The multilevel antibiotic-induced perturbations to biological systems: Early-life exposure induces long-lasting damages to muscle structure and mitochondrial metabolism in flies

• Published in: Environmental pollution (1987) Vol. 241; pp. 821 - 833
• Main Authors: Renault, David, Yousef, Hesham, Mohamed, Amr A.
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01-10-2018; Elsevier
• Subjects: Antibiotics; Biodiversity and Ecology; Ecotoxicology; Energy metabolism; Environmental Sciences; Eukaryote; Insect flight muscles; Life Sciences; Metabolomics; Mitochondrial dysfunction; Toxicology; Eukaryote; Metabolomics; Energy metabolism; Mitochondrial dysfunction; Antibiotics; Insect flight muscles
• ISSN: 0269-7491; 1873-6424
• DOI: 10.1016/j.envpol.2018.06.011

Antibiotics have been increasingly used over the past decades for human medicine, food-animal agriculture, aquaculture, and plant production. A significant part of the active molecules of antibiotics can be released into the environment, in turn affecting ecosystem functioning and biogeochemical processes. At lower organizational scales, these substances affect bacterial symbionts of insects, with negative consequences on growth and development of juveniles, and population dynamics. Yet, the multiple alterations of cellular physiology and metabolic processes have remained insufficiently explored in insects. We evaluated the effects of five antibiotics with different mode of action, i.e. ampicillin, cefradine, chloramphenicol, cycloheximide, and tetracycline, on the survival and ultrastructural organization of the flight muscles of newly emerged blow flies Chrysomya albiceps. Then, we examined the effects of different concentrations of antibiotics on mitochondrial protein content, efficiency of oxidative phosphorylation, and activity of transaminases (Glutamate oxaloacetate transaminase and glutamate pyruvate transaminase) and described the cellular metabolic perturbations of flies treated with antibiotics. All antibiotics affected the survival of the insects and decreased the total mitochondrial protein content in a dose-dependent manner. Ultrastructural organization of flight muscles in treated flies differs dramatically compared to the control groups and severe pathological damages/structures disorganization of mitochondria appeared. The activities of mitochondrial transaminases significantly increased with increased antibiotic concentrations. The oxidation rate of pyruvate + proline from isolated mitochondria of the flight muscles of 1-day-old flies was significantly reduced at high doses of antibiotics. In parallel, the level of several metabolites, including TCA cycle intermediates, was reduced in antibiotics-treated flies. Overall, antibiotics provoked a system-wide alteration of the structure and physiology of flight muscles of the blow fly Ch. albiceps, and may have fitness consequences at the organism level. Environmental antibiotic pollution is likely to have unwanted cascading ecological effects of insect population dynamics and community structure.
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•All tested antibiotics affected the survival of the flies in a dose-dependent manner.•Antibiotics provoked multiple direct and cascading effects on the structure of the flight muscles and physiology of the flies.•Antibiotics altered oxidative phosphorylation and the level of Krebs cycle intermediates.•Environmental antibiotic pollution likely has unwanted cascading ecological effects on insect population dynamics.