Divergent Responses of Earthworms (Eisenia Foetida) in Sandy Loam and Clay Soils to Cerium Dioxide Nanoparticles

doi:10.21203/rs.3.rs-1421593/v1

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Divergent Responses of Earthworms (Eisenia Foetida) in Sandy Loam and Clay Soils to Cerium Dioxide Nanoparticles

https://doi.org/10.21203/rs.3.rs-1421593/v1

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The reported biological effects of cerium dioxide nanoparticles (nCeO₂) in soils range from toxic to protective. However, divergences of nCeO₂ toxicity in soils of different textures are not known. In this study, the availability of nCeO₂ on earthworms (Eisenia foetida) in sandy loam soils and clay soils were discussed, and the biological effects of nCeO₂ (0-1000 mg/kg) on earthworms in two soils were investigated. The results showed the bioaccumulation and biological effects of Ce on earthworms in the two soils were inconsistent. The BCR sequential extraction revealed that the major portions of Ce in both soils were in the residual form (98%-99%), and the acid-soluble Ce fraction were greater in clay soils. However, compared with clay soils, nCeO₂ was more toxic to earthworms in sandy loam soils as assesses by earthworm biomass, morphology, and antioxidative damage. Thus, the high ecological risk of nCeO₂ in sandy loam soils with higher pH and lower clay contents needs to be avoided, being used in agriculture to improve both crop yield and quality.

nCeO2

soil texture

earthworm

ecological effect

bioavailability

Cerium dioxide nanoparticles (nCeO₂) have been extensively used in industrial and biomedical production, chemical mechanical polishing and environmental remediation because of their high oxygen-storage capabilities (You et al. 2021). Presently, nCeO₂ is used in fertilizer formulations to boost crop production and reduce environmental pollutants by controlling the release of beneficial components, which can reach an annual output of 1,000 tons (Deng et al. 2017, Mary Isabella Sonali et al. 2021). Thus, considerable amounts of nCeO₂ are being released into soil ecosystems, posing potential ecological risks to microorganisms and ecosystems (Wei et al. 2020). The toxicity of nCeO₂ to soil invertebrates, bacteria, and plants has been investigated previously, but the results have been contradictory, ranging from toxic to bioprotective (Carbone et al. 2016, Li et al. 2018, Tourinho et al. 2015). The complexity of soil properties (such as pH, CEC, organic matter, and clay content) leads to significant differences in the toxicity of nanomaterials. Consequently, the influence of divergent soil conditions on the behaviors and toxicity of nCeO₂ need to be considered.

The biological toxicity of nCeO₂ mainly comes from the nanoparticles themselves or the released Ce ions (Wang et al. 2016). Superoxide formation induced by an extremely high nCeO₂ level and its interference in redox-dependent biological processes have direct detrimental impacts on soil organisms owing to oxidative damage or indirect detrimental impacts by altering the nutritional values (Amde et al. 2017, Karakoti et al. 2010, Yu et al. 2016). Additionally, metal ions may lead to higher toxicity levels across biological systems than the nanoparticles themselves (Khushi et al. 2018). As a lanthanide element, Ce plays a regenerative catalytic role in the transformation between Ce (III) and Ce (IV) states (Mary Isabella Sonali et al. 2021), which spontaneously completes the redox conversion, which reduce cellular damage to tissues induced by reactive oxygen species (ROS) (Maity et al. 2018, You et al. 2021). Therefore, the impacts of nCeO₂ toxicity on soil organisms are controversial. In soil, nCeO₂ may result in generational changes in plant growth and grain quality, and it has a detrimental effect on the regulation of the antioxidative defense systems (Rico et al. 2020, Tassi et al. 2017). However, the cell senescence caused by ROS may be delayed by the antioxidative action of nCeO₂ and its ability to regenerate and cycle between the Ce (III) and Ce (IV) oxidative states (Karakoti et al. 2010). Thus, contradictory reports on the biological toxicity of nCeO₂ exist. However, very little information is available on what causes the different impacts of nCeO₂ on soil organisms under stress conditions. Earthworms (Eisenia fetida), as a bio-indicator organism having strong interactions with soil, can be assessed to help determine the toxicity of different nCeO₂ concentrations. The nCeO₂-induced accumulations of ROS and oxidative damage, shorten the earthworm life span (Ayub et al. 2019). However, the obvious growth and stress responses do not fully explain the internal metabolic adjustments earthworms undergo to adapt to stress conditions.

