Effect of metal cations on antimicrobial activity and compartmentalization of silver in Shewanella oneidensis MR-1 upon exposure to silver ions

Abstract

Silver is an antimicrobial agent that is used extensively in consumer products, such as fabrics and humidifiers. Silver ion (Ag+) uptake in bacteria represents a crucial phase of antimicrobial activity. However, the uptake mechanism of Ag+ in bacteria remains largely unknown. The genus Shewanella drives many geochemical processes of nutrients and pollutants in soils. In the present study, Ag+ uptake by Shewanella oneidensis MR-1 was first investigated in a laboratory in defined anaerobic, oligotrophic, and inorganic media with or without cations (potassium ions [K+], magnesium ions [Mg2+], and zinc ions [Zn2+]). Our results revealed variations in antimicrobial activity of Ag+ in the presence of Mg2+ and Zn2+. First, Mg2+ significantly decreased antimicrobial activity of Ag+ in S. oneidensis MR-1 by inhibiting cellular Ag+ uptake when compared with K+. The results were consistent with that of Co2+ (Mg2+ channel blocker) decreased Ag+ uptake by S. oneidensis MR-1. Moreover, Mg2+ promoted riboflavin secretion and facilitated the formation of metallic Ag nanoparticles on bacterial surfaces, which was beneficial for extracellular electron transfer and consequently reduced antibacterial activity of Ag+. Second, Zn2+ increased the antimicrobial activity of Ag+ in S. oneidensis MR-1, although the effect on Ag+ uptake was minimal. A synergistic interaction between Zn2+ and Ag+ led to an increase in dead cells and decreased ferrihydrite reduction capacity. The findings suggest that Mg2+ could reduce the environmental risk of Ag+ to soil bacteria, while Zn2+ should be of particular concern due to its synergistic antimicrobial effect on bacteria.