Risk assessment for and microbial community changes in Farmland soil contaminated with heavy metals and metalloids

https://doi.org/10.1016/j.ecoenv.2019.109685Get rights and content

Highlights

  • Cd is the main priority pollutant and poses the strongest risks.

  • Plots with higher Cd concentrations had less microbial diversity.

  • The dominant Proteobacteria and Acidobacteria were resistant to heavy metals.

  • Heavy metal stress affects soil microorganism evolution and relevant functional genes.

Abstract

Food security and human health can be seriously affected by heavy metal and metalloid (HM) pollution of soil. In this study, the risks posed by HMs and microbial community responses to HM pollution of agricultural soil in southwestern China were investigated. The C, N, P, and S (nutrients) concentrations were 12040.7–15912.7, 1298.06–1832.01, 750.91–2050.35, and 269.17–2115.52 mg/kg, respectively. The As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn concentrations were 3.11–8.20, 1.85–6.56, 22.83–43.96, 11.21–23.30, 0.08–0.81, 11.02–22.97, 24.07–42.96, and 193.63–698.39 mg/kg, respectively. Interpolation analysis indicated that the nutrient and HM concentrations varied spatially rather strongly. The concentrations of all of the elements were higher in soil from the northern sampling sites than in soil from the other sites. HMs in soil were found to pose high levels of risk (RI 898.85, i.e., >600). Cd contributed more than the other HMs to the risk assessment values (ErCd 293.72–1031.94), so was the most serious contaminant. Microbial diversity decreased over time in soil with high HM concentrations (plot S2) and was lower than in soil with low HM concentrations (plot S8). The nutrient and HM concentrations correlated with the microbial community characteristics. Proteobacteria, Acidobacteria, and Chloroflexi were (in decreasing order) the dominant bacterial phyla. We speculate that these phyla may be strongly resistant to HMs. The fourth most common phylum was Actinobacteria. Bacteria in this phylum could be used as biological indicators of the HM pollution status. Soil micro-ecosystems can self-regulate. HM stress will affect the evolution of soil microorganisms and relevant functional genes. The spatiotemporal variability in the microbial community responses to HMs and the spatial analysis and ecological risk assessment results will be useful reference data for the remediation of HM-polluted soil.

Introduction

Soil pollution is a global problem that affects food safety and sustainable development (Alisi et al., 2009; Gandolfi et al., 2010). Soil is an important component of terrestrial ecosystems. Heavy metals and metalloids (HMs) and nutrients can accumulate and be transformed in soil (Gong et al., 2018). HM concentrations in soil are related to the physical and chemical structure of the soil. High HM concentrations will affect the geochemical characteristics of soil (Kavamura and Esposito, 2010).

Nutrients are key elements that affect the physical and chemical structure of soil. N and P are found at relatively high concentrations in most soils, and migrate from and are transformed in soil through numerous processes (Komarek et al., 2013). C is the most important component of biomass and is strongly related to the microorganism population of soil. S can be involved in complexation reactions with some HMs (Zhang et al., 2018). Changes in the concentrations of nutrients in soil directly affect agricultural production, and correlations have also been found between nutrient and HM concentrations (Zhu et al., 2019a). The soil particle size distribution affects the migration and transformation of HMs in soil (Etesami, 2018).

The parent materials, water, various biogeochemical processes, and long-term human activities determine the trace metal concentrations in soil. The intensification of human activities (particularly industrial activities) in recent years has strongly affected the accumulation of pollutants in soil (Kou et al., 2017). HMs are mainly emitted from industrial wastewater and it can enter soil in surface water, in groundwater, and through atmospheric deposition (Cui et al., 2018).

When wastewater is applied to agricultural land, trace metals in the wastewater can remain in the soil and the organic material added in the wastewater can sorb HMs that enter the soil from other sources. HMs can therefore become strongly enriched in the soil (Zhao et al., 2019). The area affected by contaminated soil is continually expanding, and direct and potential risks posed by HMs in soil are becoming increasingly serious. HMs in soil can pose strong risks to human health through the food chain. A high cadmium intake can cause pain and other problems, and a high mercury intake can cause Minamata disease (Jiang et al., 2006; Valko et al., 2005). The increasing seriousness of soil pollution means that action needs to be taken to prevent and control HM emissions to soil (Li et al., 2017).

