Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology
Oxidative stress in benthic oligochaete worm, Tubifex tubifex induced by sublethal exposure to a cationic surfactant cetylpyridinium chloride and an anionic surfactant sodium dodecyl sulfate
Graphical abstract
Introduction
Nowadays water pollution is becoming a substantial threat to global ecosystems (Mareddy 2017). The significant and potential pollution sources for surface and groundwater in many advanced countries are household and industrial wastewaters (Jardak et al. 2016). The outrageously high utilization of detergents by households for washing and cleaning purposes and the subsequent drainage of water in localized water bodies has exacerbated imbalances in the aquatic ecosystem and has given rise to substantial public attention worldwide in recent decades (Goel and Kaur 2012). One of the chief constituents of popular household detergents, used for washing, cleaning, and bathing, are surfactants (Steber 2007). Surfactants are a diversified group of chemical compounds with hydrophobic and hydrophilic sites and are crucial for the solubilization of organic contaminants (Lechuga et al. 2016). The inordinate discharge of surfactant into the aquatic environment causes considerable damage to biological systems (Rosety-Rodríguez et al. 2002). The global consumption of surfactants increases every year and its global production is expected to reach US$ 28.8 billion until 2023, which attests to its importance in daily life (Kaczerewska et al. 2020). Though most surfactants are degradable, their consistent use and incongruous disposal in surface waters lead to persistent occurrence within the aquatic ecosystem (Mustapha and Bawa-Allah 2020). Many surfactants exert toxicity by affixing them to macromolecules in a biological system and modifying their efficacious functioning (Ivanković and Hrenović 2010). The surfactants are grouped comprehensively into anionic, nonionic, cationic, and zwitterionic surfactants (Jackson et al. 2016). Approximately 65% of total production conforms to compounds classified as anionic surfactants, while the second and third places in global production correspond to cationic and nonionic surfactants, respectively (Olkowska et al. 2014). The most frequently used active ingredients in household cleaners and laundry detergents are anionic and cationic surfactants (Ranji et al. 2019). The most commercially used anionic surfactants especially utilized as household products, cosmetics, and laundry purposes are sodium dodecyl sulfate (SDS) whereas the most abundant and widely utilized cationic surfactant is cetylpyridinium chloride (CPC) which is basically a quaternary ammonium compound explicitly utilized in mouthwashes for obviation of dental plaques and periodontitis (Bondi et al. 2015; Costa et al. 2013). Several studies have documented the toxic effects of SDS and CPC in several fish species as well as in rats, mice, and amphibians (Barbieri et al. 1998; Lin et al. 1991; Park et al. 2016; Rocha et al. 2007).
Tubifex tubifex is an aquatic oligochaete worm that mainly resides in freshwater sediments (Milbrink 1987). It is an important bioindicator species having a cosmopolitan distribution, tolerant to a diverse array of environmental variables, easily culturable in laboratory conditions and serves as a source of healthy food to fishes, especially the freshwater ornamental ones (Chapman 2001; Yildiz 2016).
Biomarkers are the biochemical designator of changes at the biochemical and physiological levels of an organism (Strimbu and Tavel 2010). The toxicity of pollutants contributes to the production of reactive oxygen species (ROS) and the induction of oxidative stress (Mittal et al. 2014). These ROS are capable of inflicting lipid peroxidation (LPO) via the formation of malondialdehyde (MDA) as well as induce substantial damage to biomolecules like DNA, protein, and membranes through oxidative stress (Monteiro et al. 2006). Oxidative stress occurs when an imbalance emerges between the production of these ROS and their neutralization process with antioxidant enzymes like catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GPx), glutathione S-transferase (GST), and reduced glutathione (GSH) (Raibeemol and Chitra 2018). Thus, the evaluation of alterations in the activity of antioxidant enzymes is indeed a productive and effective method for the assessment of oxidative stress and therefore could serve as a potential tool in aquatic toxicology (Kumari et al. 2014). Various studies have been carried out on alterations of oxidative stress in Tubifex tubifex exposed to pesticides (Mosleh et al., 2003, Mosleh et al., 2005, Mosleh et al., 2006, Mosleh et al., 2007, Mosleh et al., 2014; Paris-Palacios et al. 2010). However, evidence regarding the toxic effect of surfactant on alterations of oxidative stress enzymes in these worms is extremely meager.