The nature of the soil (including organic matter, CEC, pH, nutrient elements, and redox process) affects the bioavailability and biotoxicity of nanoparticles by altering ion release and nanoparticle agglomeration (Fischer et al. 2021). Exposure to TiO₂-NP differentially affects the activity and abundance levels of the microbial community in silty-clay soils and sandy soils, and the changes in plant germination and growth caused by ZnO-NP depend largely on the soil characteristics (García-Gómez et al. 2018, Simonin et al. 2015). Thus, it is difficult to deduce the biological effects of nCeO₂ from one soil to the next owing to the great heterogeneity in soil composition, structure, and characteristics (Simonin et al. 2015). Additionally, most ecotoxicological studies on nCeO₂ toxicity have been based on a single soil as the environmental medium, which may result in significantly different toxicity effects being observed (García-Gómez et al. 2018). At present, there is limited research regarding divergent responses of the toxicity of nCeO₂ in different soil conditions

To fill these knowledge gaps, two natural soils, sandy loam and clay, with different physicochemical properties, were selected to help investigate the biological effects on earthworms in response to nCeO₂.The objectives of this research were to (1) measure the bioavailability of nCeO₂ on earthworms; (2) analyze the divergent biological effects of nCeO₂ on earthworms in two soils; and (3) evaluate the ecological risks of nCeO₂ in different soils. Having a better understanding of the effects of nCeO₂ on earthworms, and the underlying mechanisms, will provide more information on nCeO₂’s environmental ecotoxicological effects on soil ecosystems.

2.1 Materials

Cerium oxide nanoparticles (particle size < 25 nm, purity > 97%) were purchased from Sigma Chemical Co., Ltd. (Shanghai, China).

Earthworms used are belong to Eisenia fetida bought from a commercial market (Nanjing, China). Before the exposure assay, earthworms were cultured in un-added soil and fed with cow manure for 14 days in the laboratory for adaptation. Then, healthy earthworms were selected to be exposed.

2.2 Soils exposure experiment

Sandy loam soils and clay soils were obtained from Yangzhou, Jiangsu (119°42E, 32°35N) and Yingtan, Jiangxi (117°04E, 28°15N), respectively. The soils were collected from 0 to 20 cm deep, air-dried, homogenized, and passed through a 2 mm sieve. The pH value of soils was measured with a pH meter (Inesa Inc., Shanghai, China). Particle size analysis of soils was identified by hydrometer method (Beverwijk 1967). Soil organic matter was determined by potassium dichromate volumetric method (Gowda et al. 2021). And their properties are displayed in Table 1.

Table.1 Basic properties of soils

Items	pH	OM^a	Particle size distribution %			Ce^e
Items	pH	OM^a	Clay^b	Silt^c	Sand^d	Ce^e
Sandy loam soil	7.4	18.4	13.7	28.5	57.8	63.3
Clay soil	4.6	9.1	51.5	28.9	19. 6	54.2
^a OM = Organic matter (g/kg); ^b Clay = (< 0.002 nm); ^c Silt = (0.002–0.02 nm); ^d Sand = (0.02–2 nm);
^e Ce = total Ce content (mg/kg)

Three replicate exposure glass beakers of 200 g soil were prepared for each treatment. Specified amounts of nCeO₂ as powder were thoroughly mixed into dry soil to get the target concentrations of 0, 10, 50,100, 500, and 1000 mg/kg. Each treatment was mixed thoroughly and appropriate amounts of distilled water were added to maintain soil humidity at 60% water holding capacity. Ten earthworms were placed in each beaker, and all earthworms were kept at a controlled temperature of 20 ℃ and in a 12–12 light-dark cycle. After 14 days’ exposure, they were counted and transferred to wetted filter paper to purge gut contents for 24 h.

