Soil bacterial community structure in the habitats with different levels of heavy metal pollution at an abandoned polymetallic mine

https://doi.org/10.1016/j.jhazmat.2022.130063Get rights and content

Highlights

  • Soil bacterial composition was significantly different between four types of habitats.

  • Soil bacterial diversity in tailing area was lowest, but highest in undisturbed area.

  • Heterogeneous selection governed the bacterial distribution across distinct areas.

  • Cu and Zn primarily shaped bacterial composition in tailing and remediation areas.

  • Soil nutrients and vegetation were key for natural recovery and undisturbed areas.

Abstract

Heavy metal pollution caused by mining activities can be harmful to soil microbiota, which are highly sensitive to heavy metal stress. This study aimed to investigate the response of soil bacterial communities to varying levels of heavy metal pollution in four types of habitats (i.e., tailing, remediation, natural recovery, and undisturbed areas) at an abandoned polymetallic mine by high-throughput 16 S rRNA gene sequencing, and to determine the dominant ecological processes and major factors driving the variations in bacterial community composition. The diversity and composition of bacterial communities varied significantly between soil habitats (p < 0.05). Heterogeneous selection played a crucial role in shaping the difference of bacterial community composition between distinct soil habitats. Redundancy analysis and Pearson correlation analysis revealed that the total contents of Cu and Zn were key factors causing the difference in bacterial community composition in the tailing and remediation areas, whereas bioavailable Mn and Cd, total nitrogen, available nitrogen, soil organic carbon, vegetation coverage, and plant diversity were key factors shaping the soil bacterial structure in the undisturbed and natural recovery areas. These findings provide insights into the distribution patterns of bacterial communities in soil habitats with different levels of heavy metal pollution, and the dominant ecological processes and the corresponding environmental drivers, and expand knowledge in bacterial assembly mechanisms in mining regions.

Introduction

Heavy metal pollution brought by mining activities causes severe damage to the soil ecosystem, and results in hazardous effects on soil microbiota (Fashola et al., 2016, Gan et al., 2022, Järup, 2003, Pereira et al., 2014, Rodríguez et al., 2009, Tchounwou et al., 2012). Compared to plants and soil animals, soil microorganisms are much more sensitive to the changes of heavy metal contents because they can rapidly respond and adapt to heavy metal stress (Giller et al., 1998, Harris et al., 1993, Turco et al., 1994). It has been observed that heavy metal pollution reduced the total biomass, diversity, and activity of soil microbial communities, and could change their composition as well (Bååth, 1989, Fashola et al., 2016, Hinojosa et al., 2005, Pereira et al., 2014, Song et al., 2018). At the same time, soil microbial communities perform many important ecosystem services and play a crucial role in driving key ecological processes in soils, such as cycling of nutrient elements (Allison and Martiny, 2008, Bardgett et al., 2005, Fierer and Jackson, 2006). Therefore, it is important to understand the changes in diversity and composition of soil microbial communities under different levels of heavy metal pollution (Azarbad et al., 2015, Hinojosa et al., 2005).

The assembly processes of microbial communities determine the microbial diversity and composition under heavy metal stresses (Sun et al., 2021). Deterministic processes and stochastic processes are complementary for explaining the microbial community assembly (Monard et al., 2016, Stegen et al., 2012, Wang et al., 2013, Zhou and Ning, 2017). Deterministic processes are driven by environmental heterogeneity, i.e. measurable environmental variables, while stochastic processes include unpredictable factors, such as dispersal limitation, mass effects, and random demographics (Caruso et al., 2011, Chase and Myers, 2011, Dini-Andreote et al., 2015). It has been suggested that stochastic processes dominantly shape some microbial communities (Inceoğlu et al., 2011, Sigler et al., 2002), while increasing evidences have confirmed the dominant role of deterministic processes in driving the microbial distribution pattern across habitats (Hassell et al., 2019, He et al., 2021, Liu et al., 2021). A recent study revealed that deterministic processes governed the microbial community assembly under heavy metal stress, and the bacterial community assembly was more deterministic with increases in heavy metal concentrations (Zhang et al., 2022). Nevertheless, the ecological processes of microbial community assembly under heavy metal pollution remains unclear. Investigating the microbial community assembly processes among different types of soil habitats in mining regions may help bridge this knowledge gap.

