Toxic impacts induced by Sodium lauryl sulfate in Mytilus galloprovincialis

https://doi.org/10.1016/j.cbpa.2020.110656Get rights and content

Highlights

  • Mussels bioaccumulated SLS, with lower BCF values at the highest exposure concentration.

  • Respiration rate strongly decreased in contaminated mussels.

  • Metabolic capacity was increased at intermediate concentrations.

  • Defense mechanisms presented limited activity, although redox balance was maintained.

  • Cellular damage was observed at the highest exposure concentration.

Abstract

Pharmaceuticals and personal care products (PPCPs) are continuously dispersed into the environment, as a result of human and veterinary use, reaching aquatic coastal systems and inhabiting organisms. However, information regarding to toxic effects of these compounds towards marine invertebrates is still scarce, especially in what regards to metabolic capacity and oxidative status alterations induced in bivalves after chronic exposure. In the present study, the toxic impacts of Sodium lauryl sulfate (SLS), an anionic surfactant widely used as an emulsifying cleaning agent in household and cosmetics, were evaluated in the mussel Mytilus galloprovincialis, after exposure for 28 days to different concentrations (0.0; 0.5; 1.0; 2.0 and 4.0 mg/L). For this, effects on mussels respitation rate, metabolic capacity and oxidative status were evaluated. The obtained results indicate a significant decrease on mussel's respiration rate after exposure to different SLS concentrations, an alteration that was accompanied by a decrease of bioconcentration factor along the increasing exposure gradient, especially at the highest exposure concentration. Nonetheless, the amount of SLS accumulated in organisms originated alterations in mussel's metabolic performance, with higher metabolic capacity up to 2.0 mg/L followed by a decrease at the highest tested concentration (4.0 mg/L). Mussels exposed to SLS revealed limited antioxidant defense mecanhisms but cellular damage was only observed at the highest exposure concentration (4.0 mg/L). In fact, up to 2.0 mg/L of SLS limited toxic impacts were observed, namely in terms of oxidative stress and redox balance. However, since mussel's respiration rate was greatly affected by the presence of SLS, the present study may highlight the potential threat of SLS towards marine bivalves, limiting their filtration capacity and, thus, affecting their global physiological development (including growth and reproduction) and ultimely their biochemical performance (afecting their defense capacity towards stressful conditons).

Introduction

Currently, a vast diversity of substances reaches the aquatic environment, including newly developed chemicals, identified as contaminants of emerging concern (CECs) (Ebele et al., 2017; Lorenzo et al., 2018; Richardson and Ternes, 2014, Richardson and Ternes, 2018; Richardson and Kimura, 2016), posing at risk a wide diversity of marine biological resources with ecological and economical relevance. For decades, classical pollutants (as trace metals) have been monitored worldwide, but regarding CECs information on their environmental concentrations has recently been a topic of concern. Nevertheless, although for some of the CECs information has increased on the last decade, still scarce data is available on the concentration levels of these substances for the majority of the coastal systems worldwide, and less is known on their impacts towards inhabiting organims.

Among the most worldwide dispersed CECs are Personal care products (PCPs), with increasing information on their occurrence and, as a consequence, with a high number of these substances already included in the Watch List adopted by European Union (EU). Although impacts towards marine species were already identified, still scarce information exists on their concentrations and toxic impacts towards non-target organisms, and in particular in what regards to marine invertebrate species (see for review: Brausch and Rand, 2011; Montesdeoca-Esponda et al., 2018). PCPs represent a group of substances that includes surfactants, foaming agents, wetting agents, detergents, emulsifier solubilizers and antimicrobials. As a consequence of their properties, including the capacity to lower the surface tension of a liquid, allowing easier spreading, PCPs are used in a wide variety of detergents and cosmetics (Daughton and Ternes, 1999; Loraine and Pettigrove, 2006; Olkowska et al., 2015; Ramos et al., 2015; Sharma et al., 2009; Teo et al., 2015). Many of these compounds are not susceptible to biodegradation, being eventually discharged into receiving waters in their pareting forms. Also, metabolic conjugates can be converted back into their free parenting forms. In addition, many of these PCPs and their metabolites have bioaccumulation potential and/or are bioactive substances that can put living organisms at risk (Peck, 2006; Mackay and Barnthouse, 2010; Biel-maeso et al., 2018).

