Chemical- and species-specific toxicity of nonylphenol and octylphenol to microalgae Chlorella pyrenoidosa and Scenedesmus obliquus

https://doi.org/10.1016/j.etap.2020.103517Get rights and content

Highlights

  • Toxicity of octylphenol (OP) to microalgae is lower than that of nonylphenol (NP).

  • Chlorella pyrenoidosa has better tolerant to NP stress than Scenedesmus obliquus.

  • S. obliquus has better tolerant to OP stress than C. pyrenoidosa.

  • Toxicity of NP and OP to two species of algae are chemical- and species-specific.

Abstract

As typical endocrine disrupters, nonylphenol (NP) and octylphenol (OP) are emerging pollutants that have attracted wide attention. This study investigated the toxicity effects of NP and OP on microalgae Chlorella pyrenoidosa and Scenedesmus obliquus, particularly on their growth inhibition, photosynthetic pigment, chlorophyll fluorescence, and superoxide dismutase and malondialdehyde levels. Results showed that the 96 h EC50 of NP and OP was 2.89 and 5.21 mg/L on C. pyrenoidosa, respectively, and 1.54 and 8.48 mg/L on S. obliquus, respectively. NP exerted a stronger inhibitory effect on cell growth, photosynthesis, and PSII activity, and it contributed more oxidative stress on C. pyrenoidosa than on S. obliquus. By contrast, OP exerted a stronger inhibitory effect on S. obliquus than on C. pyrenoidosa. Furthermore, the toxicity of OP to the tested microalgae was lower than that of NP. Principal component analysis (PCA) and Pearson’s correlation indicate that the accumulation of reactive oxygen species is the dominant mechanism of NP and OP cellular toxicity. The principal components of NP and OP affecting microalgae are distinct in the PCA plot, and different endocrine disrupters have varying chemical-specific influences on algal cells. This study confirmed that the toxicity of NP and OP to microalgae C. pyrenoidosa and S. obliquus is chemical- and species-specific. These findings should be considered when assessing the health risk of environmental pollution.

Introduction

As typical endocrine disrupters, nonylphenol (NP) and octylphenol (OP) have received broad attention because they negatively affect the endocrine function, normal metabolism, and reproductive system of human beings by interfering with the synthesis, secretion, and transportation of natural hormones (Chen et al., 2014; Ömeroğlu et al., 2015). Liu et al. (2013) reported that long-term NP and OP exposure seriously affect water ecosystem and human health as a result of their biological toxicity, endocrine disruption, persistence, and bioaccumulation.

NP and OP are widely used in industry and medicine, which is why they are frequently detected in different regions. The concentrations of NP and OP are 367–997 ng/g and 21–86 ng/g (dry weight), respectively, in sediments of the Beihai estuary (Xie et al., 2006) and 0.09–1.4 ng/L and 0.013–0.3 ng/L, respectively, in the North Sea of Germany (Heemken et al., 2001). Xu et al. (2006) reported that the concentration of NP in the Lanzhou basin of the Yellow River is 34.2–599 ng/L. Among the 164 tested groundwater samples from 23 European countries, 11 % contained NP, which is the most abundant industrial chemical in groundwater samples from Austria (Mao et al., 2012). In the USA, the average loading of NP to sewage sludge is 5510 metric tons, of which 3306 tons were introduced into the environment via land applications in 2011 (Lu and Gan, 2014). Diao et al. (2017) reported that the concentration of NP in the Pearl River estuary is 233.04–3352.86 ng/L. The dispersed endocrine disrupters are enriched by organisms, enter the food chain, and substantially affect aquatic environmental safety. She et al. (2012) reported that NP concentrations range from 2.6 μg/kg to 27.4 μg/kg in fruit and from 0.52 μg/kg to 35.82 μg/kg in vegetables, with the highest concentration of 72.5 μg/kg found in maize. Chen et al. (2014) found that the concentrations of NP and OP in the Pearl River estuary, China, are 7.23–21.98 and 1.81–5.87 μg/g in fish, respectively, and 0.21–37.02 and 1.13–4.83 μg/g in shellfish, respectively. Studying the ecotoxicity and risk assessment of NP and OP on aquatic environmental safety, food chain, and human health is of great ecological importance.

