Effects of soil chemical properties and fractions of Pb, Cd, and Zn on bacterial and fungal communities

https://doi.org/10.1016/j.scitotenv.2020.136904Get rights and content

Highlights

  • Acid-extractable Pb was the main fraction affecting bacterial community structure.

  • Water-extractable Pb and Zn were dominant factors shaping fungal community.

  • Heavy metals together with soil chemical properties determined microbial communities.

  • Marmoricola, Nocardioides and Gibberella could be considered as bioindicators.

Abstract

Heavy metal contamination in soils poses a serious threat to microorganisms, which play important roles in soil biogeochemical process. However, the key fractions of heavy metals affecting soil microorganisms are still unclear. In this study, DNA sequencing, redundancy and variance partition analysis were performed to investigate the combined effects of heavy metal fractions and soil chemical properties on microbial communities in Pb, Cd, and Zn co-contaminated soils. The results showed that long-term exposure of microorganisms to these metals changed the richness, diversity, and structure of their communities. The bacterial and fungal Chao richness indexes decreased, but only the bacterial Shannon index improved with increasing metal concentrations. Moreover, soil available potassium and acid-extractable Pb made the greatest contributions to variations in the bacterial community structure, while soil pH, water-extractable Pb and Zn were the dominant factors influencing the fungal community structure. In addition, Marmoricola, Nocardioides, and Gibberella were sensitive to these metals. Overall, the effects of different heavy metal fractions on microorganisms varied significantly, and these metal fractions together with soil chemical properties determined the soil microbial communities.

Introduction

Soil microorganisms, being the most abundant and diverse life forms on Earth, have important effects on biogeochemical processes and nutrient transformation (Smith et al., 2015; Beattie et al., 2018). Their communities not only rely on soil chemical properties, including pH values, organic matter, and soil nutrients (Lauber et al., 2008), but are also influenced by toxic metals (Singh et al., 2019; Xavier et al., 2019). Many studies have investigated the influences of various soil properties on microbial communities in natural soils (Bååth et al., 1995; Geisseler and Scow, 2014). For example, some investigations showed that soil pH, organic carbon, and exchangeable cation contents had strong effects on soil microbial community composition and function (Wakelin et al., 2016; Bom Van Der et al., 2018). However, only a few studies have reported the long-term influences of heavy metals on microbial populations (Chen et al., 2018; Kasemodel et al., 2019).

In recent years, heavy metal contamination in soils has gained worldwide attention because of its high toxicity, non-biodegradability, and long-term accumulative behavior (Wuana and Okieimen, 2011; Fajardo et al., 2019). Heavy metals not only change the soil fertility, also disturb the microbial community and lead to biodiversity loss (Kasemodel et al., 2019). Previous studies reported that total lead (Pb) and zinc (Zn) in soils can lead to different bacterial community structures (Xu et al., 2017; Fajardo et al., 2019), while others showed that total cadmium (Cd) was negatively correlated with most dominant fungal phyla in lightly polluted soils (Lin et al., 2019). Nevertheless, the toxicity of heavy metals depends on their fractions, especially the more biologically extractable forms (Zimmerman and Weindorf, 2010; Kim et al., 2015). However, it is still unclear how their fractions affect the microbial abundance, biomass and community structure. Consequently, it is essential to explore the impacts of different heavy metal fractions on soil microbial communities.

Effective methods for studying soil microbial communities are essential. In the last few decades, community-level physiological profile (Söderberg et al., 2004), phospholipid fatty acid composition (Frostegård et al., 2011), and emerging DNA-sequencing (Shokralla et al., 2012) technologies have been widely used to investigate soil microbial communities. Among these technologies, high-throughput sequencing has been widely applied to study the impact of environmental factors on microbial communities because of its ability to provide vast bioinformatic resources quickly and effectively with relatively low costs (Shokralla et al., 2012; Dang et al., 2019). Recently, some studies based on high-throughput sequencing have shown that heavy metal exposure causes blooms of metal-tolerant microbial populations, such as Proteobacteria and Firmicutes (Singh et al., 2019; Zhao et al., 2019). Other studies demonstrated that some microbes, such as α-Proteobacteria, were sensitive to heavy metals based on decreases in their abundances in polluted soils (Liao and Xie, 2007). Changes in the microbial community composition of polluted soils depend on species replacement in which the tolerant species replace more sensitive ones, leading to changes in biodiversity (Yin et al., 2015). And loss of biodiversity is considered as one of the major threats to soils (Calderón et al., 2017). Under heavy metal contamination, it is essential to investigate and evaluate the sensitivity or indicator of soil microorganisms for soil ecosystem conservation (Xavier et al., 2019), however, few such studies have been conducted to date (Tang et al., 2019).

In this study, we investigated whether soil heavy metal fractions and chemical properties caused changes in microbial diversity and composition. The objectives of this research were to: 1) investigate the richness, diversity and structure of microbial communities in Pb, Cd, and Zn co-contaminated soils through high-throughput sequencing; 2) identify which heavy metal fractions affected the microbial community composition; and 3) identify sensitive bioindicators to these metals.

Section snippets

Site characterization and sample collection

The study sites are located in a typical lead–zinc mining area in Hanyuan (29°24′ N, 102°37′ E), Sichuan Province, China, where there is a humid subtropical monsoon climate. This area has been mined for 32 years, and mining activities, particularly the storage and accumulation of tailings, have caused serious pollution of the local environment, especially serious contamination of the soils surrounding the tailing pond by Pb, Cd, and Zn. Therefore, long-term pollution problems related to these

Soil chemical characteristics and heavy metal concentrations

The soil textures of all six sites were sandy loam (Fig. S2), and soil properties showed significant variation among these sites (Table 1, p < 0.05). All soil pH values were neutral (6.53–7.24). The soil TOC, TN, TP, AN, AP, and AK at Site 1 were highest. Specifically, the soil TOC in Site 1 was three times as more as that in Site 6. Besides, the mean levels of the soil TK, AN, AP, and AK at Site 2 were lowest.

The concentrations of total Pb, Zn, and Cd in all sites except for Site 6 exceeded

Impacts of soil chemical properties on microbial community

Soil microbial biomass and diversity are influenced by various soil environmental variables (Geisseler and Scow, 2014). In the current study, although the measured soil parameters were not significantly related to the bacterial and fungal Chao richness indexes (Table S4), these factors were correlated with the microbial Shannon index. Especially, soil pH was obviously positively correlated with the bacterial Shannon index, but negatively related to the fungal Shannon diversity (p < 0.05, Table

Conclusions

The richness, diversity, and structure of the microbial community were altered in Pb, Cd, and Zn co-contaminated soils. The bacterial and fungal Chao indexes decreased, while the bacterial Shannon diversity improved with increasing heavy metals concentrations. Among the five fractions of these metals, acid-extractable Pb made the greatest contributions to variations in soil bacterial community structures, while water-extractable Pb and Zn were the dominant factors influencing fungal community

Declaration of competing interest

All the authors have reviewed this manuscript and mutually agree for its submission in Science of the Total Environment. This manuscript has not been published in whole or in part, nor is it being considered for publication elsewhere. Furthermore, the authors have no competing interests to declare.

Acknowledgments

This study was supported by the Science and Technology Project for Sichuan Environmental Protection, China (2018HB30) and the Key Research and Development Program of Sichuan Province, China (2019YFN0020). The authors also acknowledge Shanghai Majorbio Co., Ltd. for technical assistance with DNA sequencing.

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