Influences of the micropollutant erythromycin on cyanobacteria treatment with potassium permanganate
Graphical abstract
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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2023, Journal of Environmental Sciences (China)Citation Excerpt :In the present study, the ultrastructural characteristic changes indicated that cell integrity was damaged under CAA (5 mg/L) exposure for 72 hr, which resulted in the efflux of cellular contents and the extra-MC-LR concentration increased compared with the control. The release of MC-LR to extracellular space is due to the membrane permeability changes caused by serious lipid peroxidation (Lin et al., 2020). The mcyH gene is a putative ABC transporter, and toxin transference is mainly controlled by the mcyH gene (Pearson et al., 2004; Wu et al., 2018).