Microbial communities in rare earth mining soil after in-situ leaching mining

https://doi.org/10.1016/j.scitotenv.2020.142521Get rights and content

Highlights

  • This is the first study to reveal the microbial structure in rare earth mining soil.

  • Ionic REEs contents significantly and negatively influenced microbial abundances.

  • TREEs and ammonium shaped the bacterial community in mining soils.

  • Archaea rather than bacteria were predominantly responsible for ammonia oxidation.

Abstract

In-situ leaching technology is now widely used to exploit ion adsorption rare earth ore, which has caused serious environmental problems and deterioration of mining soil ecosystems. However, our knowledge about the influences of mining operation on the microbiota in these ecosystems is currently very limited. In this study, diversity and composition of prokaryote and ammonia-oxidizing microorganisms in rare earth mining soil after in-situ leaching practice were examined using quantitative Polymerase Chain Reaction (qPCR) and Illumina high-throughput sequencing. Results showed that in-situ leaching mining considerably impacted microbial communities of the mining soils. The abundances of bacterial, archaeal, and ammonia-oxidizing archaea (AOA) were significantly and negatively correlated with ionic rare earth elements (REEs), while their diversities were relatively stable. Total rare earth elements (TREEs) and ammonium were the strongest predictors of the bacterial community structure, and organic matter was the key factor predicting the variation in the archaeal community. Chloroflexi, Proteobacteria, Acidobacteria, and Actinobacteria were the most abundant bacterial phyla, and archaeal communities were dominated by Thaumarchaeota. Phylogenetic analysis indicated that unclassified Thaumarchaeota and Crenarchaeota were the predominant AOA groups. The non-detection of ammonia-oxidizing bacteria (AOB) and the abundance of AOA indicated that archaea rather than bacteria were predominantly responsible for ammonia oxidation in the mining soil. Network analysis demonstrated that positive interactions among microorganisms could increase their adaptability or resistance to this harsh environment. This study provides a comprehensive analysis of the prokaryotic communities and functional groups in rare earth mining soil after mining operation, as well as insight into the potential interactive mechanisms among soil microbes.

Introduction

Rare earth elements (REEs) consist of 17 elements, i.e., 15 lanthanides plus scandium (Sc) and yttrium (Y). REEs have become vital and indispensable material of many high-tech products, devices, and technologies, including clean energy, national security systems, and military/defense applications. Found in Jiangxi Province in 1969, China's ion adsorption rare earth ores (REO) is the most unique rare earth deposit in the world. Because of the stable chemical properties, these absorbed rare earth minerals do not hydrolyze and dissolve in neutral water, but can be leached by electrolyte solution due to their ion-exchange properties (Chi et al., 2005). Scientists and engineers proposed an ion-exchange leaching method for REEs extraction. Over years of development, the in-situ leaching mining has become the dominant technology. The leaching solution is 3–5% ammonium sulfate ((NH4)2SO4), and the leaching process takes 150–400 days. Unfortunately, the in-situ leaching process has a significant impact on the mining soil ecosystem, including soil acidification, soil erosion, ground-water contamination, mine collapses, and landslides (Packey and Kingsnorth, 2016). Besides, the capillary forces surrounding leaching holes accumulate large amounts of leaching solution and REEs in mining soil, which not only completely change the original soil properties but also destroy surface vegetation, making rehabilitation more difficult (Feng et al., 2012; Yang et al., 2013).

