Response of soil enzyme activities and bacterial communities to the accumulation of microplastics in an acid cropped soil

https://doi.org/10.1016/j.scitotenv.2019.135634Get rights and content

Highlights

  • PE and PVC MPs inhibited FDAse activity and stimulated urease and acid phosphatase activities.

  • PE MPs pollution caused a higher OTUs reduction compared to the PVC MPs pollution in the soil.

  • PE MPs promote the abundance of the bacterial family associated with nitrogen fixation in the soil.

  • High PVC MPs level significantly reduced the abundance of family Sphingomonadaceae in the soil.

Abstract

The ecological stress of microplastics (MPs) contamination in agroecosystems raise worldwide concerns. However very few studies concentrated on the effects of MPs exposure on soil microbial community. The alterations of enzymatic activities and bacterial communities were assayed by spiking 1% and 5% (w/w) of polyethylene (PE) and polyvinyl chloride (PVC) MPs in an acid soil. The results showed that both PE and PVC addition inhibited fluorescein diacetate hydrolase activity and stimulated urease and acid phosphatase activities, and declined the richness and diversity of the bacterial communities. More severe effects were observed in the PE treated soils compared to the PVC treated soils generally. The relative abundances of families Burkholderiaceae increased significantly (p < .05) after MPs addition, suggesting the bacteria associated with nitrogen fixation stimulated by the MPs input. Meanwhile, significant (p < .05) decline of Sphingomonadaceae and Xanthobacteraceae after addition of 5% PVC and 1% PE MPs, respectively implied that MPs might inhibit the biodegradation of xenobiotics in the soil. Mover, the PICRUSt analysis demonstrated that membrane transporter was a sensitive prediction functional gene of microplastics exposure in the soil. Future studies could be focused on the role of MPs on the regulation of nitrogen cycling and organic compounds degradation in soils.

Introduction

The threats of microplastics (MPs) pollution on the terrestrial ecosystems have raised great concerns worldwide in recent years (de Souza Machado et al., 2018; Ng et al., 2018; Zhang et al., 2018a). Especially in agroecosystems, the burden of MPs litters in the soils even higher than ocean basin (Nizzetto et al., 2016), which has been deemed as a type of emerging pollutants in soil environment. A variety of sources was recognized as the input of MPs to the soils, including plastic mulching, residual of plastic wastes, soil amendments application and irrigation water (Blasing and Amelung, 2018; Nizzetto et al., 2016; Steinmetz et al., 2016; Weithmann et al., 2018). An estimation of 35 billion to 2.2 trillion pieces of MPs was input into the cropped soils via the pathway of compost application in Germany every year (Weithmann et al., 2018). However, only limited papers have reported the abundance of MPs in the soils. Fuller and Gautam (2016) found that MPs level in the topsoil was high up to 7% by weight near roads and industrial areas around Sydney (Australia), which is the highest value for soils ever reported by now. In the rice-planting soil, a previous study showed that the MPs abundance was 16.1 ± 3.5 pieces kg−1 on average (Lv et al., 2019). However, a level up to 18,760 pieces kg1 of the MPs was reported in the cropped soil with plastic mulching and most of the MPs had a size of <1 mm in diameter (Liu et al., 2018; Zhang and Liu, 2018).

MPs may persisted in soils for over a hundred years due to the low light and oxygen conditions for degradation (Zalasiewicz et al., 2016). Therefore, MPs in soils might have impacts on the soil chemistry, biophysical environment and microbiome. For instance, Liu et al. (2017) reported that addition of MPs in Chinese loess soil changed the composition of soil dissolved organic matter (DOM), which might impact on the biogeochemistry of elements eventually. Certain MPs may change the elements of soil via leaching of components. Fuller and Gautam (2016) reported that soil chlorinity had a positive correlation with plastic content near industrial areas where polyvinyl chloride (PVC) was used. The impacts of MPs on biophysical environment of the soil and their consequences for microbial activity and plant performance were proposed by the research team of Matthias C. Rillig recently (de Souza Machado et al., 2019; de Souza Machado et al., 2018). They investigated the effects of different MPs on soil structure and water dynamic using soil incubation experiments, and their findings indicated that changes of soil bulk density and water hold capacity trigged by MPs might cause pronounced impacts on microbial activity, plant traits and function. However, the effects were uncertainty due to the variations of shapes, polymers and sizes of the MPs.