2.3 Determination of Ce concentration in earthworms and soils

The Ce distribution of soil samples was extracted by BCR (the European Community Bureau of Reference) sequential extraction procedure (Rauret et al. 1999). Earthworm samples were microwave digested (CEM MARS6, USA) in a mixture of HNO₃ and H₂O₂ (v/v, 5:2 ) at 180°C for 30 min (Zhu et al. 2020). The concentration of Ce was measured by inductively coupled plasma massspectro - metry (ICP-MS).

2.4 Transmission electron microscopy (TEM) observation

The earthworm samples were fixed in 2.5% glutaraldehyde for 24 h, stained with osmium tetroxide, dehydrated, embedded, and ultrathin sectioned (Xia et al. 2008). The earthworm samples were observed by TEM (HITACHI 7650, Japan)

2.5. Determination of ROS, MDA, and PCO

The samples of earthworm were cut into small pieces, which were then quickly rinsed with ice-cold physiological salt water. About 0.3 g of tissue was weighed and homogenized quickly on ice for 1 min after the addition of 2.0 ml of 10.0 mM Tris buffer (pH 7.5) for assessment of biomarkers. The extracts were centrifuged at 12000 rpm for 20 min at 4℃. Supernatant of the homogenized tissue was preserved at -40℃ for analysis within 5 days.

Reactive oxygen species (ROS) was captured by Polybutylene naphthalate. About 0.1 g of tissue was weighed and added to 1.0 mL 50 mM Ntert-Butyl-α-phenylnitrone (PBN). Supernatant of the homogenized tissue was stocked in liquid nitrogen immediately for electron paramagnetic resonance (EPR) measurement(Shi et al. 2005).

Malondialdehyde (MDA) content of earthworms was determined by thenthiobarbituric acid colorimetry method (Ohkawa et al. 1979) and measured by using diagnostic reagent kits (Nanjing Jiancheng Bioengineering Institute, China). Protein carbonylation (PCO) content was measured by 2,4-Dinitrophenylhydrazine (DNPH) colorimetry under UV spectrophotometer at 370 nm (Chiaradia et al. 2019).

2.6 Determination of CAT activity, GSH/GSSG ratio, and MT content

Total protein in the enzyme extracts was estimated based on the Bradford method (Hong et al. 2014). The reduced glutathione/oxidized glutathione (GSH/GSSG) ratio and GSH and GSSG contents were measured by the 5,5’-dithiobs-(2-nitro-benzoic)-acid (DTNB) circular reaction which used DTNB as a substrate to measure the absorbance change at 430 nm (Hissin &Hilf 1976). The method of determining metallothionein (MT) content in earthworms was based on Onosaka and Cherian (Onosaka &Cherian 1981). Catalase (CAT) activity was determined by UV spectrophotometer at 240 nm, and the H₂O₂ absorbance was measured every 10 s within 0-100 s (Tang et al. 2020).

2.7 Statistical analysis

Data were expressed as means ± standard deviation (SD) and analyzed by analysis of variance (ANOVA). Significant differences were defined to exist between two groups when p was less than or equal to 0.05.

