Causes and mechanisms on the toxicity of layered double hydroxide (LDH) to green algae Scenedesmus quadricauda

Highlights

• The growth of S. quadricauda was significantly inhibited by LDH.

• The light and dark 24 h EC50s for algae by LDH was 10 and 25 mg L⁻¹, respectively.

• LDH induced changes in algal photosynthesis, oxidative stress and lipid peroxidation.

• Shading effect, agglomeration and oxidative stress mainly contributed such toxicity.

Abstract

Layered double hydroxides (LDHs) are widely used nanomaterials in industrial catalysis, pharmaceuticals, and environmental remediation, and may pose potential negative effects in the aquatic environment. However, little information is available on their toxicity to aquatic organisms. In this study, toxicity of LDH to a typical freshwater green algae Scenedesmus quadricauda was systematically investigated and the underlying mechanisms were elucidated. The growth of S. quadricauda was significantly inhibited by LDH at 72 h with a half maximal effective concentration (EC₅₀) and lowest observed effect concentration (LOEC) of 10.0 and 1.5 mg L⁻¹, respectively. Shading effect was observed, and the photosynthetic activity and cellular chlorophyll production were also severely suppressed by LDH. LDH also enhanced the reactive oxygen species production from S. quadricauda and lipid peroxidation in algal cells. Such algal toxicity of LDH might be mainly induced by the shading effect, agglomeration and physical interactions, and oxidative stress. The agglomeration and physical interactions contributed more to the algal toxicity at 72 h-EC₅₀ LDH concentrations. The results from the present study provided new insights and a better understanding of the environmental behavior and adverse effects of LDHs in the surface waters.

Introduction

Nanomaterials (NMs) have attracted a great deal of interest due to their unique optical, electronic and magnetic characteristics as compared to their bulk counterparts (Zhu et al. 2009). Hydrotalcite or hydrotalcite-like layered double hydroxide (LDH) nanoparticles are a family of inorganic lamellar materials with a general formula of [M_1-x²⁺M_x³⁺(OH)₂]^x+[A_x/n]^n-·mH₂O, where M²⁺ is a divalent cation, M³⁺ a trivalent metal cation, x the molar ratio of the trivalent cation [M³⁺/(M²⁺ +M³⁺)], and A^n–a gallery anion with charge n (Sideris et al. 2008). Layered double hydroxides have received wide-spread attention in the application of catalysis (Zhao et al. 2007), polymer nanocomposites (Manzi-Nshuti et al. 2009), pharmaceuticals (Ladewig et al. 2009; Choi and Choy 2011), and sensors (Han et al. 2011). Additionally, as environmental pollution has emerged as an important issue in the recent decades, interests in using LDHs to remove environmental contaminants (e.g., heavy metal, pesticides and polycyclic aromatic hydrocarbons) are growing (Ambrogi et al. 2009; Koilraj et al. 2016; Li et al. 2016; Peligro et al. 2016). The rapidly increasing use of LDHs may lead to the occurrence of LDHs in the effluents and the freshwater systems receiving effluent discharge, which has not been reported so far. It may raise ecological and human health concerns as LDHs can pose toxic effects on non-target organisms. A considerable amount of literature has been published on the toxicity effects of organic NMs, such as fullerenes and carbon nanotubes (Sergio et al. 2013; Ging et al. 2014) to organisms including algae (Schwab et al. 2011; Long et al. 2012), zooplankton (Zhu et al. 2006; Zhu et al. 2009), fish (Kim et al. 2012; Myer et al. 2017) and human cells (Hu et al., 2010; Larner et al. 2017). However, studies on the toxicity of inorganic LDHs to aquatic organisms are few.

Algae are one of the most common species in natural waters, and are commonly used as model organisms in regulatory testing and ecotoxicological studies (Zhang et al. 2013; Zhang et al. 2015; Ding et al. 2017a). As environmental concern over the presence of NMs in the environment and their potential subtle effects on non-target organisms is increasing, many studies have been conducted to examine the potential effects of NMs to algae and the associated mechanisms. For example, NMs (e.g., carbon nanotubes, silver nanoparticles) could generate reactive oxygen species (ROS) to pose a variety of interrelated effects on algae (e.g., Pseudokirchneriella subcapitata), such as lipid peroxidation and DNA damage (Nel et al. 2006; Ma et al. 2010). In addition, nanoparticle aggregates may attach to and/or entrap algal cells, reducing available light needed for photosynthesis and restricting other cellular functions. This phenomenon is defined as shading effect (Aruoja et al. 2009; Evers, 1991; Li et al. 2015; Navarro et al. 2008; Petersen et al. 2014; Wright et al. 2018). For example, Long et al. (2012) reported that multi-layered carbon nanotubes (MWCNTs) showed shading effects on algal growth and accounted for approximately 25% of algal growth inhibition to Chlorella sp. The agglomeration of NMs and algae could also lead to the algal growth inhibition. For instance, Zhang et al. (2015) reported that MWCNTs could agglomerate with a green algae (Chlorella pyrenoidosa) and lead to damage in the organelles. The electrostatic attraction between nanoparticle and the organisms could also lead to the heteroagglomeration (Thill et al. 2006). In addition to these toxic causes, the toxicity of NMs or NPs to algal cells could be caused by a number of other factors, such as physiological changes, the blocking of nutrient uptake, and the heavy metal release from NPs. For instance, Meyer et al. (2010) found that AgNPs exerted sublethal toxicity to Caenorhabditis elegans at low concentrations in the low mg L⁻¹ levels, which was mediated by the release of ionic silver (Ag⁺). However, to date no studies have focused on the toxicity of LDHs to algae, and the potential toxicity mechanism of LDHs to algae is still unclear.

The specific objectives of this study were (1) to evaluate the toxicity of Cu-Mg-Fe LDHs (LDH) to a typical freshwater green algae S. quadricauda, (2) to explore the possible toxicity mechanisms of LDH to algae, and (3) to provide information for better assessing biological behavior and ecological risks of LDHs in aquatic environments.