The authentic and realistic assessment of pollutant toxicity on aquatic organisms by individual biomarkers is not possible and ergo, it is prevalently recommended to use the combined biomarker study to comprehend the response of an organism to toxic substances (Sanchez et al. 2012). The integrated biomarker response (IBR) thus consequently provides a holistic approach, consolidating all biomarker responses, and plays a crucial role in evaluating pollutant toxicity. (Beliaeff and Burgeot 2002; Serafim et al. 2012).
Therefore, the study aims to evaluate the in vivo toxic effects of SDS and CPC on Tubifex tubifex during sublethal exposure by visually examining the alterations in oxidative stress biomarkers using sublethal concentrations. Moreover integrated biomarker response (IBR) is employed to gain a superior comprehension of the toxic effects of CPC and SDS on Tubifex tubifex.
Section snippets
Experimental organism
Tubifex tubifex (Phylum: Annelida, Class: Clitellata, Order: Oligochaeta and Family: Naididae) were collected from a local aquarium shop in Burdwan, West Bengal, India and acclimatized in a stock aquarium for a period of 24 h in unchlorinated water with continuous aeration using Venus Aqua Ap-208 aerator (temperature 27.9 ± 0.4 °C, pH 7.5 ± 0.3, free CO2 16.6 ± 0.6 mg L−1, dissolved oxygen 6.5 ± 0.4 mg L−1, total alkalinity 187 ± 7.6 mg L−1 as CaCO3, hardness 121 ± 4.2 mg L−1 as CaCO3).
Chemicals
The
Result
The effects of CPC and SDS on oxidative stress parameters in Tubifex tubifex are depicted in Fig. 1, Fig. 2.
Discussion
Antioxidant enzymes are insightful biomarkers of oxidative stress than can detoxify and annihilate reactive oxygen species (ROS) and other prooxidants from the cells under normal circumstance (Ajima et al. 2017; Iheanacho and Odo 2020). Among the antioxidant enzymes, SOD (superoxide dismutase) is one of the enzymes that induce major defense mechanisms against oxidative stress in the cell by converting reactive oxygen radical to hydrogen peroxide (Kim et al., 2017, Kim et al., 2019). In the
Conclusion
The results of this study revealed that, with the integration of surfactant CPC and SDS, Tubifex tubifex exhibited alterations in oxidative stress parameters. Consequently, the current results on the toxicity of CPC and SDS to Tubifex tubifex demonstrate that oxidative stress biomarkers are an important tool for evaluating the intricate health status of aquatic organisms, including sediment macroinvertebrates in a stressed condition. However further studies are required to extract the toxic
Ethical approval
This article contains no animal studies by any of the authors requiring endorsement from the ethical committee. In fact, according to the current regulatory studies, no ethical authorization is required for invertebrates like Tubifex tubifex.
Declaration of competing interest
The authors declare that they have no conflict of interest.
Acknowledgement
The authors are thankful to the Department of Zoology, The University of Burdwan, West Bengal, India for providing all sorts of laboratory facilities to conduct this research.
References (73)
- et al.
Neurotoxic effects, molecular responses and oxidative stress biomarkers in Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) exposed to verapamil
Comp. Biochem. Physiol. Part - C Toxicol. Pharmacol.
(2017) - et al.
Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples
Methods Enzymol.
(1981) - et al.
Melatonin ameliorates bisphenol A-induced biochemical toxicity in testicular mitochondria of mouse
Food Chem. Toxicol.
(2011) - et al.
Superoxide dismutase: improved assays and an assay applicable to acrylamide gels
Anal. Biochem.