3.1 Biomass and Ce content of earthworms

Figure 1 shows the biomass and Ce content of earthworms exposed to different nCeO₂ concentrations. The initial Ce concentration of earthworm in clay soils was higher than in sandy loam soils. In sandy loam soils, the Ce content in earthworms was not significantly changed by the addition of low nCeO₂ concentrations (10–100 mg/kg), except 500–1000 mg/kg nCeO₂ treatments, in which the Ce content significantly increased compared with the control. In contrast, in clay soils, the Ce contents in earthworms ranged from 1.4 to 2.7 mg/kg, increasing along with nCeO₂ concentration (0–50 mg/kg), after which the content was stable at 2.3 to 2.4 mg/kg, independent of the added nCeO₂ concentration (100–1000 mg/kg). Moreover, nCeO₂ had no adverse effects on earthworm survival within the range of the tested concentrations in clay soil, whereas in sandy loam soils, significant reductions in earthworm biomass occurred, compared with the control group, after exposure to nCeO₂ treatments. In particular, the Ce contents of earthworms in clay soils treated with 50 mg/kg nCeO₂ reached as high as 2.7 mg/kg, an increase of 91.7% compared with the control (1.4 mg/kg), but there was no significant effect on the earthworm biomass. Thus, the bioaccumulation and toxicity effects of nCeO₂ on the earthworms in the two soils were inconsistent.

There are two main metal bioaccumulation pathways in earthworms: (1) the ionic form of the soluble metal passes into the tissue by dermal uptake though the process of diffusion and then accumulates in the circular and longitudinal muscles of earthworms; or (2) the metal particles entrapped in soil and pore water are consumed by earthworms and then undergo degradation and absorption under the actions of intestinal enzymes. The unused part finally being excreted in the form of earthworm feces (Li et al. 2019, Yuvaraj et al. 2021). Thus, the uptake of nCeO₂ by earthworm is different from that of plants, in which nanoparticles enter through cell walls and root epidermal cell membranes (Tripathi et al. 2017). For plants, soil bioavailability metals are mainly in the ionic state, the complex dissolved organic matter state, and the acid-soluble fraction (Lewis et al. 2021). Yet, the Ce accumulated in earthworms includes not only easily available fraction, but also the residual fraction, owing to the ways earthworms ingested metals. It can be inferred from the BCR sequential extraction analysis (Fig. 5). Meanwhile, residual fraction is the main Ce form in clay soil, and its toxicity is much less than that of non-residual fraction (A et al. 2016). So, even if the Ce content in earthworms in clay soil was higher, the biomass of earthworm would not be significantly affected.

3.2 Ultrastructural characterization of earthworm intestines

The intestinal mucosal epithelial cells of earthworms were observed as a columnar epithelial monolayer using TEM (Fig. 2A&C). The cell surfaces were densely covered with short microvilli, and the cell structures include a small number of lysosomes and a high electronic density. The cell structures of earthworms treated with nCeO₂ were fuzzy and appeared to contain cavities. The organelle structures were decomposed, autolyzed, and diffuse (Fig. 2B&D). Earthworms accumulate pollutants through passive epidermal absorption and active intestinal absorption, which could cause morphological damage to the coelom tissues and intestinal epithelia in the earthworms (Tang et al. 2020). The intestinal mucosal epithelial cells of earthworms were morphologically damaged, indicating that nCeO₂ caused toxic reactions in the earthworm at the tissue or organ level (Kwak &An 2021).

3.3 Oxidative stress responses of earthworms

The ROS produced by mitochondria can transmit information and maintain organ functions, and the production and elimination of ROS in the body are in a balanced state under normal conditions (Roy et al. 2020). When stimulated by external pollutants, cells produce excessive oxygen anions and hydrogen peroxide, potentially causing mitochondrial damage, that could interrupt protein synthesis and transport, inhibit cell proliferation, and induce apoptosis (Li et al. 2003). The percentages of free-radical change in earthworms exposed to nCeO₂ are shown in Fig. 3. On the whole, in sandy loam soils, the free-radical changes in earthworms were evidently greater than in clay soils. The ROS contents of the exposed groups in sandy loam soils, compared with the control, significantly increased by 17.6% − 46.5%. However, in clay soils, the free-radical levels in the nCeO₂ treatment groups were not much different from that of the control, except for 100 mg/kg nCeO₂ group, which increased by 27.3%.

