Dynamic response of enzymatic activity and microbial community structure in metal(loid)-contaminated soil with tree-herb intercropping

Highlights

• Tree-herb intercropping improves the biological quality of polluted soil.

• Soil enzyme activity and microbial diversity benefited from tree-herb intercropping.

• Acid phosphatase activity was further enhanced by SL, GL, and GSLW intercropping.

• Tree-herb intercropping had a significant impact on the AM fungal community in soil.

Abstract

Tree-herb intercropping was proposed for use in remediation of metal(loid)-contaminated soil. Changes in the enzymatic activities and microbial communities in contaminated soil during tree-herb intercropping were studied through dynamic sampling in a greenhouse experiment. Two herb plants, Pteris vittata L. (W) and Arundo donax L. (L), and two tree plants, Morus alba L. (S) and Broussonetia papyrifera L. (G), were selected for tree-herb intercropping, namely SL, GL, GW, SW, and GSLW intercropping. The activities of four enzymes, dehydrogenase activity (DHA), urease activity (UA), sucrase activity (SA) and acid phosphatase activity (APA), are involved in N, C, P cycling and were measured colorimetrically, while the bacterial and arbuscular mycorrhizal (AM) fungal community structures were determined using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE). The results showed that tree-herb intercropping could effectively recover enzymatic activity, and bacterial and AM fungal diversity in metal(loid)-contaminated soil. Compared with treatment without plants, the SA and APA activity after the five tree-herb intercropping treatments were significantly (p < 0.05) increased by 1.64–2.51 times and 2.35–5.70 times after 270 d of cultivation, respectively. Meanwhile, the Shannon-Wiener indexes for bacteria and AM fungi increased by 13.6–17.7% and 20.0–36.9%, respectively. Soil DHA, UA, and SA were slightly affected by tree-herb intercropping; however, APA was further significantly enhanced by SL, GL, and GSLW intercropping when compared to the monoculture treatments after 270 d of cultivation. These results indicated that tree-herb intercropping could effectively mitigate the toxic effects of metal(loid)s on soil enzyme activities and microbial community structures and enhance the potential for ecological remediation of metal(loid)-contaminated soil in mining areas.

Introduction

Anthropogenic activities, such as mining, manufacturing, smelting activities, etc. have caused heavy metal and metalloid accumulation in soil, which has become a serious global environmental problem that severely threatens human health (Rachwał et al., 2017; Cao et al., 2018; Huang et al., 2019). Furthermore, metal(loid)s, such as cadmium (Cd), arsenic (As), zinc (Zn) and lead (Pb), are toxic to physiological functions in living organisms (Li et al., 2017; Lü et al., 2018). Soil microorganisms and enzymes are the primary mediators of soil biological processes, including organic matter degradation, mineralization, and nutrient recycling and transformation, of all which play an important role in maintaining soil quality and ecosystem functionality (Li et al., 2009; Xiao et al., 2017). Recently, studies have been demonstrated that metal(loid)s have an adverse influence on the biological features in soil, including the activity, composition and diversity of the microbial community in soil (Zhu et al., 2013; Guo et al., 2017; Jia et al., 2017) and the activity of enzymes involved in C (sucrase), N (urease), P (phosphatase) and S (arylsulfatase) transformation (Ai et al., 2018; Duan et al., 2018; Martín-Sanz et al., 2018). Soil enzyme activities and microbial communities are considered to be reliable biological indicators of soil function and health (Cao et al., 2017; Liu et al., 2017; Zeng et al., 2018). Consequently, it is urgent to reduce the adverse influences of metal(loid)s on soil microorganisms and restore normal biological properties in contaminated soil (Yang et al., 2007).