Soil habitats in mining regions are complex and diverse, and both the physicochemical properties of soils and the total contents and bioavailability of heavy metals can vary largely between different sites (Li et al., 2020b, Pan et al., 2020, Rodríguez et al., 2009). These environmental factors could influence the distribution of microbial communities in different soil habitats. A few studies have explored the impact of heavy metal pollution on the structure of soil microbial communities in mining regions, and found that the total contents of heavy metals could reduce microbial diversity and change microbial composition (Duan et al., 2021, Fashola et al., 2016, Garaiyurrebaso et al., 2017, Li et al., 2020a, Qian et al., 2022). Epelde et al. (2015) found that the bioavailability of heavy metals (Cd, Pb, and Zn) could well explain the difference in microbial community composition between the soils with different pollution levels. Zhen et al. (2019) showed that the bioavailability of heavy metals (Cu, Zn, Pb, and Cd) was equally significant as their total contents in determining the composition and function of microbial communities in the soils of different land use types. It has also been reported that both the physicochemical properties of soils, including available potassium (AK), soil organic carbon (SOC), and soil pH, and the total contents of heavy metals, affected the distribution of microbial communities in five types of soil habitats (i.e., active mining area, dressing area, heap mining area, tailing area, and vegetable field) in a mining region (Zhao et al., 2019). Meanwhile, Marcin et al. (2013) found that even in the soil severely polluted by heavy metals, soil nutrients, such as SOC and total nitrogen (TN), were the most important environmental factors affecting microbial communities, while the total contents of heavy metals (Cd, Pb, and Zn) showed no significant effect on them. Vegetation cover can mitigate heavy metal pollution, improve soil quality, and establish distinct microenvironment (Garaiyurrebaso et al., 2017, Gonçalves et al., 2020, Hernández-Cáceres et al., 2022, Herrera et al., 2007). Meanwhile, plant productivity, coverage, diversity and species richness are also recognized to play crucial roles in shaping the diversity and composition of soil microbial communities in mining regions (Eisenhauer et al., 2017a, Garaiyurrebaso et al., 2017, Gazitúa et al., 2021, Herrera et al., 2007). To the best of our knowledge, no study has attempted to compare the diversity and composition of microbial communities in various types of soil habitats in mining regions to understand the variations of bacterial community structure under different levels of heavy metal pollution and the recovery of soil microbial communities within the remediation and natural recovery areas of such regions.

Based on the foregoing literature review, the assembly mechanisms of soil bacterial communities under heavy metal pollution, and their variations with the environmental factors between different soil habitats of mining regions are still not conclusive. The objective of this study was to comprehensively investigate the diversity and composition of bacterial communities in the tailing area, remediation area, natural recovery area, and undisturbed area of an abandoned polymetallic mine, and explore the major ecological processes and environmental factors that drove the distribution patterns of the bacterial community structure in these soil habitats. The following hypotheses were developed: (1) soil bacterial community composition was significantly different between the four types of soil habitats; (2) soil bacterial community diversity was the lowest in the tailing area, but the highest in the undisturbed area; and (3) the bacterial community composition in different types of soil habitats was shaped by the total contents and bioavailability of heavy metals, as well as soil physicochemical properties. A total of 54 topsoil samples were collected from 18 sites located in the tailing, remediation, natural recovery, and undisturbed areas of an abandoned polymetallic mine in Guangdong province of southern China. Bacterial community diversity and composition in different soil habitats were investigated based on 16 S rRNA gene sequencing, and their relationships with the environmental factors that could affect the soil bacterial community structure were systematically examined to test the above hypotheses. The findings provide important insights into the variations in diversity and composition of bacterial communities among different areas of mining regions, and shed new light on the assembly of bacterial communities across soil habitats under heavy metal pollution.

Section snippets

Sample collection and analysis

Surface soil samples were collected from different types of areas in the Yaopo mountain mining district (24°31′16″ N, 113°04′29″ E), which is located in the southwest of Shaoguan, Guangdong Province of China. Deposits of limonite, pyrite, lead-zinc ore, and some rare earth minerals were found at this polymetallic mine, and opencast mining of lead-zinc ores was carried out intensively between 2012 and 2014 (Sun et al., 2020). Due to the depletion of the rich ores, this mine became abandoned

Soil physicochemical properties and vegetation density

The TN (342.9–3351 mg/kg), AN (26.10–416.4 mg/kg), and SOC (1140–39760 mg/kg) contents of the soil samples were significantly different (p < 0.001) between the four types of areas, and decreased in the order of: undisturbed area > natural recovery area > remediation area > tailing area (Fig. 1). The contents of MBC and AK of the soil samples ranged from 7.53 to 403.7 mg/kg, and from 14.33 to 189.5 mg/kg, respectively (Fig. 1). They also varied significantly between the four types of areas (p

Conclusions

This study shed light on the variations in the diversity and composition of bacterial communities in the surface soils from four types of areas (with varying levels of heavy metal pollution) in an abandoned mining district, and the ecological processes and major environmental factors that drove their structure. Bacterial diversity in the four types of soil habitats showed significant difference, and decreased in the order of: undisturbed area > natural recovery area > remediation area > tailing

Environmental implication

Mining activities cause widespread heavy metal pollution that damages the soil ecosystem, in which microorganisms are most sensitive to the stress of heavy metals. This study revealed that the total contents of Cu and Zn were the most important factors causing the difference in the composition of bacterial communities in the tailing and remediation areas of a polymetallic mine, whereas bioavailable Mn and Cd, total and nitrogen, soil organic carbon, vegetation coverage, and plant diversity were

CRediT authorship contribution statement

Yue Yin: Conceptualization, Data curation, Visualization, Methodology, Writing – original draft, Writing – review & editing. Xiaojie Wang: Data curation, Methodology. Yuanan Hu: Conceptualization, Funding acquisition, Resources. Fadong Li: Project administration, Resources. Hefa Cheng: Conceptualization, Funding acquisition, Resources, Supervision, Writing – original draft, Writing – review & editing.

Declaration of Competing Interest

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.

Acknowledgements

The constructive comments of the anonymous reviewers on an earlier version of this manuscript are greatly appreciated. The authors would like to thank Professor Z. Tang (Peking University) for helpful suggestion and discussion on plant diversity. This work was supported in parts by the Natural Science Foundation of China (Grant Nos. 41877112, 42077110, and 41725015).

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