Elsevier

Water Research

Volume 177, 15 June 2020, 115786
Water Research

Influences of the micropollutant erythromycin on cyanobacteria treatment with potassium permanganate

https://doi.org/10.1016/j.watres.2020.115786Get rights and content

Highlights

  • Cyanobacteria pre-exposed to erythromycin were less effectively treated by KMnO4.

  • The expression of mcyB and mcyH was downregulated by a high dose of erythromycin.

  • High dose of erythromycin reduced the efficiency of KMnO4 in MC oxidation.

Abstract

Cyanobacteria blooms and micropollutants (e.g., antibiotics) in source waters are two increasing environmental issues worldwide. This study hypothesized that the coexisting antibiotics may possibly alter the efficiency of water treatment processes through affecting the physiological and biochemical characteristics of cyanobacterial cells. A toxic strain of Microcystis aeruginosa was exposed to the common antibiotic erythromycin (ERY) at environmentally relevant concentrations; then, samples were collected on days 1, 4 and 6 to assess the efficiency of potassium permanganate (KMnO4) in cyanobacteria oxidation. The percentage of intact cells remained constant after treatment with 2 mg L−1 KMnO4 in M. aeruginosa samples dosed with 0–5.0 μg L−1 ERY. Although 6 mg L−1 KMnO4 could damage cyanobacterial cells, its ability was considerably reduced as the concentrations of ERY increased. KMnO4 oxidation degraded the intracellular microcystins (MCs) in all of the cyanobacterial samples, even the samples with intact cells, possibly resulting from the stimulation of intracellular reactive oxygen species (ROS). The highest amounts of total MCs remained after oxidation with 2 and 6 mg L−1 KMnO4 in 0.2 μg L−1 ERY-treated cyanobacterial samples, which may be due to large amounts of MC production. The 5.0 μg L−1 ERY inhibited the growth of cyanobacterial cells and downregulated the expression of the MC synthesis gene (mcyB), which resulted in the lowest amounts of total MCs. However, it led to the highest concentration (4.6 μg L−1) of extracellular MCs after treatment with 2 mg L−1 KMnO4 for 300 min. Generally, this study indicates that the effectiveness of KMnO4 oxidation in cyanobacteria treatment decreased when the concentration of ERY increased. Hence, the possible risks caused by the coexistence of cyanobacteria and antibiotics, such as reduced efficiency of water treatment processes in cyanobacteria inactivation and degradation of the dissolved MCs, need to be taken into account.

Introduction

The frequent occurrence of cyanobacterial blooms, such as the bloom formation of Microcystis spp., can seriously impair drinking water quality. In particular, microcystins (MCs) produced by Microcystis spp., primarily Microcystis aeruginosa, may induce severe liver injury in humans (Ueno et al., 1996; Codd et al., 2005). Meanwhile, micropollutants (e.g., antibiotics) in source waters are becoming a growing environmental problem worldwide. In recent years, the amounts of antibiotics observed in freshwater bodies, such as rivers and lakes, have ranged from ng L−1 to μg L−1 in many countries (Tamtam et al., 2008; Homem et al., 2014; Wu et al., 2016). As two continuously critical contaminants, antibiotics may co-occur with cyanobacteria in surface waters.

Recent studies have shown that the growth, membrane integrity, toxin productivity and macromolecular biomarkers of M. aeruginosa cells could be influenced by some types of micropollutants (e.g., organic pesticides, polycyclic aromatic hydrocarbons and heavy metals) in aquatic environments (Tsai, 2015; Martinez-Ruiz and Martinez-Jeronimo, 2018; Zhang et al., 2018). It has been reported that 0.02–0.2 mg L−1 nonylphenol (NP) stimulated the cell growth of four selected M. aeruginosa strains, whereas it inhibited their growth at a dosage of 2 mg L−1. For the toxic strain M. aeruginosa PCC7820, 0.2 mg L−1 NP induced the largest amount of intracellular MCs, which was 75% higher than that in the control sample (Wang et al., 2007). Recently, increasing studies have reported that antibiotic residuals in source waters also show a potential impact on the growth and toxin production of M. aeruginosa cells (Liu et al., 2016; Rico et al., 2018). A study by Liu et al. (2015) has documented that the physiological responses, such as cell proliferation, antioxidation activity and toxin release, of M. aeruginosa cells could be increased when they were exposed to 200 and 500 ng L−1 amoxicillin. For instance, the cell densities, activity of superoxide dismutase and extracellular MCs of M. aeruginosa samples treated with 500 ng L−1 amoxicillin for 7 days were increased by 8%, 75% and 85%, respectively, compared to the samples without amoxicillin. Therefore, antibiotics of ambient concentrations may seriously affect the formation of cyanobacteria blooms and induce variations in cell characteristics. It should be noted that these resulting changes in cyanobacteria cells may lead to other consequences. It is generally the case that greater amounts of oxidants (e.g., ozone and chlorine) and prolonged times were required during water treatment when cyanobacteria biomass and their toxin production were enhanced (Hitzfeld et al., 2000; Zhang et al., 2017). In addition, the changes in cell morphology, size distribution and surface properties may cause the neutralization of the zeta potential, which could promote the coagulation of Microcystis cells (Chen et al., 2017). Consequently, this study hypothesizes that the potential changes in cyanobacterial cells caused by the coincident antibiotics in source waters, will possibly affect the efficiency of the followed water treatment processes. However, to date, studies on such possibilities and the underlying mechanisms are unknown.