Phytoremediation, a cost-effective “green technology”, plays a crucial role in improving the biological properties of contaminated soil (Fiorentino et al., 2017; Wang et al., 2017). To regulate nutrient uptake and reduces stresses caused by environmental metals, plants can secrete numerous low molecular weight compounds, including amino acids, organic acids, phenolics, and sugar, and high molecular weight compounds, including mucilage and proteins from roots, into the rhizosphere soil (Chen et al., 2017). The variety of exudates released by plants has been considered to be a key factor that influences microbial diversity in the rhizosphere (Grayston et al., 1998). For example, enzymatic activities and microbial communities in Cd-contaminated soil have been shown to benefit from phytoremediation using five ornamental plants (Zeng et al., 2018). Soil microbial diversity has been increased by the cultivation of Arundo donax L. in As-, Cd-, and Pb-contaminated soil (Liu et al., 2017). Elsholtzia haichowensis was able to reduce the availability of metal(loid)s and as a result reduce stress in rhizospheric microbes (Deng et al., 2018). Chen et al. (2018) found a specific assembly pattern in root-associated microbiomes in Hibiscus cannabinus during phytoremediation of metal(loid)-contaminated soil. The soil microbial population has been shown to play an important role in plant growth by producing beneficial substances, such as mineral phosphate solubilizers, indole acetic acid (IAA), siderophores and 1-aminocyclopropane-1-carboxylate (ACC) deaminase, and increasing the tolerance of plants to heavy metals that cause soil fungi and bacteria to play different ecological roles during the phytoremediation of copper tailing dam (Jia et al., 2017). Plant root activity has been shown to stimulate soil enzyme activity and induce important shifts in bacterial community structure over time in metal(loid)-enriched mine tailings (Touceda-González et al., 2017). Accordingly, soil enzyme activities and microbial communities act as important biological components during the process of phytoremediation.

Intercropping is the simultaneous cultivation of several plant species that can potentially increase the efficient use of land and spatial resources in agriculture and is regarded as a practical technique that is based on the ecological principles of diversity, competition and facilitation (Hong et al., 2017). Intercropping can significantly enhance crop yields (Li et al., 2013; Latati et al., 2014) and effectively enhance the efficiency of the phytoextraction of metal(loid)s from contaminated soil (Wan et al., 2017; Zeng et al., 2019a). Furthermore, intercropping has been reported to augment soil enzyme activity (Ma et al., 2017; Zeng et al., 2019b), microbial diversity (Zhou et al., 2011; Li et al., 2016), and soil physico-chemical properties (Chen et al., 2019), which can alleviate the negative impacts of heavy metals or metal(loid)s on soil microbes. For instance, the intercropping of Zea mays with Digitaria ciliaris has been shown to increase soil microbial activity and functional group diversity and alleviate the negative impacts of Pb on soil microbes in contaminated soil (Yang et al., 2012); intercropping of Brassica juncea with Festuca arundinacea Schreb has been shown to increase microbe populations and the activities of phosphatase, dehydrogenase and urease in the presence of combined Cd and Pb contamination (Gao et al., 2012). Plant diversity was shown to play a significant role in restoring the quality of contaminated soil (Yang et al., 2007; Yang et al., 2012; Zeng et al., 2019c). Such positive interactions resulting from intercropping are largely be driven by the rhizosphere microbial communities harboured by plants, while soil biota may reinforce negative complementarity effects by competing with plants for nutrients, space, and other resources, thereby reducing community productivity (Eisenhauer, 2012). However, few studies have focused on the microbiological properties of the rhizosphere of tree-herb intercropping on metal(loid)-contaminated soil as determined by dynamic sampling. Therefore, we hypothesized that tree-herb intercropping can increase the diversity of soil microbes and effectively maintain or improve enzymatic activity and bacterial and arbuscular mycorrhizal (AM) fungal microbial communities in metal(loid)-contaminated soil. In this study, two herb plants (P. vittata L. and A. donax L.) and two woody plants (M. alba L. and B. papyrifera L.) were selected for tree-herb intercropping using a greenhouse experiment. The specific objectives of the study were: (1) to study the changes in soil enzyme activity, bacterial and AM fungal communities in metal(loid)-contaminated soil resulting from tree-herb intercropping based on dynamic sampling, and (2) to evaluate the relationship between the available contents of As, Cd, Pb, Zn, and Cu and the microbial (bacterial and AM fungal) communities in contaminated soil during tree-herb intercropping.