Environmental quality assessments focused on soil can provide scientifically based data for planning environmental management strategies to prevent and control pollution. Physical and chemical indicators and changes in microbial communities are used in more comprehensive macro- and micro-ecological assessments of regional environments (Chen et al., 2016a). In previous environmental pollution studies, environmental data have usually only been analyzed using common statistical methods, and spatial information has not been fully utilized, so the conclusions have rarely effectively reflected the spatial characteristics of the environmental variables (Li et al., 2006).

Soil contains diverse microorganisms, and the indigenous microorganism community will be relatively stable (Xu et al., 2019). Stress caused by HM pollution changes the characteristics of microbial communities and causes the microecology to become very unstable (Lin et al., 2016). HM pollution permanently affects the microbial biomass and microbial activity (Kavamura and Esposito, 2010). There are complex relationships between HM concentrations and microorganism communities. Some HMs can stimulate microorganism growth at low concentrations but are toxic at high concentrations. Many microbes are involved in the geochemical cycling of HMs. This can occur through HMs being captured by microbe cells and sorbing to binding sites in the cell walls, through soluble HMs being converted into insoluble hydroxides, carbonates, phosphates, and sulfides through microbial metabolism, and through other processes (Kieu et al., 2011; Li et al., 2014; Wen et al., 2009). Most previous studies of microbial responses to HMs have involved using artificially prepared HM-contaminated soil and then identifying changes in soil microorganism diversity. Research into microbial responses to HMs using real soil that has been contaminated with HMs for a long time has only recently started (Bolan et al., 2014). No study of the relationships between HMs and microbial communities in agricultural soil in southwestern China, an important grain-producing area, has previously been performed.

The aims of this study were: (1) to determine the spatial distributions of nutrients and HMs in typical agricultural soil in southwestern China; (2) to use various methods to evaluate the risks posed by key pollutants in soil using environmental physical and chemical indices and microbial diversity characteristics; and (3) to analyze the temporal and spatial microbial community responses to different levels of HM stress.

Section snippets

Study area and soil sample collection

The study area was in Shifang (31°7ʹ33ʺ–31°7ʹ42ʺ N, 104°3ʹ27ʺ–104°3ʹ33ʺ E), Sichuan Province, China. The study area is one of the main grain-producing areas in Sichuan Province. The study area was about 7000 m2, and is shown in Fig. 1. The study area is irrigated with water from an adjacent river, the flow of which fluctuates seasonally. The river has previously suffered HM pollution from wastewater discharged by upstream non-ferrous metal smelting plants. These pollution sources have now been

Soil particle size distribution

The soil particle sizes directly and indirectly affect HM and nutrient migration and transformation in soil. Exogenous HMs will tend to sorb to small particles (such as clay minerals) and accumulate in the soil (Perfect and Kay, 1995). The particle size distributions are shown in Table E5 in SI, and a particle size frequency chart is shown in Fig. G1 in SI. Overall, level two particles (fine powder) contributed the largest proportion of particles (31.67%–60.51% of the total), level seven

Conclusions

Fine particles contributed 31.67%–60.51% of the particles in soil in the study area. The pH and CEC and the C, N, P, and S concentrations varied spatially, and the mean total nutrient concentrations decreased in the order TC > TN > TP > TS. The As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn concentrations varied spatially in a similar way to the nutrient concentrations. The whole study area has potentially high ecological risks from HMs (RI 898.85, i.e., >600), and Cd was the primary pollutant. The

Conflicts of interest

The authors declare no conflict of interest associated with this work.

Acknowledgments

This research was supported by Sichuan Science and Technology Plan (Key Project) of China (2017SZ0184) and the Youth Innovation Promotion Association CAS (Wenzhong Tang, 2017059) and the National Natural Science Foundation of China (No. 41877368). We are grateful to all reviewers for their suggestions, which have made the quality of the paper better.

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