To minimize the degree of oxidative damage, CAT is induced by cells to catalyze peroxides into harmless O₂ and H₂O (Zhu et al. 2020). Excessive ROS likely caused oxidative stress, which resulted in the continuous increase in the CAT activity of earthworms exposed to nCeO₂ in sandy loam soils (Fig. 3b). However, in clay soils, the CAT activity was obviously reduced.

When generated free radicals cannot be completely neutralized by the antioxidative enzyme system, they eventually cause oxidative damage that decreases proteins solubility and causes lipid peroxidization in the organism (Zhang et al. 2021). Protein carbonylation (PCO) is the most frequent form of protein oxidation, and it is stable and irreversible (Márquez-Lázaro et al. 2021). Malondialdehyde (MDA) is the most abundant reactive carbonyl compound generated through the degradation of unstable lipid hydroperoxide (Maity et al. 2018). Thus, PCO and MDA indirectly reflect the influence of free radicals on proteins and lipids, respectively. As shown in Fig. 3c, in clay soils, the MDA contents of the exposed groups significantly decreased compared with the control. However, in sandy loam soils, the MDA content of exposed groups increased by a certain amount compared with the control. In particular, the MDA content after exposure at 10 mg/kg nCeO₂ reached 12.8 nmol/ (g Pr). The fluctuations in the PCO contents were similar to those of the MDA contents (Fig. 3d). Compared with the control, the PCO contents of the exposed groups in clay soils significantly decreased to between 3.2 and 4.1 nmol/ (mg Pr), whereas, in sandy loam soils, it increased by a certain amount. These results demonstrated that, in sandy loam soils, excessive ROS caused oxidative stress, which induced CAT activity in earthworms exposed to nCeO₂, and finally led to an increase in their PCO and MDA contents to varying degrees. However, the CAT activities, MDA contents and PCO contents of the exposed groups in the clay soils significantly decreased compared with the control. Thus, the toxicity effects of nCeO₂ on earthworms were different in the two soils.

3.4 The MT contents and GSH/GSSG ratio of earthworms

The MT concentrations in earthworms from the two soils are shown in Fig. 4a. MT is a metal-binding peptide with a molecular weight of 6–7 kDa that can chelate various metals ions, such as Zn²⁺, Cu²⁺, Cd²⁺, and Cr³⁺, through mercaptide linkages and transport the bound metals to chloragogenous tissues to complete the detoxification process (Blindauer &Leszczyszyn 2010, Homa et al. 2016, Hussain et al. 2021). The Ce ions that accumulate in the circular and longitudinal muscles of earthworms cause stress, which can trigger MT synthesis to reduce damage to the epidermal and midgut cells (A et al. 2020).

The Ce bioaccumulation in earthworms in the two soils increased under nCeO₂ treatments (Fig. 1b), but the MT contents in earthworms did not increase significantly. Even in earthworms in clay soils exposed to the 50 mg/kg nCeO₂ treatment (Ce content, 2.7 mg/kg), the MT content did not significantly increase. This indicated that the concentration of Ce ions in the earthworms in the two soils did not increase and, in clay soils, the Ce bound form may exist in earthworm body with high Ce content. Nanoparticles can penetrate directly into the tissue when the external cuticle layer of organism is eroded or damaged and may also be attached to the inner wall of intestinal lumen (Unrine et al. 2010). Therefore, we speculated that the bioaccumulation and biological effects of nCeO₂ on earthworms are related not only to the Ce ion accumulation in the body but also to the unused Ce bound form. Moreover, in addition to the high available acid-soluble, reducible, and oxidizable fraction, the residual fraction can be consumed by earthworms. Therefore, the traditional BCR analysis method, being used to determine the bioavailability of heavy metals for plants, which is not suitable for analyzing the bioaccumulation of nanoparticles in earthworms.

