Oxidative stress responses and cellular energy allocation changes in microalgae following exposure to widely used human antibiotics

This work was partly funded by the EU Transnational Territorial Cooperation programme INTERREG IVB NWE projects (PILLS project 008B & “noPILLS in our waters”); and A. Aderemi was also funded by a PhD studentship from SEBE, Glasgow Caledonian University. This study also had the support of the Fundação para a Ciência e a Tecnologia (FCT) Strategic Project UID/MAR/04292/2013 granted to MARE, project ProTEoME - PROteomic Tools to assess Endocrine disruptiOn MEchanisms ((PTDC/AAG-MAA/1302/2014), and the post-doc grant to Sara C. Novais (SFRH/BPD/94500/2013). The project was also partially funded by the Integrated Programme of SR&TD “SmartBioR” (reference Centro-01-0145-FEDER-000018) cofunded by Centro 2020 program, Portugal2020, European Union, through the European Regional Development Fund.

The individual effect of four human antibiotics on the microalgae Raphidocelis subcapitata was investigated following a 120-h exposure. The effects were assessed by analyzing growth, and biochemical parameters related with: 1) antioxidant capacity and oxidative damage by measuring superoxide dismutase (SOD) activity and lipid peroxidation (LPO) levels; and 2) cellular energy allocation (CEA) by quantifying the content in energy reserves, which represents the energy available (Ea), and the electron transport system activity that represents a measure of oxygen and cellular energy consumption (Ec). Growth yield inhibitory concentrations of sulfamethoxazole (18–30%), clarithromycin (28.7%), ciprofloxacin (28%) and erythromycin (17–39%) were found to elicit a considerable increase in Ec, thereby causing a significant decrease in the CEA. The elevated Ec can be a result of the need to respond to oxidative stress occurring under those conditions given the significant increase in SOD activity at these levels. For sulfamethoxazole, erythromycin and ciprofloxacin, the antioxidant responses do not seem to be enough to cope with the reactive oxygen species and prevent oxidative damage, given the elevated LPO levels observed. A stimulatory effect on growth yield was observed (up to 16%) at ciprofloxacin lowest concentration, which highly correlated with the increase in CEA. Based on the no observed effect concentration (NOECs) and/or effective concentration (EC10) results, Ec, SOD and CEA were more sensitive than the classical endpoint of growth rate for all the tested antibiotics. By revealing the antibiotic stress effects in R. subcapitata at the cellular level, this study suggests CEA as a more reliable indicator of the organisms’ physiological status.

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