Elsevier

Chemosphere

Volume 248, June 2020, 125974
Chemosphere

Changes in oxidative stress biomarkers in Sinonovacula constricta in response to toxic metal accumulation during growth in an aquaculture farm

https://doi.org/10.1016/j.chemosphere.2020.125974Get rights and content

Highlights

  • Pb, Hg, Cd and Cr levels in Wenyang aquafarm could be considered as light pollution.

  • Toxic metal pollution should be monitored in bivalve-culture aquafarms.

  • The visceral mass of Sinonovacula constricta should not be eaten as food.

  • MDA might be a biochemical marker for a Hg-contaminated aquatic environment.

  • MT and SOD may play a role in the response of S. constricta to toxic metal pollution.

Abstract

Clam farming comprises an important part of China’s economy. However, increasing pollution in the ocean caused by toxic metals has led to the bioaccumulation of toxic metals in marine animals, especially the bivalves such as clams, and the consequence of heavy metal-associated toxicity in these animals. Such toxicity can enhance the production of reactive oxygen species (ROS) within the tissues of the animals. In aquatic species, oxidative stress mechanisms have been studied by measuring the antioxidant and oxidative damage index in the tissues. The objectives of this study were to investigate the levels of different toxic metals and the extent of oxidative stress responses in the clam Sinonovacula constricta at different growth periods (from May to October) in an aquaculture farm in Wengyang, an important economic shellfish culture zone in Zhejiang Province, China. Water and sediment samples taken from the farm were subjected to Pb, Hg, Cd, Cr assays. Overall, the levels of these metals in the water and sediment could be considered as light pollution, though the levels of Hg in the water (0.266) and Cd in the sediment (0.813) could be considered as reaching moderate pollution. In addition, the levels of these metals, H2O2, MDA and GSH content, antioxidant enzyme (CAT, SOD, GPx) activities as well as the level of metallothioneins (MT) mRNA in the tissues of S. constricta were also analyzed. The levels of Pb, Hg, Cd, Cr increased with increasing culturing time, and a higher level of these metals was accumulated in the visceral mass than in the foot. The levels of MDA and GSH, as well as the level of SOD activity in the viscera and foot of S. constricta increased with increasing metal accumulation. However, CAT and GPX activities, H2O2 level and the expression of MT initially increased and then decreased. This suggested that S. constricta might have the ability to control oxidative damage by triggering antioxidant defense in coordination with the metal sequestering response. The results also implied that toxic metal pollution should be taken into account when selecting the site to be used as an aquaculture farm. In addition, the visceral mass should be considered to be a good tissue for measuring the level of metal pollutants.

Introduction

Rapid economic development and ever-increasing human activities have led to severe pollution of the aquaculture industry by toxic metals. Contamination of the aquatic environment by toxic metals has received increased attention worldwide (Adami et al., 2002; Biruk et al., 2017; Dong et al., 2015; Tsangaris et al., 2010). These contaminants are of particular concern due to their non-degradability, bioaccumulation, and potential toxicity to living organisms (Dong et al., 2015; Kumaqai and Sacki, 1998; Li and Gao, 2014; Lavradas et al., 2016; Velez et al., 2015). Bivalves are extremely vulnerable to toxic metal contamination because they are benthic organisms and filter-feeders, and therefore, they have been regarded as indicator species in the assessment of environmental pollution (Adami et al., 2002; Bao et al., 2018; Chen et al., 2011; Chandurvelan et al., 2015; Lv et al., 2010; Mahmoud et al., 2010). Gupta and Singh (2011) also suggested that benthic mollusks play an important role as bio-indicators for trace metal pollution, making them ideal tools for global monitoring programs. A number of shellfishes in different parts of the coastal water of China have been exposed to toxic metals (Cd or Pb), and they include Tegillarca granosa in Zhejiang coast (Chen et al., 2011), Sinonovacula constricta and Arkshell in Dalian coastline (Pang et al., 2012), Mytilus edulis in Shandong coast (Du et al., 2009) and oyster (Crassostrea rivularis and C. gigas) in the coast of South China Sea (Wang et al., 2011). The razor clam, Sinonovacula constricta, is one of the four shellfishes of high economic values that are cultured in the coastal and estuarine environments in China, especially along the coast of Zhejiang. Sinonovacula constricta is also considered as an ecologically important bivalve (Ke and Wang, 2018). It is a filter feeder that lives mainly in muddy substrates in the lower intertidal and shallow sub-tidal areas, and therefore it is considered as an indicator of both acute and chronic contamination of the environment (Huang et al., 2007).