Soil enzymes produced by microbes and plants are closely related to soil energy flows and nutrient cycling and respond rapidly to soil changes (Cui et al., 2018). The soil fluorescein diacetate hydrolase (FDAse) activity which represents overall microbial metabolic activity was found increase with addition of polypropylene smaller than 180 μm in Chinese Loess soils (Liu et al., 2017). However, recent studies revealed that impacts of MPs on the soil FDAse activity might depend on MPs types (de Souza Machado et al., 2019; de Souza Machado et al., 2018). Meanwhile, different soil enzymes may contrast react to the same MPs. For the same study of Liu et al. (2017), they also analyzed phenol oxidase (PO) activity and found it was lower in the soils with MPs exposure than that in the control soils in the first seven days. In addition to the soil enzymatic activities, quantification the microbial communities are an alternative way to reflect the ecological response to soils changes. The sequencing of bacterial 16S rRNA gene for the extracted soil DNA is an advance technology for microbial community analysis. With this advanced technology, researchers found that exposure of PVC MPs significantly enhanced bacterial diversity of soil collembolan (F. candida) gut (Zhu et al., 2018), while the bacterial diversity of F. candida gut decreased after exposure of PE MPs. Notwithstanding, very few studies have concentrated on the microbial community in soils under the stress of MPs contamination. No clear trends of the microbial community structure were found in the soils addition of high-density polyethylene (HDPE), polyethylene terephthalate (PET), or PVC MPs (Judy et al., 2019). Therefore, we quantified soil bacterial communities via high-throughput sequencing of bacterial 16S rRNA gene as well as enzyme activities to reveal the effects of MPs contamination on the microbial communities and functions of the soil. The acid paddy soil was selected for experiment because it is a type of soil distributed widely in tropical or subtropical monsoon climate region. These results will help us to enhance the understanding of the ecological risk from the MPs in agroecosystems.

Section snippets

Soil incubation experiment

This experiment was carried out in the climate-controlled chamber (PRX-600B, Hangzhou, China) at Zhejiang Agricultural and Forestry University, China. A tested soil is a loamy soil, collected from the surface (0–20 cm) of an agricultural field in Lin'an, Zhejiang Province (30°18′59.32″ N, 119°44′ 32.85″E). The tested soil is Stagnic Anthrosols based Chinese soil taxonomy and is a common soil type distributed widely in subtropics of China (Chen, 1981). The physicochemical properties of the soil

Soil enzymatic activities

Three soil enzymes including urease, acid phosphatase and FDAse were measured in the study. Fig. 2 shows the changes of soil enzymatic activities over time during the incubation period. Slight fluctuation of the enzymatic activities is observed for all the three soil enzymes during the incubation. The changes of urease activity with time can be divided into two types, the first type is involved of CK and PVC1 while the second type is involved of other three treatments (PVC5, PE1 and PE5) (Fig. 2

Effects of microplastics on soil enzymatic activities

This study revealed that urease, acid phosphatase and FDAse activities were all affected by the addition of both PVC and PE MPs in the soil. The effects of microplastics on soil enzymatic activities have been assayed in the previous studies, in which FDAse and phenol oxidase (PO) were involved in the test (de Souza Machado et al., 2019; de Souza Machado et al., 2018; Liu et al., 2017). The negative effects of MPs on the FDAse in present study was different from previous studies in Chinese Loess

Conclusions

This study demonstrated that microplastics contamination in an acidic soil affected both soil enzymatic activities and bacterial community structures although such effects depended on MPs types and contamination levels. Microorganism activities and alpha diversity of the bacterial communities declined as a result of MPs contamination. The PE MPs with an average diameter of 678 μm contaminated soil had a higher OTUs reduction compared to the PVC MPs with an average diameter of 18 μm contaminated

Declaration of competing interests

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.

CRediT authorship contribution statement

Yufan Fei: Investigation, Writing - original draft. Shunyin Huang: Investigation. Haibo Zhang: Supervision. Yazhi Tong: Software, Visualization. Dishi Wen: Formal analysis. Xiaoyu Xia: Investigation. Han Wang: Investigation. Yongming Luo: Writing - review & editing. Damià Barceló: Writing - review & editing.

Acknowledgments

This research was funded by the Zhejiang Provincial Natural Science Foundation of China (No. LZ19D010001), National Natural Science Foundation of China (No. 41771351), Zhejiang Agriculture and Forestry University Research Fund (2017FR021), Key Research Program of Frontier Sciences, CAS (No. QYZDJ-SSW-DQC015) and the 111 Project (D18008).

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