Abstract

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.

Highlights

  • The fate and effects of engineered nanomaterials within the aquatic environment has become a subject of concern and focus of research in recent years.[1,2,3,4] Silver nanoparticles (AgNPs) are present in approximately one quarter of commercially marketed nano-products, primarily because of their antibacterial properties.[5, 6] This represents the fastest growing class of engineered nanomaterials used for commercial purposes.[7]

  • Using the model Prochlorococcus strain MED4 grown under environmentally-relevant conditions we show for the first time that the toxicity and ability of populations to recover from short-term stress caused by AgNP exposure is largely dependent on cell density, a feature often overlooked in ecotoxicological studies upon microbial organisms

  • Under environmentally-relevant conditions citrate-stabilised AgNPs exert a toxic response upon marine phytoplankton, being the dominant cyanobacterium Prochlorococcus mostly affected

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Summary

Introduction

The fate and effects of engineered nanomaterials within the aquatic environment has become a subject of concern and focus of research in recent years.[1,2,3,4] Silver nanoparticles (AgNPs) are present in approximately one quarter of commercially marketed nano-products, primarily because of their antibacterial properties.[5, 6] This represents the fastest growing class of engineered nanomaterials used for commercial purposes.[7] Global production of AgNPs is currently over 800 metric tonnes per annum[8] and is predicted to rise.[9] The surfaces of AgNPs can be altered to control the release of ionic Ag+, thought to be primarily responsible for their antibacterial properties.[10] Citrate-stabilised AgNPs represent the most widely used silver colloids for research and commercial purposes.[11,12,13,14] The widespread use of AgNPs and the significant increase in production of consumer goods utilising nanosized Ag, has increased

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