Planktonic and biofilm-grown nitrogen-cycling bacteria exhibit different susceptibilities to copper nanoparticles

• Published in: Environmental toxicology and chemistry 2015-04, Vol.34 (4), p.887-897
• Main Authors: Reyes, Vincent C., Opot, Stephen O., Mahendra, Shaily
• Format: Article
• Language: English
• Subjects: Ammonium Compounds - metabolism; Azotobacter vinelandii; Azotobacter vinelandii - drug effects; Azotobacter vinelandii - growth & development; Bacteria; Bacteria - drug effects; Bacteria - growth & development; Biofilms; Biofilms - growth & development; Control equipment; Copper; Copper - toxicity; Culture; Environmental Pollutants - toxicity; Extracellular polymeric substances; Gene Expression Regulation, Bacterial - drug effects; Inhibition; Metal Nanoparticles - toxicity; Metallic; MICRO ORGANISMS; Nanomaterials; Nanoparticles; Nitrates - metabolism; NITROGEN; Nitrogen Fixation; Nitrosomonas europaea; Nitrosomonas europaea - drug effects; Nitrosomonas europaea - growth & development; Oxidation; Oxidation-Reduction; Paracoccus denitrificans; Paracoccus denitrificans - drug effects; Paracoccus denitrificans - growth & development; PARTICLES; Plankton - microbiology; Reduction; Stress
• ISSN: 0730-7268; 1552-8618
• DOI: 10.1002/etc.2867

Proper characterization of nanoparticle (NP) interactions with environmentally relevant bacteria under representative conditions is necessary to enable their sustainable manufacture, use, and disposal. Previous nanotoxicology research based on planktonic growth has not adequately explored biofilms, which serve as the predominant mode of bacterial growth in natural and engineered environments. Copper nanoparticle (Cu‐NP) impacts on biofilms were compared with respective planktonic cultures of the ammonium‐oxidizing Nitrosomonas europaea, nitrogen‐fixing Azotobacter vinelandii, and denitrifying Paracoccus denitrificans using a suite of independent toxicity diagnostics. Median inhibitory concentration (IC50) values derived from adenosine triphosphate (ATP) for Cu‐NPs were lower in N. europaea biofilms (19.6 ± 15.3 mg/L) than in planktonic cells (49.0 ± 8.0 mg/L). However, in absorbance‐based growth assays, compared with unexposed controls, N. europaea growth rates in biofilms were twice as resilient to inhibition than those in planktonic cultures. Similarly, relative to unexposed controls, growth rates and yields of P. denitrificans in biofilms exposed to Cu‐NPs were 40‐fold to 50‐fold less inhibited than those in planktonic cells. Physiological evaluation of ammonium oxidation and nitrate reduction suggested that biofilms were also less inhibited by Cu‐NPs than planktonic cells. Furthermore, functional gene expression for ammonium oxidation (amoA) and nitrite reduction (nirK) showed lower inhibition by NPs in biofilms relative to planktonic‐grown cells. These results suggest that biofilms mitigate NP impacts, and that nitrogen‐cycling bacteria in wastewater, wetlands, and soils might be more resilient to NPs than planktonic‐based assessments suggest. Environ Toxicol Chem 2015;34:887–897. © 2014 SETAC