Glutathione (GSH) can further combine with free radicals or heavy metals through its sulfhydryl moiety to excrete harmful substances from the body, thereby maintaining a healthy immune system (Ighodaro &Akinloye 2017). The GSH/GSSG ratio can be used as an indicator of oxidative stress to signify the health and detoxification capability of cells (Colacevich et al. 2011). In our study, the GSH/GSSG ratios of earthworms in clay soils were significantly greater than in sandy loam soils. Additionally, there was a decreased GSH/GSSH ratio in earthworms exposed to nCeO₂ in sandy loam soils (Fig. 4b), which may be related to the production of antioxidative enzymes under oxidative stress conditions. This was not enough to alleviate the damage caused by nCeO₂ and the inhibition of enzyme activities, indicating that the detoxification capability of the antioxidative defense system was weakened (Yin et al. 2017).

3.5 Ce distribution in soils

As shown in Fig. 5, the major portions of Ce, 80.8% and 83.7%, in the original sandy loam and clay soils, respectively, were associated with the residual phase. With as the nCeO₂ concentration added to the two soils increased, the acid-soluble, oxidizable, and reducible fraction continued to decrease, whereas the residual fraction increased to 98.1%-98.9%. This may be related to the increase in the soil pH caused by the nCeO₂ concentration, which resulted in the nCeO₂ transforming into lower-activity residue. Under neutral or alkaline conditions, the precipitation reactions of hydroxides, sulfides, phosphates, and carbonates that generate heavy metals owing to pH account for larger proportions (García-Gómez et al. 2018), which was also reflected in the sandy loam treatment groups (pH = 7.4).

In the nCeO₂-treatment groups, only very small fractions of Ce (0.24–0.29 mg/kg) were present as acid soluble fractions in the sandy loam soils. However, in clay soils, the range of extractable Ce in the acid-soluble fraction was observed as 0.48 -3.0 mg/kg, which was slightly greater than in sandy loam soils. This may be because the low pH of the clay soils (pH = 4.6, Table 1) increased nCeO₂ solubility (Cornells et al. 2011). In addition, a high clay content also increases the retention of available Ce in the soil (García-Gómez et al. 2018).

The oxidized Ce fractions in the sandy loam soils were higher than that those in the clay soils at low and very high Ce concentrations. Sandy loam soil has strong water and fertilizer retention capabilities, and its high organic matter (18.4 g/kg) content can convert organic matter in the carbonate-bound state to the organic bound state, thereby reducing the bioavailability of Ce. This type of soil has a large number of colloids and a large specific surface area and surface charge. It is prone to obligate adsorption to form the iron-manganese oxidation-combined state (Li et al. 2021). Natural organic matter makes nCeO₂ highly stable in soil suspension owing to the positive surface charged (Van Koetsem et al. 2018). Additionally, surface charge influenced by pH can affect particle-particle interactions as well as particle-soil interactions (Saleh et al. 2008).

The bioaccumulations of heavy metals in earthworms may be significantly affected by soil characteristic (such as pH and organic matter) (Wang et al. 2013). The high clay contents (51.5%, Table 1) of clay soils may enhance the aggregation of nCeO₂ and lead to the formation of clusters (Khushi et al. 2018, Van Koetsem et al. 2018), reducing ion release and its toxic effects on earthworms. This might explain why the biomass of earthworms in clay soils is not obvious negatively affected even when there is high Ce concentration in the organisms. Similarly, even after 28 days of exposure to 10,000 mg/kg concentration, nCeO₂ has no effects on the survival and reproduction of earthworms (Lahive et al. 2014).

