Variable cyanobacterial death modes caused by ciprofloxacin in the aquatic environment: Prioritizing antibiotic-photosynthetic protein interactions for risk assessment

Abstract

Antibiotics continuously discharged into the aquatic environment pose threats to phototrophs via high-affinity binding to photosynthetic apparatuses and interfering with their energy metabolism and growth. However, studies attributed the sublethal effects of antibiotics on phototrophs to damaging photosystem (PS) II (PSII) proteins while neglecting PSI proteins as potential targets. Herein, we report that frequently detected ciprofloxacin (CIP) with concentrations of 3–8 μg/L was lethal to Microcystis aeruginosa, the widely distributed phytoplankton in freshwater, via damaging DNA. Besides, CIP damages on different photosynthetic proteins at different exposure levels were evidenced to influence the cyanobacterial death phenotypes. In detail, CIP at 3 μg/L bound to PSII D1 protein exclusively, activating the tricarboxylic acid cycle for energy and proline catabolism. This favored the execution of apoptosis-like regulated cell death (RCD). However, CIP at 8 μg/L exhibited additional binding to the PSI iron-sulfur reaction center, apart from PSII, inducing carbon and arginine starvation. This shifted the RCD from apoptosis-like RCD to mazEF-mediated RCD. Furthermore, microcystin-LR risks were elevated after CIP exposure with enhanced microcystin-LR release and biosynthesis for apoptosis-like and mazEF-mediated RCD, respectively. Thus, the present study underscores the intricate interactions between antibiotics and different photosynthetic apparatuses, which alter antibiotic lethal effects at different exposure levels. This could provide new perspectives on the risk assessment and prediction of antibiotics from the standpoint of chemical-photosynthesis interactions.