Eco-friendly drugs from the marine environment: spongeweed-synthesized silver nanoparticles are highly effective on Plasmodium falciparum and its vector Anopheles stephensi, with little non-target effects on predatory copepods

Abstract

Mosquitoes act as vectors of devastating pathogens and parasites, representing a key threat for millions of humans and animals worldwide. The control of mosquito-borne diseases is facing a number of crucial challenges, including the emergence of artemisinin and chloroquine resistance in Plasmodium parasites, as well as the presence of mosquito vectors resistant to synthetic and microbial pesticides. Therefore, eco-friendly tools are urgently required. Here, a synergic approach relying to nanotechnologies and biological control strategies is proposed. The marine environment is an outstanding reservoir of bioactive natural products, which have many applications against pests, parasites, and pathogens. We proposed a novel method of seaweed-mediated synthesis of silver nanoparticles (AgNP) using the spongeweed Codium tomentosum, acting as a reducing and capping agent. AgNP were characterized by UV-Vis spectroscopy, Fourier transform infrared (FTIR) spectroscopy, scanning electron microscopy (SEM), energy-dispersive X-ray spectroscopy (EDX), and X-ray diffraction (XRD). In mosquitocidal assays, the 50 % lethal concentration (LC50) of C. tomentosum extract against Anopheles stephensi ranged from 255.1 (larva I) to 487.1 ppm (pupa). LC50 of C. tomentosum-synthesized AgNP ranged from 18.1 (larva I) to 40.7 ppm (pupa). In laboratory, the predation efficiency of Mesocyclops aspericornis copepods against A. stephensi larvae was 81, 65, 17, and 9 % (I, II, III, and IV instar, respectively). In AgNP contaminated environment, predation was not affected; 83, 66, 19, and 11 % (I, II, III, and IV). The anti-plasmodial activity of C. tomentosum extract and spongeweed-synthesized AgNP was evaluated against CQ-resistant (CQ-r) and CQ-sensitive (CQ-s) strains of Plasmodium falciparum. Fifty percent inhibitory concentration (IC50) of C. tomentosum were 51.34 μg/ml (CQ-s) and 65.17 μg/ml (CQ-r); C. tomentosum-synthesized AgNP achieved IC50 of 72.45 μg/ml (CQ-s) and 76.08 μg/ml (CQ-r). Furthermore, low doses of the AgNP inhibited the growth of Bacillus subtilis, Klebsiella pneumoniae, and Salmonella typhi, using the agar disk diffusion and minimum inhibitory concentration protocol. Overall, C. tomentosum metabolites and spongeweed-synthesized AgNP may be potential candidates to develop novel and effective tools in the fight against Plasmodium parasites and their mosquito vectors. The employ of ultra-low doses of nanomosquitocides in synergy with cyclopoid crustaceans seems a promising green route for effective mosquito control programs.

Keywords: Anopheles stephensi; Anti-bacterial activity; Codium tomentosum; Malaria; Mesocyclops aspericornis; Mosquito-borne diseases; Plasmodium falciparum.