The differences in the toxicity levels of heavy metal ions are also largely the result of the different reducing capabilities of soils (Shahid et al. 2017). Although nCeO₂ has a nanotoxicity level, the high clay contents of clay soils will directly or indirectly lead to spontaneous redox reactions involving Ce ions, producing properties similar to those of SOD and CAT that reduce the toxicity of free radicals (Ashraf et al. 2017, Lin et al. 2019). If this property is dominant during the whole process, then oxidative damage is alleviated, and the MDA and PCO contents in earthworms can be reduced (Tassi et al. 2017, You et al. 2021). In addition, under acidic conditions, nCeO₂ exists as spherical particles instead of rod-shaped particles, which increases migratory capacity and reduces toxicity because of the reduced radii (Darlington et al. 2009). Thus, the Ce bioaccumulation in earthworms in clay soils was higher, whereas nCeO₂ was more toxic to earthworms in sandy loam soils as assessed by their biomass, morphology, and antioxidative damage.

This study mainly addressed the bioavailability and ecological effects of nCeO₂ on earthworms in sandy loam and clay soils. The Ce distribution in the two soils mainly represented the residual fractions, and the acid-soluble fraction of Ce was also greater in clay soils than in sandy loam soils. Meanwhile, compared with sandy loam soil, the negative effects of nCeO₂ exposure on groups of earthworms were less profound in clay soils, whilst the Ce content in earthworms in clay soil was higher. These revealed that the Ce devoured by earthworms in soil was mainly the residual fraction, and the bioaccumulation and toxicity effects of nCeO₂ on earthworms in the two soils were inconsistent. The ecological risks posed by nCeO₂ are higher in sandy loam soils with higher pH and lower clay contents. In addition, the traditional BCR analysis method, being used to determine the bioavailability of heavy metals for plants, which is not suitable for analyzing the bioaccumulation of metal nanomaterial in earthworms. These findings are helpful for establishing a broader understanding of nanoparticles characteristics in practical applications, although further research is needed.

Ethics approval and consent to participate

The reported studies did not involve human participants and human data.

Consent for publication

This does not involve any individual’s data.

Availability of data and materials

All data generated or analyzed during this study are included in this publishedarticle.

Competing interests

The authors declare that they have no competing interests.

Acknowledgments

The present study was supported byNational Natural Science Foundation of China (No. 21876083, No. 42177003, and No. 42077116) and Primary Research& Development Plan of Jiangsu Province(BE2019624 and BE2021706)

Authors' contributions

Dun Chen: Data curation,Writing-original draft, Investigation. Wenxuan Xu: Investigation. Shenglai Cao: Investigation. Yan Xia: Investigation. Wenchao Du: Conceptualization, Supervision, Writing-review& editing. Ying Yin: Conceptualization, Data curation, Writin- review & editing, Project administration, Funding acquisition. Hongyan Guo: Conceptualization, Supervision, Funding acquisition.

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Reviews received at journal
25 Mar, 2022
Reviewers invited by journal
16 Mar, 2022
Editor invited by journal
16 Mar, 2022
Editor assigned by journal
10 Mar, 2022
First submitted to journal
04 Mar, 2022

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Divergent Responses of Earthworms (Eisenia Foetida) in Sandy Loam and Clay Soils to Cerium Dioxide Nanoparticles

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Abstract

Figures

1. Introduction

2. Materials And Methods

2.1 Materials

2.2 Soils exposure experiment

2.3 Determination of Ce concentration in earthworms and soils

2.4 Transmission electron microscopy (TEM) observation

2.5. Determination of ROS, MDA, and PCO

2.6 Determination of CAT activity, GSH/GSSG ratio, and MT content

2.7 Statistical analysis

3. Results And Discussion

3.1 Biomass and Ce content of earthworms

3.2 Ultrastructural characterization of earthworm intestines

3.3 Oxidative stress responses of earthworms

3.4 The MT contents and GSH/GSSG ratio of earthworms

3.5 Ce distribution in soils

4. Conclusion

Declarations

References

Status:

Version 1