(1971) - et al.
Article: a spectrophotometric method for measuring the breakdown of hydrogen peroxide
J. Biol. Chem.
(1952) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Anal. Biochem.
(1976)- et al.
Indices for the assessment of environmental pollution of the Baltic Sea coasts: integrated assessment of a multi-biomarker approach
Mar. Pollut. Bull.
(2006) - et al.
Integrative assessment of biomarker responses in teleostean fishes exposed to glyphosate-based herbicide (Excel Mera 71)
Emerg. Contam.
(2016) - et al.
SOD and catalase inactivation by singlet oxygen and peroxyl radicals
Free Radic. Biol. Med.
(1996) - et al.
Biomarkers and energy reserves in the isopod Porcellionides pruinosus: the effects of long-term exposure to dimethoate
Sci. Total Environ.
(2015)
Glutathione S transferases. The first enzymatic step in mercapturic acid formation
J. Biol. Chem.
Toxic effects on hematological parameters and oxidative stress in juvenile olive flounder, Paralichthys olivaceus exposed to waterborne zinc
Aquac. Reports
Glutathione peroxidase activity in selenium-deficient rat liver
Biochem. Biophys. Res. Commun.
Acute toxicity of anionic and non-ionic surfactants to aquatic organisms
Ecotoxicol. Environ. Saf.
Effects of 1-methyl-3-octylimidazolium bromide on the anti-oxidant system of earthworm
Chemosphere
Use of hematological and plasma biochemical parameters to assess the chronic effects of a fungicide propiconazole on a freshwater teleost
Chemosphere
Acute inhalation toxicity of cetylpyridinium chloride
Food Chem. Toxicol.
The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish
Impacts on water environment
Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion)
Comp. Biochem. Physiol. - C Toxicol. Pharmacol.
Metallothioneins induction and antioxidative response in aquatic worms Tubifex tubifex (Oligochaeta, Tubificidae) exposed to copper
Chemosphere
Effects of chitosan on oxidative stress and metallothioneins in aquatic worm Tubifex tubifex (Oligochaeta, Tubificidae)
Chemosphere
Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction
Anal. Biochem.
Toxic effects and bioaccumulation of the herbicide isoproturon in Tubifex tubifex (Oligocheate, Tubificidae): a study of significance of autotomy and its utility as a biomarker
Aquat. Toxicol.
Developmental and acute toxicity of cetylpyridinium chloride in Bombina orientalis (Amphibia: Anura)
Aquat. Toxicol.
Effects of anionic surfactant and salinity on the bioenergetics of juveniles of Centropomus parallelus (Poey)
Ecotoxicol. Environ. Saf.
Morpho-histochemical changes in the gills of turbot, Scophthalmus maximus L., induced by sodium dodecyl sulfate
Ecotoxicol. Environ. Saf.
Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems
Ecol. Indic.
Oxidative injury caused by individual and combined exposure of neonicotinoid, organophosphate and herbicide in zebrafish
Toxicol. Reports
The ecotoxicity of cleaning product ingredients
Ecotoxicological effects of a veterinary food additive, copper sulphate, on antioxidant enzymes and mRNA expression in earthworms
Environ. Toxicol. Pharmacol.
The effect of SDS, sodium dodecyl sulfate, on the metabolism and swimming capacity of Cyprinus carpio
Rev. Bras. Biol.
Integrated biomarker response: A useful tool for ecological risk assessment
Acute toxicity and ethological responses of oligochaete worm Tubifex tubifex (Muller) exposed to a cationic surfactant cetylpyridinium chloride
Int. J. Sci. Res. Biol. Sci.
Sodium dodecyl sulphate induced acute toxicity and ethological responses to oligochaete worm Tubifex tubifex (Muller)
Res. Rev. Int. J. Multidiscip.
Human and environmental toxicity of sodium lauryl sulfate (SLS): evidence for safe use in household cleaning products
Environ. Health Insights
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