Ciprofloxacin enhances cadmium toxicity to earthworm Eisenia fetida by altering the gut microorganism composition

Abstract

The concurrent existence of cadmium (Cd) and ciprofloxacin (CIP) in agricultural soils is very common, but presents a challenge to soil organisms. As more attention has been paid to the effect of toxic metals on the migration of antibiotic resistance genes, the critical role of the gut microbiota in CIP-modifying Cd toxicity in earthworms remains unclear. In this study, Eisenia fetida was exposed to Cd and CIP alone or in combination at environmentally relevant concentrations. Cd and CIP accumulation in earthworm increased as their respective spiked concentrations increased. In fact, Cd accumulation increased by 39.7% when 1 mg/kg CIP was added; however, the addition of Cd did not affect CIP uptake. Compared with exposure to Cd alone, a greater ingestion of Cd following combined exposure to Cd and 1 mg/kg CIP resulted in greater oxidative stress and energy metabolism disturbances in earthworms. The reactive oxygen species (ROS) contents and apoptosis rate of coelomocytes were more sensitive to Cd than these biochemical indicators. In fact, 1 mg/kg Cd induced the derivation of ROS. Similarly, the toxicity of Cd (5 mg/kg) to coelomocytes was promoted by CIP (1 mg/kg), ROS content in coelomocytes and the apoptosis rate increased by 29.2% and 113.1%, respectively, due to increased Cd accumulation. Further investigation of the gut microorganisms revealed that the decreased abundance of Streptomyces strains (known as Cd accumulation taxa) could be a critical factor for enhanced Cd accumulation and greater Cd toxicity to earthworms following exposure to both Cd and CIP; this was because this microorganism group was eliminated by the simultaneous ingestion of CIP. This study stressed the role of gut microorganisms in altering the toxicity of Cd and CIP combined contamination in soil organisms. More attention should be paid to the ecological risks of such combined contamination in soils.

Keywords: Antioxidant response; Cadmium; Ciprofloxacin; Coelomocyte; Gut microbiome.