The accumulation of toxic metals in organisms will induce the production of reactive oxygen species (ROS), a major precursor of oxidative stress (Semedo et al., 2012) capable of causing oxidative damages, including significant inactivation of enzymes, protein degradation, DNA damage, and lipid peroxidation (El-Gazzar et al., 2014; Kanerva et al., 2012; Lai et al., 2011). Organisms are able to adapt to increased ROS production through enzymatic or nonenzymatic antioxidants (Cao et al., 2010; El-Gazzar et al., 2014; Lin et al., 2017). Antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidases (GPx) have specific functions in detoxifying the ROS generated by toxic metals in the tissues of invertebrates (Arojojoye et al., 2018). They have been extensively used as biomarkers of oxidative stress (Almeida et al., 2002; Javed et al., 2015; Lin et al., 2017; Semedo et al., 2012; Xia et al., 2016). Nonenzymatic antioxidant systems include glutathione (GSH) and metallothioneins (MT), which are considered to be important components involved in the protection of cells, acting both as metal chelating agents and as oxygen-radical scavengers (Farombi et al., 2007; Fang et al., 2010; Knapen et al., 2007; Lavradas et al., 2016). These proteins act to reduce the toxicity of the non-essential metals Cd and Pb (Lavradas et al., 2016). The production of MT within an organism can be induced by metals (Fang et al., 2010; Le et al., 2016; Min et al., 2016) and therefore, it is considered as a biomarker for monitoring the biological effects resulting from exposure to metals (Knapen et al., 2007; Lavradas et al., 2016). GSH is a central component in the multifaceted cellular detoxification system that constitutes an important mechanism in cellular protection against metal-induced formation of radical oxygen species, and the content of GSH is an important factor for measuring the antioxidant capacity of the organism (Delalande et al., 2010; Nair et al., 2015; Wang et al., 2013).

Previous reports have indicated that S. constricta can accumulate heavy metals and other pollutants from the environment to a high level within its tissue, a property that reflects the pollution of the water and sediment in its habitat (Ke and Wang, 2018; Pang et al., 2012). Despite the increasing toxic metal pollution in aquaculture farms in China, little is known about the accumulation of toxic metals and oxidative stress responses of razor clams during their growth in an aquaculture farm. It is therefore important to know how S. constricta copes with the toxicity presented by high levels of toxic metals in the environment. Wengyang is one of the important shellfish breeding bases in Zhejiang, and it has been subjected to a great deal of pollution brought about by the surrounding industries (Wang et al., 2015). Thus, the objective of this study was to investigate the concentrations of toxic metals (Hg, Pb, Cd and Cr) in the water and sediment taken from a shellfish farm in Wengyang as well as to determine the accumulated levels of these metals in the foot and visceral mass of S. constricta raised in the farm. The data obtained were then compared with the national standard levels of toxic metals permissible in seawater, sediment and seafood. Such information would be useful for evaluating the status of toxic metal pollution and for assessing whether the consumption of this species would bring potential health risks to human consumers. At the same time, the antioxidative response of S. constricta to heavy metals was also evaluated in order to explain the influences of toxic metal accumulation on oxidative damage and oxidative stress in cultured shellfish.

Section snippets

Sample collection and preparation

The clams (S. constricta) were randomly collected from a shellfish aquafarm in Wengyang, Zhejiang Province, China from May to Oct 2018. The shell size and weight of each clam were then recorded (Supplementary Table A1). Water samples were taken at a depth of about 8 cm below the surface while the sediment samples were collected at a depth of less than 10 cm below the surface. Both water and sediment samples were collected into separate polyethylene bottles. All samples were immediately

Evaluation of metal levels in the water and sediment

The concentrations of different metals in the water and sediments taken from the S. constricta aquaculture farm are shown in Table 1, Table 2, respectively. Except for Hg, all the other metals measured in the water fulfilled the second-class water quality standard (Table 1). The pollution index for Hg was 1.330, indicating moderate pollution. In May, September and October, the water was found to have light pollution, but from June to August, there appeared to be no pollution in the water (

Toxic metal pollution in aquatic ecosystem and factors affecting the bioaccumulation of metals in mollusks

The concentration of toxic metals in aquatic animals can be affected by several factors, such as the size, sex, age, sexual maturity stage, and food habits of the animals. In addition, the presence of other metal species, physical and chemical properties of the water and sediment, metallothioneins and other metal detoxifying proteins in the body of the animal can also have an effect (Fidan et al., 2008; Gupta and Singh, 2011; Li et al., 2008). Different metals can be accumulated in the various

CRediT authorship contribution statement

Mengxu Chen: Conceptualization, Methodology, Writing - original draft, Validation, Funding acquisition. Jiayi Zhou: Conceptualization, Methodology, Investigation, Writing - original draft, Formal analysis. Jinhuang Lin: Investigation, Methodology, Software, Formal analysis. Hongchao Tang: Methodology, Software, Resources, Funding acquisition. Yifei Shan: Resources, Methodology, Validation. Alan K. Chang: Writing - review & editing, Supervision. Xueping Ying: Conceptualization, Methodology,

Declaration of competing interest

There is no conflict of interest.

Acknowledgments

This study was supported by the Nature Science Foundation of Zhejiang Province, China under Grant number LY13C040003, LY18C030005 (to XPY), the National Student Innovation Training Project under Grant number DC2017072 (to CRQ) and JW201910351039 (to THC), the Student Innovation Training Project of Zhejiang province under Grant number 2018R429033 (to CJJ) and 2019R429021 (to CMX).

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