As a low-trophic-level aquatic organism, microalgae are the base of aquatic food chain and are widely selected as biological models for ecotoxicology assays (Zhang et al., 2017; Harris, 1986), which is why they are extensively used in studying the effects of endocrine disrupters (Zhu et al., 2019). Hou et al. (2016) found that the 96 h median effective concentration (EC50) of NP to Chlorella pyrenoidosa is 3.13 mg/L, and its 48 h median lethal concentration (LC50) to Daphnia magna is 37.4 μg/L. Ward and Boeri (1990) reported that NP exposure remarkably inhibits Selenastrum capricornutum growth with a 96 h EC50 of 0.979 mg/L. Correa-Reyes et al. (2007) investigated the toxic effects of NP on Isochrysis galbana and found that NP concentrations above 1 mg/L inhibit algal photosynthesis. Furthermore, Cahyanurani et al. (2017) reported that the 96 h EC50 of OP on Ceratophyllum demersum is 0.939 mg/L. Gao et al. (2017) found that exposure to 1 mg/L NP substantially changes the antioxidant system of Chlorella vulgaris, including superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD). Although previous research has proven that endocrine disrupters will affect algal growth, a comparatively systematic and complete system for comparing and assessing the different physiological and biochemical responses of green microalgae to NP and OP, including algal growth, photosynthetic activity, and oxidative stress, is lacking. For instance, Perron and Juneau (2011) reported that the photosynthetic activity of Chlamydomonas reinhardtii is substantially inhibited by NP and OP when their concentrations range from 0.1 μg/mL to 5 μg/mL, whereas the present research is limited to the response of algal photosynthetic activity to NP and OP.

In this study, green microalgae C. pyrenoidosa and Scenedesmus obliquus were employed for the toxicity test due to their excellent characteristics of fast growth cycle, easy observation, and sensitivity to toxic pollutants (Liu and Xiong, 2009). This work aims to deepen the understanding of the acute toxicity effect of NP and OP on microalgae C. pyrenoidosa and S. obliquus by determining algal growth inhibition, chlorophyll fluorescence, photosynthetic pigment, and SOD and malondialdehyde (MDA) levels. The results provide a theoretical basis for a deep and comprehensive understanding of the toxicity of endocrine disrupters NP and OP on aquatic organisms, food chain, and human health.

Section snippets

Test chemicals

NP and OP were purchased from Kayon, Shanghai, China (> 99.5 %). They were dissolved in a solution with the aid of dimethyl sulfoxide (DMSO), which is commonly known as an excellent solubilizer. The required concentrations of NP and OP were diluted using the DMSO. The influence of the solubilizer on algal growth was evaluated by adding it or not adding it. Therefore, the concentration of solubilizer in the solution was controlled at 0.03 % (v/v).

Algae cultivation

The algal strains C. pyrenoidosa and S. obliquus

Effect of NP on the growth of C. Pyrenoidosa and S. Obliquus

Fig. 1 presents the C. pyrenoidosa and S. obliquus growth curves under NP and OP exposure. Varying cell growth was observed between C. pyrenoidosa and S. obliquus exposed to NP and OP under the same concentrations during the treatment period. As shown in Fig. 1A, the growth of C. pyrenoidosa was slightly stimulated at NP low concentrations (0.5 mg/L) and inhibited when the NP concentration was equal to or higher than 1 mg/L. The algal growth rapidly decreased and exhibited the lowest values at

Toxicity of NP and OP to C. pyrenoidosa and S. Obliquus

Our study used EC50 to evaluate the toxicity of NP and OP to microalgae C. pyrenoidosa and S. obliquus. Low EC50 values correspond to high toxicity. The toxicity results for C. pyrenoidosa (96 h EC50 of 2.89 and 5.21 mg/L for NP and OP, respectively) and S. obliquus (96 h EC50 of 1.54 and 8.48 mg/L for NP and OP, respectively) were partly inconsistent with previous findings. For instance, the 96 h EC50 of NP ranges from 0.87 mg/L to 0.98 mg/L on Selenanstrum subspicatus (Hense et al., 2005),

Conclusions

The toxicities of NP and OP on microalgae C. pyrenoidosa and S. Obliquus were investigated. Growth inhibition, photosynthetic pigment, chlorophyll fluorescence, SOD, and MDA were measured and used to determine the toxicity effects. The results indicate that the growth inhibition, photosynthetic pigments, and PSII activity of S. obliquus were more sensitive to NP-induced oxidative stress than those of C. pyrenoidosa, whereas an opposite conclusion was drawn under OP stress. Furthermore, the

Conflict of interest

The authors declare no conflict of interest.

CRediT authorship contribution statement

Wenfeng Yang: Methodology, Formal analysis, Investigation, Writing - original draft, Visualization, Writing - review & editing. Xinxin Gao: Data curation, Formal analysis, Investigation. Yixiao Wu: Validation, Writing - review & editing, Project administration. Liang Wan: Validation, Writing - review & editing, Project administration. Chongyang Lu: Data curation, Formal analysis, Investigation. Jiayi Huang: Visualization, Project administration. Houjiang Chen: Visualization, Project

Acknowledgments

This work was supported by the National Natural Science Foundation of China (51869006), Jiangxi Natural Science Foundation of China (20171BAB216050), Water Science and Technology Fund of Jiangxi Province in China (KT201412, KT201607, KT201702, and 201821ZDKT09).

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