Elsevier

Chemosphere

Volume 236, December 2019, 124337
Chemosphere

Embryonic exposure to soil samples from a gangue stacking area induces thyroid hormone disruption in zebrafish

https://doi.org/10.1016/j.chemosphere.2019.07.068Get rights and content

Highlights

  • Soil leachate from coal gangue stacking area affects the development of zebrafish.

  • Soil leachate exposure alters the expression of HPT axis regulating genes.

  • Soil leachate exposure attenuates the THs levels of zebrafish embryos.

Abstract

The total accumulative stockpiles of gangue from long-term coal mining exceed 1 billion tons and occupy 182 square kilometers, and 50 million tons of additional gangue are generated per year in Shanxi, a major energy province in China. The objective of this study was to examine whether exposure to village soils affected by gangue stacking would disrupt thyroid hormone system homeostasis and eventually affect endocrine system and development, using zebrafish (Danio rerio) as a model organism. The zebrafish embryos were exposed to village soil leachates at 0, 1:9, 1:3 and 1:1 from 1 to 120 h postfertilization (hpf), and the sample caused a dose-dependent increase in the mortality and malformation rate, and decrease in the heart rate, hatching rate and body length of zebrafish larvae. Importantly, the soil leachate alleviated the whole-body triiodothyronine (T3) and thyroxine (T4) levels at higher concentrations, and altered the expression of the hypothalamic-pituitary-thyroid (HPT) axis-regulating genes crh, trh, tshβ, nis, tg, nkx2.1, pax8, hhex, ttr, dio1, dio2, ugt1ab, trα, and trβ and the PAH exposure-related genes ahr2 and cyp1a. These findings highlight the potential risk of thyroid hormone disruption and developmental toxicity from soil samples around coal gangue stacking areas.

Introduction

Coal gangue is a kind of black-gray rock that is associated with coal seams during the coal formation process and has a lower combustion value than raw coal. Coal gangue is discharged from coal exploitation and washing, accounting for 10%–15% of raw coal production, depending on the changes in geological and mining conditions (Liu and Liu, 2010). The cumulative reserves of coal gangue in China reach total 4.5 billion tons, with an annual increase of 659 million tons (National Development and Reform Commission, China, 2012), and the reserves occupy approximately 65,000 ha of land (Li et al., 2010). Coal gangue hills are prone to spontaneous combustion and heat release during the stacking process, resulting in an increase in the temperature of the coal gangue hills, accelerating its physical and chemical weathering process and discharging harmful heavy metals, radioactive elements, polycyclic aromatic hydrocarbons (PAHs) and other organic pollutants into the surface soil. These pollutants may permeate the deep soil and contaminate groundwater through the leaching process, and eventually causing ecological fragilities and health risks (Fan et al., 2013). As reported, PAHs in the sediments of the Tennessee Valley and the Cumberland River Basin in the United States, contaminated by coal mining activities, caused adverse effects on mussels (Wang et al., 2013a). Moreover, 15 PAHs (221–432 μg/kg) have been detected in the tissues of winter wheat collected from coal combustion areas (Tian et al., 2018). The average concentrations of 16 PAHs in the surface water and groundwater were 426.98 and 381.20 ng/L, respectively, in the Heshan coal district of Guangxi, South China (Huang et al., 2016b). These findings indicate that residents living in coal gangue stacking areas might pose direct or indirect exposure to the pollutants through food chains. Therefore, it is critical to investigate the potential health risks of residents in the regions.

