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

Abstract

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.

Trophic transfer of heavy metals along a pollution gradient in a terrestrial agro-industrial food web

“…Such studies improve our understanding of the ecological effects of pollution on wildlife (Saaristo et al, 2018). So far, a range of works have examined the effects of pesticides (Dewer et al, 2016;Serra et al, 2020;Engell Dahl et al, 2021), heavy metals (Berni et al, 2019;Cosio and Renault, 2020), pharmaceuticals (Prud'homme et al, 2018;Renault et al, 2018) or polymers (de Souza Machado et al, 2018;Kögel et al, 2020) on the biology and physiology of plants and insects. In ACCEPTED MANUSCRIPT -CLEAN COPY 4 addition to describing the conspicuous impacts on growth and development, these investigations have revealed the latent effects pollutants can have on the ecology and biology of wildlife.…”

“…In ACCEPTED MANUSCRIPT -CLEAN COPY 4 addition to describing the conspicuous impacts on growth and development, these investigations have revealed the latent effects pollutants can have on the ecology and biology of wildlife. The insidious nature of xenobiotics toxicity includes, for instance, deleterious effects of antibiotics on the muscle structure of flies (Renault et al, 2018), impacts of ibuprofen on the development of mosquitoes (Prud'homme et al, 2018), or cryptic effects of low doses of pesticides on plant metabolism (Serra et al, 2013) and animal behavior (Desneux et al, 2007;Hanlon and Relyea, 2013).…”

Impact of Gut Bacteria on the Infection and Transmission of Pathogenic Arboviruses by Biting Midges and Mosquitoes

“…Antibiotic treatment may inhibit formation of a peritrophic matrix around the blood bolus after blood-feeding [81], thereby enhancing the possibility of virus particles to interact with the midgut epithelial cells. Furthermore, it was shown that antibiotics can induce long-lasting damaging effects on muscle structure and mitochondrial metabolism in blow flies [84]. Similar effects on midgut cells may result in a "leaky gut," which is a well-described physiological change in insect vector midgut cells that results in increased virus infection [66,85,86].…”

Effect of different doses of the catecholamine epinephrine on antioxidant responses of larvae of the flesh fly Sarcophaga dux

“…These pollutants, which can persist over the long term, can greatly threaten biodiversity (Santos et al 2010;Richmond et al 2016). For instance, in a recent study, Renault et al (2018) experimentally evidenced the deleterious effects of antibiotics on the development and survival of the blow fly Chrysomya albiceps. In mosquitoes, chronic exposure of the parental generation to the antiinflammatory ibuprofen had consistent effects on the progeny by accelerating their development and increasing their capacity to handle starvation periods (Prud'homme et al 2018).…”