In addition to the obvious environmental quality degradation at the macroscale, in-situ leaching mining can also alter the soil microorganisms. As an essential component of the soil ecosystem in mines, microorganisms not only play an important role in element cycling, interactions among biological processes, and maintenance of plant diversity, but also make great contributions to ecosystem diversity and the restoration of ecosystem function (Gobat et al., 2004). Because of in-situ leaching mining, large amounts of REEs and ammonium are accumulated in mining soils. Microbial communities and essential biogeochemical processes are disrupted, and microbial populations and their dynamics associated with leaching solution and REEs should be shifted/reshaped (either enhanced or inhibited). Moreover, long-term exposure of microbes in this harsh environment may force the microbial population evolving into a community with a higher level of tolerance and resistance to the harsh environmental conditions. Up to now, previous studies have focused on the effects of exogenous REEs on microorganisms in agricultural soil by employing pure culture and traditional biological methods (Jiang et al., 2008; Tang and Li, 2002; Zhu et al., 2002) and, thus, provided limited information about the microbes in mining soils. It is not yet clear how microbial communities are shaped by the prevailing geochemical factors in the distinctive environments of mining soils, and whether major environmental determinants of microbial communities are influenced by the in-situ leaching mining. Furthermore, ammonium pollution persists long after mining ceases through exacerbated nutrient pollution (Yang et al., 2013), and influences the nitrogen biogeochemical process in the mining soil. Ammonia oxidation, the first and rate-limiting step of nitrification, is performed by both ammonia-oxidizing archaea (AOA) and bacteria (AOB). They have been found to coexist in many different types of soil and may have functional differences in their response to soil physicochemical properties (Jiang et al., 2014; Tao et al., 2017; Yao et al., 2017). So far, we know little about the ammonia-oxidizing microorganisms in REO sites, and the effects of in-situ leaching mining on AOA and AOB communities and function in mining soils.

Here, we applied qPCR and MiSeq sequencing technique to conduct an in-depth examination of prokaryotic communities, including AOA and AOB, in rare earth mining soil after in-situ leaching mining, and to gain insight into the potential interactions of these extraordinary microorganisms. We further examined how leaching practice influenced the microbial communities, and explored the potential relevance between soil microorganisms and soil biochemical processes. The observations and related findings represent the first step in understanding the effects of long-term mining operation on the mining soil, and will deepen our understanding of microbial ecology and evolution associated with ion-exchange leaching of REEs.

Section snippets

Site description and sample collection

Longnan County, which is famous for the first discovery of ion adsorption REOs and the application of in-situ leaching for REE extraction, is located approximately 133 km south of Ganzhou City, Jiangxi Province, China. This region is characterized by a subtropical wet monsoonal and humid climate, with a mean annual precipitation of 1536 mm and average minimum and maximum temperatures of 8.3 °C and 33.2 °C, respectively. Located in the south of Longnan County, the ion adsorption REO is in a

Soil physicochemical characteristics

The REO mining soils exhibited distinctive types of physical and geochemical gradients compared with the reference soils (CKS and CKT), as summarized in Table 1. The mining soils were characterized by acidic pH values ranging from 4.27 to 5.19 (4.75 ± 0.33, mean ± s.d.), which were all significantly (p < 0.05) lower than the reference soils (7.35 ± 0.63). Organic matter of the mining soil samples, except for LK4–2, generally were higher than those of the reference soils, but in LK1–1, LK1–2,

Discussion

In this investigation, 12 mining soil samples were collected in a rare earth mining area where in-situ leaching practice had been used to extract REEs. The community structures of bacteria, archaea, and ammonia-oxidizing microorganisms were analyzed to elucidate the impacts of in-situ leaching mining on soil physicochemical properties and microbial communities. This study is the first to reveal the diversity and community structure of prokaryote and ammonia-oxidizing microorganisms in rare

Conclusions

As a whole, the REE mining soil was characterized by acidic pH and high levels of ionic REEs, TREEs, and ammonium. Detailed information about the soil microbiota was provided by qPCR and Illumina high-throughput sequencing. Chloroflexi, Proteobacteria, Actinobacteria, and Acidobacteria were the most abundant bacterial phyla, and they might play important roles in C/N-related pathways. Thaumarchaeota was dominant in the archaeal community, and AOA-related Thaumarchaeota accounted for a large

CRediT authorship contribution statement

Jingjing Liu: Conceptualization, Investigation, Methodology, Data curation, Writing - original draft, Project administration. Wei Liu: Conceptualization, Data curation, Software, Formal analysis, Funding acquisition, Writing - review & editing. Yingbin Zhang: Investigation, Data curation, Validation. Chongjun Chen: Resources, Software, Formal analysis, Visualization, Writing - review & editing. Weixiang Wu: Conceptualization, Supervision, Writing - review & editing. Tian C. Zhang: Writing -

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

This work was supported by the National Natural Science Foundation of China (Grant No. 31760157), Education Department of Jiangxi Province Project (GJJ160627), and Natural Science Foundation of Hebei Province (D2019201332). The authors would like to gratefully acknowledge Dr. Bing Han from The University of Melbourne for critical comments that improved the manuscript.

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