Normal thyroid function is essential for several biological processes, including cognitive (Taylor et al., 2014), cardiovascular (Cappola et al., 2019), skeletal muscle (Salvatore et al., 2014), neurodevelopmental (Dingemans et al., 2011) and immune system functions (Fabris et al., 1995). Some studies have shown that several environmental contaminants have been recognized as endocrine-disrupting compounds (EDCs) that interfere with the hypothalamus-pituitary-thyroid (HPT) axis, leading to thyroid disruption and dysfunction (Calsolaro et al., 2017). The HPT axis plays crucial roles in the growth and development of vertebrates and is responsible for hormone synthesis, secretion, transport and metabolism and the maintenance of normal physiological hormone concentrations (Zhang et al., 2018). Altered HPT axis function usually indicates endocrine and developmental effects (Spachmo and Arukwe, 2012). The prolonged occupational exposure to coal dust resulted in a significant increase in serum thyroid stimulating hormone (TSH) levels in coal mine workers compared to the non coal-exposed population, which interfered with the HPT axis (Tumane et al., 2015). The total prevalence of subclinical thyroid disease in the Xuzhou mining area in China is as high as 52.14% (Zhang et al., 2010). Exposure to coal-water extract significantly inhibited the synthesis of thyroid hormones (triiodothyronine (T3) and thyroxine (T4)) in Buffalo rats (Gaitan et al., 1993). However, little is known about the impacts of coal gangue stacking on thyroid function and even the development.

The development of the endocrine system can be easily visualized in real-time during the whole period of early development in zebrafish (Jacobs et al., 2018). An additional advantage of zebrafish embryos is that they are highly homologous to humans, and the thyroid system of zebrafish is similar to that of mammals and amphibians in many aspects (Segner, 2009). These properties make zebrafish a suitable model for investigating the thyroid system in vivo, which can provide valuable information for humans. In the present study, we used zebrafish (Danio rerio) as the model organism and investigated the thyroid-disrupting potential of village soil samples contaminated by coal gangue stacking, including the developmental toxicity, thyroid hormones (THs) contents, and gene transcription levels associated with the HPT axis.

Section snippets

Study area and soil sample collection

In this study, a coal gangue hill of the Qinxin coal mine in Qinyuan County was selected as the study area. Qinyuan County is located in the southeast portion of Shanxi Province, at 36°34′12.24″N and 12°8′55.67″E, and is the key coal production base in Shanxi Province. We collected village soil samples in the vicinity of the coal gangue stacking area. The soil sampling site included 3 subsamples, and for each, the surface soil was removed, and 0–20 cm of topsoil was collected, packaged and

Developmental changes in zebrafish embryos

After exposure for 120 h, soil leachate sample affected developmental parameters in a concentration-dependent manner (Fig. 1A–D). The mortality rates in the 1:3 and 1:1 treatment groups significantly increased and reached 3.62- and 3.98-fold of the control, respectively. The heart rate decreased with the increase of exposure concentration. Moreover, the hatching time delayed following the exposure at higher concentrations, and the hatching rate significantly decreased functioning as the

Discussion

Environmental pollutants that cause the interruption of TH synthesis have attracted much attention (Kim et al., 2016, Zhang et al., 2017, Zhang et al., 2018). To determine the possible endocrine disruption risks following exposure to the contaminated soil adjacent to coal gangue, we used developing zebrafish as a model and assessed the thyroid dysfunction after exposing the zebrafish to soil leachate at various concentrations.

The main harmful organic components in coal gangue have been

Conclusion

In the present study, the village soil leachate from coal gangue stacking area caused a dose-dependent increase in the mortality and malformation rate, and decrease in the heart rate, hatching rate and body length of zebrafish larvae. Importantly, the soil leachate alleviated the whole-body T3 and T4 levels at higher concentrations, and altered the expression of the HPT axis-regulating genes crh, trh, tshβ, nis, tg, nkx2.1, pax8, hhex, ttr, dio1, dio2, ugt1ab, trα, and trβ and the PAH

Acknowledgements

This study was supported by National Science Foundation of China (No. 21477070), Research Project for Shanxi young Sanjin scholarship of China, Program for the Outstanding Innovative Teams of Higher Learning Institutions of Shanxi, Fund for Shanxi "1331 Project" Key Innovative Research Team.

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