Among the most widely used PCPs is Sodium lauryl sulfate (SLS), also identified as Sodium dodecyl sulfate (SDS), an anionic surfactant used as an emulsifying cleaning agent in household detergents such as dishwashing soaps, but also in cosmetics, including toothpastes, shampoos, shaving foams, hand soap, facial cleanser, body wash, and shaving creams (Chaturvedi and Kumar, 2010). In the pharmaceutical industry, SLS is used as an agent to improve the absorption of chemicals through the skin, gastrointestinal mucosa and other mucous membranes (Hauthal, 1992). In the industry SLS can be used in fire fighting products, detergents and soaps, as flocculant and de-inking agent (among others, Chaturvedi and Kumar, 2010). The concentration of SLS found in these products may vary depending on the product and the manufacturer, with biodegradation of SLS ranging from 45% to 95% within 24 h (Fatma et al., 2015). Nevertheless, the continuous introduction of SLS into the environment through domestic and industrial waste discharges result into high concentrations of this pollutant (Cserháti et al., 2002). Anionic detergents, as SLS, have a strong tendency to bind to the lipid component of the membrane, with high concentrations being responsible for alterations at the cellular level (Brunelli et al., 2008). Although impacts of SLS were already demonstrated in aquatic organisms, still scarce information is available regarding molecular mechanisms of surfactants toxicity, and in particular in what regards to SLS (Freitas and Rocha, 2012; Messina et al., 2014; Nunes et al., 2005, Nunes et al., 2008; Rocha et al., 2007). However, recent studies pointed out that toxic effects of SLS may be related to the disruption of the osmotic balance and induction of oxidative stress, as demonstrated by Messina et al. (2014) and Nunes et al. (2008). It has been shown that oxidative stress is induced by a wide variety of pollutants, with published studies revealing the impacts of a wide diversity of pharmaceuticals and PCPs (PPCPs), including surfactants, on marine species oxidative stress performance (among others, Almeida et al., 2015; Freitas et al., 2019; Messina et al., 2014; Nunes et al., 2005; Nunes et al., 2008). Among the biomarkers most widely measured as a consequence of PPCPs exposure are: i) lipid peroxidation (LPO), which reveal injuries at a cellular level caused by the overproduction of reactive species (ROS); ii) activity of antioxidant enzymes, corresponding to organisms defense mechanisms to eliminate the excess of ROS; iii) content of reduced glutathione (GSH) that is considered to be one of the most important scavengers of ROS and its ratio with oxidised glutathione (GSSG) may be used as a marker of oxidative stress. Besides oxidative stress related biomarkers, measurements of organisms' metabolic capacity and energy reserves have been used to assess the impacts of different stressful conditions in marine organisms, namely bivalves. Commonly used as a proxy of the organism metabolism, the electron transport system (ETS) activity revealed to be an efficient marker to identify the impacts resulting from pollutants. When under stressful conditions, such as in the presence of pollutants, bivalves are able to change their metabolic activity to cope with the stress induced (Coppola et al., 2017, Coppola et al., 2018; Fanslow et al., 2001; Freitas et al., 2017). In what regards to energy reserves, different studies demonstrated that organisms have the capacity to control the use of glycogen or lipids according to the stress level that they are subjected to (Anacleto et al., 2014; Coppola et al., 2017, Coppola et al., 2018; Duquesne et al., 2004; Freitas et al., 2019; Timmins-Schiffman et al., 2014).

Therefore, the present study aimed to assess the effects induced in the mussel species Mytilus galloprovincialis after a chronic exposure (28 days) to SLS (0.00–4.00 mg/L). For this, biochemical markers related with organisms metabolism and oxidative status were evaluated.

Section snippets

Experimental setup

Mytilus galloprovincialis specimens were collected in the Ria de Aveiro (northwest Atlantic coast of Portugal), in February 2018. To avoid the effect of body weight on biological responses and SLS accumulation, organisms with similar weight (0.45 ± 0.11 g dry weight, DW; condition index 10.64 ± 1.92) were selected.

After arriving to the laboratory organisms were acclimated for fifteen days prior to exposure, in separate aquaria (20 L each). Aquaria were set up by the addition of artificial sea

Sodium dodecyl sulfate quantification in water and mussel's tissues

For each tested concentration, SLS values obtained in water samples colected every week immediately after spiking revealed no significant differences among weeks. Concentrations measured each week showed significant differences among SLS tested concentrations, with nominal concentrations close to the measured ones, validating the spiking process (Table 1).

Concentrations of SLS measured in mussels tissues increased with the increasing SLS exposure concentration, with significantly lower values

Discussion

The exposure of an organism to xenobiotics can lead to alterations in cell homeostasis, probably causing oxidative stress (Hoarau et al., 2004; Livingstone, 2003). In the case of SLS, previous studies already demonstrated the capacity of this compound to stimulated intracellular ROS levels (Mizutani et al., 2016), which will result into oxidative stress. Nevertheless, pollutants may also cause alterations on organism's metabolism (among others, Coppola et al., 2019; Cruz et al., 2016; Freitas

Conclusion

As a result of increasing application of PPCPs and the consequent release in aquatic ecosystems, the present study provides relevant data on the potential risk of SLS in the aquatic environment and inhabiting organisms, namely in Mytilus galloprovincialis. Nevertheless, the study of SLS toxicity may be lacking in ecological importance since in the environment different conditions can act in combination modifying the behavior and toxicity of the different PPCPs. Therefore, future studies should

Declaration of Competing Interest

None.

Acknowledgments

Francesca Coppola benefited from a PhD grants (SFRH/BD/118582/2016) given by the National Funds through the Portuguese Science Foundation (FCT), supported by FSE and Programa Operacional Capital Humano (POCH) e da União Europeia. Silvana Costa benefited from a BSc grant on behalf of the project ASARISAFE ASARISAFE - Safety and sustainable management of valuable clam product in Portugal and China NSFC/0001/2016, funded by Projetos conjuntos de Investigação Científica e Desenvolvimento

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