In drinking water treatment plants, there are various processes applied for cyanobacteria removal/inactivation, such as pre-oxidation and coagulation (Zamyadi et al., 2013). Potassium permanganate (KMnO4) is applied as a common oxidant for cyanobacteria treatment because of its low cost, simple operation and high efficiency (Li et al., 2014; Gong and Chu, 2018). In addition, KMnO4 oxidation is considered as an environmentally friendly process compared to the use of other oxidation processes (e.g., ozonation and chlorination), which may create undesirable disinfection by-products (DBPs) (Fang et al., 2010; Coral et al., 2013). Therefore, KMnO4 was selected as a model treatment process in this study. In addition, erythromycin (ERY) was chosen in this study, since ERY and its derivatives are some of the most commonly used macrolide antibiotics in human medicine and veterinary practice. Its concentration detected in rivers/lakes in China is generally from tens to hundreds ng L−1 (Xu et al., 2014; Ding et al., 2017; Zhou et al., 2017), and the maximum concentration observed can even reach μg L−1 (Lin and Tsai, 2009; Bu et al., 2013; Chen et al., 2018).

Consequently, the objectives of this study were to: (1) investigate the effects of a common antibiotic - ERY, on the growth of M. aeruginosa and their cell viability and associated toxin production; (2) assess the subsequent influences on KMnO4 oxidation in M. aeruginosa treatment; and (3) explore the possible mechanisms of the alteration in the effectiveness of M. aeruginosa treatment by KMnO4, when the cells were pre-exposed to ERY.

Section snippets

Cell culture

A toxic strain of M. aeruginosa FACHB-905 was provided by the Institute of Hydrobiology, Chinese Academy of Sciences, China. The cyanobacterial strain was routinely cultured in basal glucose (BG-11) medium (Stanier et al., 1971) to maintain logarithmic growth. All cultures were incubated at a constant temperature of 25 ± 1 °C under cool fluorescent light flux (27 μmol photons m−2 s−1, 12 h:12 h light-dark cycle). Prior to use in the experiments, the cyanobacterial cultures were adjusted to pH

Cell proliferation and membrane integrity

The cell densities of M. aeruginosa samples gradually increased during the cultivation time, where the initial ERY concentrations of 0, 0.2, 1.0, and 5.0 μg L−1 were spiked (Fig. 1a). The cell density in E-control (0 μg L−1 ERY) increased from 4.9 × 105 (day 0) to 6.7 × 106 cells mL−1 (day 6). For ERY-treated samples, the cell density in ERY-0.2 was 16% higher than that in E-control on day 4 (p < 0.05). The cell density in ERY-1 was increased to 7.4 × 106 cells mL−1 on day 6, which was 10%

The effects of ERY on the characteristics of M. aeruginosa cells

Cyanobacteria, which are similar to bacteria (Stanier and Cohen-Bazire, 1977), have been reported as cells that are sensitive to various antibiotics (van der Grinten et al., 2010; Rico et al., 2018). In this study, the cell growth of M. aeruginosa was stimulated by ERY at a low concentration (0.2 μg L−1), while it was inhibited at a high concentration (5.0 μg L−1). These findings are in agreement with a previous study, which observed that the growth of Microcystis flos-aquae was stimulated by

Conclusions

The cell growth of cyanobacteria and associated production of total MCs could be promoted by a micropollutant, such as ERY, at an environmentally relevant concentration (0.2 μg L−1). The extracellular MCs in the M. aeruginosa cells pre-exposed to 0.2 μg L−1 ERY were hardly detectable within intact cells during treatment with 2 mg L−1 KMnO4. However, 6 mg L−1 KMnO4 caused cellular damage in M. aeruginosa samples dosed with 0.2 μg L−1 ERY, which led to a concentration of extracellular MCs higher

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was supported by projects 51708490 and 41776084 from the National Natural Science Foundation of China.

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