Morpho-physiological effects of ibuprofen on Scenedesmus rubescens

https://doi.org/10.1016/j.etap.2014.06.005Get rights and content

Highlights

  • First surveys on the effects of ibuprofen on Scenedesmus rubescens.

  • Growth curve, cell morphology, ultrastructure, and photosynthetic pigments.

  • Effects of ibuprofen produce large cytoplasmic inclusions.

  • It will be interesting to investigate the nature of these inclusions.

Abstract

The pollution of aquatic bodies by drugs is an emerging environmental problem, because of their extensive use in animal and human context. Ibuprofen, 2-[4-(2-methylpropyl)phenyl]propanoic acid, is the non-steroidal anti-inflammatory drug mainly present both in wastewater and in rivers and lakes in Europe. Since in literature there is little information about the effects of ibuprofen on microalgae, in this paper we presented the results on the effects of this molecule at different concentrations (62.5 μg L−1, 250 μg L−1 and 1000 μg L−1) on cultures of the freshwater microalga Scenedesmus rubescens (P.J.L. Dangeard) E. Kesslet et al. Ibuprofen effects on the alga were assayed at first through analyses of the growth curve. Moreover, analyses of cell morphology, ultrastructure, and photosynthetic pigments were additionally performed. The first negative effect of the drug was on the microalga growth, suggesting a drug action dose-dependent mechanism type, more evident at the concentration of 1000 μg L−1 ibuprofen and in the last phase of the growth curve. In support of this, following ibuprofen exposure, the cells exhibited morphological and ultrastructural alterations, mainly consisting in large cytoplasmic inclusions, probably of lipids and/or carotenoids. The decrease of chlorophyll amounts and, on the contrary, the increase of carotenoids were correlated with a stressful condition induced by drug.

Introduction

The presence of pharmaceutically active compounds (PACs) in the aquatic ecosystems, including both human and veterinary therapeutic agents and active ingredients in cosmetic products, has become a recent research topic. PACs are excreted through feces and urine as a mixture of metabolites and unchanged substances. Differently by some pollutants, PACs are continuously delivered in both aquatic and terrestrial ecosystems and they can also cause synergistic toxic effect in the presence of other compounds (Cleuvers, 2003). PACs can negatively affect both the chemical and biochemical processes that take place in aquatic and terrestrial ecosystems. Despite the large amount of analytical data, studies assessing the possible effects on aquatic photosynthetic organisms of detected PAC residues are scarce. Since photoautotrophic microalgae are the primary producers of essential nutrients in the aquatic ecosystems, the evaluation of toxicity of these compounds against these organisms is considered relevant. It is known that PACs elicit a biological response at very low levels and even small concentrations could have negative effects on target and non-target organisms. Toxic effects of PACs on algae are generally evaluated by toxicity tests based on growth inhibition. Moreover, other parameters could be modified such as pigment content that is considered reliable indicator of xenobiotic toxicity (Nie et al., 2009, Vannini et al., 2011), inhibition of photosynthesis (Escher et al., 2005) and metabolic processes related to growth (Pomati et al., 2004).

Among PACs non-steroidal anti-inflammatory drugs (NSAIDs), compounds like analgesic are included. Ibuprofen (IBU), belonging to NSAIDs, is a propanoic acid derivative, widely used as analgesic, antirheumatic and antipyretic drug. This compound is a persistent pollutant found in river water, because it is not destroyed in municipal water treatment stations (Fent et al., 2006). Ibuprofen has the tendency to bio-accumulate, inducing harmful effects in aquatic and terrestrial environments (Miège et al., 2009).

Detectable quantities of ibuprofen have been found in several typologies of European surface waters with concentrations ranging from ng L−1 to μg L−1 (Zuccato et al., 2000, Farre et al., 2001, Sanderson et al., 2003, Ashton et al., 2004, Pomati et al., 2004, Weigel et al., 2004). Ibuprofen was identified in sewage (≤3.35 μg L−1) and in river water (0.01–0.05 μg L−1). In very low doses (1–6 ng L−1) this drug could be detected even in drinking water (Stampf et al., 1996).

Some microalgal species belonging to the genus Scenedesmus, known for their ability to accumulate nutrients and heavy metals (Awasthi and Rai, 2005, Pellón et al., 2008, Ruiz-Marin and Mendoza-Espinosa, 2008), are used in bioremediation to remove pesticides (Guanzon et al., 1996, Cai et al., 2007, Dosnon-Olette et al., 2010). Scenedesmus obliquus (Turpin) Kützing was recommended for acute tests as ecological indicator since its sensitivity to chemicals (Ma et al., 2002). In many toxicology studies different species belonging to this genus have been used for evaluation of aquatic toxicity by many PACs, in particular: Scenedesmus dimorphus (Turpin) Kützing (strain UTEX 1648) for two veterinary sulfonamides (De Liguoro et al., 2010); S. obliquus (Turpin) Kützing for perfluorinated compounds (Liu et al., 2009), for the chemotherapeutic norfloxacin and for the food preservative butylated hydroxyanisole (Nie et al., 2009); Scenedesmus subspicatus Chodat for the antimicrobial triclosan (Orvos et al., 2002).

In this report we have examined the effects of IBU at different concentrations (62.5, 250, 1000 μg L−1) on cultures of Scenedesmus rubescens (P.J.L. Dangeard) E. Kesslet et al. evaluating at first algal growth responses. Moreover, analyses of cell morphology and ultrastructure, quantification of chlorophylls and carotenoids were carried out in order to provide information on the possible effects of IBU on morpho-physiology of this microalga and to evaluate the ecological risks of this drug.

Section snippets

IBU solution and algae

Ibuprofen (IBU) was purchased from Sigma–Aldrich (Milano, Italy). Due to its low solubility in water, IBU solution was prepared in ethanol to obtain a stock solution with a final concentration of 0.05%, stored at room temperature for the duration of the experiments. Working solutions were prepared by diluting the stock solution in MilliQ water.

S. rubescens (P.J.L. Dangeard) E. Kessler et al. (strain SAG 5.95) was purchased from Culture Collection of Algae at Goettingen University (SAG) and it

Growth and vitality of S. rubescens

The growth rates of S. rubescens after exposure to different concentration of IBU for 30 days were shown in Fig. 1. At the beginning of the experiments the optical density (O.D.) of the cultures maintained in all the experimental conditions was 0.1 (about 2 × 103 cells mL−1). The exponential phase began on the seventh day after inoculation. In this phase the control cultures had the same O.D. of that measured for cultures treated with IBU 62.5 μg L−1. The cultures treated with 250 and 1000 μg L−1 IBU

Discussion

The present work represents a first investigation on the morpho-physiological effects of ibuprofen on the freshwater microalga S. rubescens. The first negative effect of IBU was observed on the microalga growth. In particular the treatment with IBU 62.5 μg L−1 caused at first a stimulation of the growth both in the adaptation and in the exponential phase, then an inhibitory effect in the stationary phase. Differently the treatment with IBU 1000 μg L−1 showed clearly a growth inhibition already 3–4 

Conclusions

In the present study we have investigated the effects of IBU on the freshwater microalga S. rubescens. The results showed clearly a growth inhibition in the treatment with IBU 1000 μg L−1 already 3–4 days after inoculum until the stationary phase.

In support of this, following ibuprofen exposure, the cells exhibited morphological and ultrastructural alterations mainly consisting in large cytoplasmic inclusions, probably of lipids and/or carotenoids. Moreover the decrease of chlorophyll amounts and,

Conflict of interest

The authors declare that there are no conflicts of interest.

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References (41)

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