
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Zhao, Y.; Wang, Y.; Sun, G.; Feng, L. The Effects of Coexisting Elements (Zn and Ni) on Cd Accumulation and Rhizosphere Bacterial Community in the Soil-Tomato System. Processes 2023, 11, 1523. https://doi.org/10.3390/pr11051523

AMA Style

Zhao Y, Wang Y, Sun G, Feng L. The Effects of Coexisting Elements (Zn and Ni) on Cd Accumulation and Rhizosphere Bacterial Community in the Soil-Tomato System. Processes. 2023; 11(5):1523. https://doi.org/10.3390/pr11051523

Chicago/Turabian Style

Zhao, Yufeng, Yuhui Wang, Guojin Sun, and Lu Feng. 2023. "The Effects of Coexisting Elements (Zn and Ni) on Cd Accumulation and Rhizosphere Bacterial Community in the Soil-Tomato System" Processes 11, no. 5: 1523. https://doi.org/10.3390/pr11051523

APA Style

Zhao, Y., Wang, Y., Sun, G., & Feng, L. (2023). The Effects of Coexisting Elements (Zn and Ni) on Cd Accumulation and Rhizosphere Bacterial Community in the Soil-Tomato System. Processes, 11(5), 1523. https://doi.org/10.3390/pr11051523

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