Chronic Exposure to Complex Metal Oxide Nanoparticles Elicits Rapid Resistance in Shewanella Oneidensis MR-1

Authors

Stephanie L. Mitchell, University of Minnesota - Twin Cities
Natalie V. Hudson-Smith, University of Minnesota - Twin Cities
Meghan S. Cahill, University of Minnesota - Twin Cities
Benjamin N. Reynolds, University of Minnesota - Twin Cities
Seth D. Frand, Augsburg University
Curtis M. Green, University of Wisconsin-Madison
Chenyu Wang, University of Wisconsin-Madison
Mimi N. Hang, University of Wisconsin-Madison
Rodrigo Tapia Hernandez, Augsburg University
Robert J. Hamers, University of Wisconsin-Madison
Z. Vivian Feng, Augsburg UniversityFollow
Christy L. Haynes, University of Minnesota - Twin Cities
Erin E. Carlson, University of Minnesota - Twin Cities

ORCID

0000-0002-3329-3781

Document Type

Article

Publication Date

8-30-2019

DOI

10.1039/C9SC01942A

Abstract

Engineered nanoparticles are incorporated into numerous emerging technologies because of their unique physical and chemical properties. Many of these properties facilitate novel interactions, including both intentional and accidental effects on biological systems. Silver-containing particles are widely used as antimicrobial agents and recent evidence indicates that bacteria rapidly become resistant to these nanoparticles. Much less studied is the chronic exposure of bacteria to particles that were not designed to interact with microorganisms. For example, previous work has demonstrated that the lithium intercalated battery cathode nanosheet, nickel manganese cobalt oxide (NMC), is cytotoxic and causes a significant delay in growth of Shewanella oneidensis MR-1 upon acute exposure. Here, we report that S. oneidensis MR-1 rapidly adapts to chronic NMC exposure and is subsequently able to survive in much higher concentrations of these particles, providing the first evidence of permanent bacterial resistance following exposure to nanoparticles that were not intended as antibacterial agents. We also found that when NMC-adapted bacteria were subjected to only the metal ions released from this material, their specific growth rates were higher than when exposed to the nanoparticle. As such, we provide here the first demonstration of bacterial resistance to complex metal oxide nanoparticles with an adaptation mechanism that cannot be fully explained by multi-metal adaptation. Importantly, this adaptation persists even after the organism has been grown in pristine media for multiple generations, indicating that S. oneidensis MR-1 has developed permanent resistance to NMC.

Comments

Final version published in the journal Chemical Science at https://doi.org/10.1039/C9SC01942A

Recommended Citation

Mitchell, S.M.; Hudson-Smith, N.V.; Cahill, M.S.; Reynolds, B.N.; Frand, S.D.; Green, C.M.; Wang, W.; Hang, M.N.; Hernandez, R.T.; Hamers, R.J.; Feng, Z.V.; Haynes, C.L. and Carlson, E.E., “Chronic exposure to complex metal oxide nanoparticles elicits rapid resistance in Shewanella oneidensis MR-1”, Chem. Sci., 2019, 10, 9768-9781.