Mechanisms of silver nanoparticle toxicity on the marine cyanobacterium Prochlorococcus under environmentally-relevant conditions.

Abstract

[eng] Global demand for silver nanoparticles (AgNPs), and their inevitable release into the environment, is rapidly increasing. AgNPs display antimicrobial properties and have previously been recorded to exert adverse effects upon marine phytoplankton. However, ecotoxicological research is often compromised by the use of non-ecologically relevant conditions, and the mechanisms of AgNP toxicity under environmental conditions remains unclear. To examine the impact of AgNPs on natural marine communities, a natural assemblage was exposed to citrate-stabilised AgNPs. Here, investigation confirmed that the marine dominant cyanobacteria Prochlorococcus is particularly sensitive to AgNP exposure. Whilst Prochlorococcus represents the most abundant photosynthetic organism on Earth and contributes significantly to global primary productivity, little ecotoxicological research has been carried out on this cyanobacterium. To address this, Prochlorococcus was exposed to citrate-stabilised AgNPs, as well as silver in its ionic form (Ag2SO4), under simulated natural conditions. Both AgNPs and ionic silver were observed to reduce Prochlorococcus populations by over 90% at concentrations ≥10 μg L−1, representing the upper limit of AgNP concentrations predicted in the environment (10 μg L−1). Longer-term assessment revealed this to be a perturbation which was irreversible. Through use of quenching agents for superoxide and hydrogen peroxide, alongside incubations with ionic silver, it was revealed that AgNP toxicity likely arises from synergistic effects of toxic superoxide species generation and leaching of ionic silver. The extent of toxicity was strongly dependent on cell density, and completely mitigated in more cell-dense cultures. Hence, the calculation and reporting of the particle-to-cell ratio reveals that this parameter is effective for standardisation of experimental work, and allows for direct comparison between studies where cell density may vary. Given the key role that marine cyanobacteria play in global primary production and biogeochemical cycling, their higher susceptibility to AgNP exposure is a concern in hotspots of pollution.