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Title: Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes

Abstract

We report that design of nanomedicines and nanoparticle-based antimicrobial and antifouling formulations, and assessment of the potential implications of nanoparticle release into the environment require understanding nanoparticle interaction with bacterial surfaces. Here we demonstrate electrostatically driven association of functionalized nanoparticles with lipopolysaccharides of Gram-negative bacterial outer membranes and find that lipopolysaccharide structure influences the extent and location of binding relative to the lipid-solution interface. By manipulating the lipopolysaccharide content in Shewanella oneidensis outer membranes, we observed electrostatically driven interaction of cationic gold nanoparticles with the lipopolysaccharide-containing leaflet. We probed this interaction by quartz crystal microbalance with dissipation monitoring (QCM-D) and second harmonic generation (SHG) using solid-supported lipopolysaccharide-containing bilayers. Association of cationic nanoparticles increased with lipopolysaccharide content, while no association of anionic nanoparticles was observed. The harmonic-dependence of QCM-D measurements suggested that a population of the cationic nanoparticles was held at a distance from the outer leaflet-solution interface of bilayers containing smooth lipopolysaccharides (those bearing a long O-polysaccharide). Additionally, smooth lipopolysaccharides held the bulk of the associated cationic particles outside of the interfacial zone probed by SHG. Lastly, our results demonstrate that positively charged nanoparticles are more likely to interact with Gram-negative bacteria than are negatively charged particles, and this interactionmore » occurs primarily through lipopolysaccharides.« less

Authors:
 [1];  [2];  [3];  [4];  [3];  [5];  [6];  [6];  [7];  [6];  [4];  [2];  [8]
+ Show Author Affiliations
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering; Federal Inst. of Technology (ETH), Zurich (Switzerland)
  2. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Chemistry
  3. Univ. of Wisconsin, Madison, WI (United States). Environmental Chemistry and Technology Program
  4. Northwestern Univ., Evanston, IL (United States). Dept. of Chemistry
  5. Univ. of Illinois at Urbana−Champaign, Urbana, IL (United States). Dept. of Chemistry
  6. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  7. Univ. of Illinois at Urbana−Champaign, Urbana, IL (United States). Dept. of Chemistry
  8. Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering; Univ. of Wisconsin, Madison, WI (United States). Environmental Chemistry and Technology Program
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1221471
Report Number(s):
PNNL-SA-112154
Journal ID: ISSN 0013-936X; 47975; KP1704020
Grant/Contract Number:  
AC05-76RL01830; CHE- 1240151; T32 GM008347; DMR-0832760; CBET-0826204
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Science and Technology
Additional Journal Information:
Journal Volume: 49; Journal Issue: 17; Journal ID: ISSN 0013-936X
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Lipopolysaccharide; nanoparticle; bacterial outer membranes; antimicrobial; Environmental Molecular Sciences Laboratory

Citation Formats

Jacobson, Kurt H., Gunsolus, Ian L., Kuech, Thomas R., Troiano, Julianne M., Melby, Eric S., Lohse, Samuel E., Hu, Dehong, Chrisler, William B., Murphy, Catherine J., Orr, Galya, Geiger, Franz M., Haynes, Christy L., and Pedersen, Joel A. Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes. United States: N. p., 2015. Web. doi:10.1021/acs.est.5b01841.
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Jacobson, Kurt H., Gunsolus, Ian L., Kuech, Thomas R., Troiano, Julianne M., Melby, Eric S., Lohse, Samuel E., Hu, Dehong, Chrisler, William B., Murphy, Catherine J., Orr, Galya, Geiger, Franz M., Haynes, Christy L., & Pedersen, Joel A. Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes. United States. https://doi.org/10.1021/acs.est.5b01841
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Jacobson, Kurt H., Gunsolus, Ian L., Kuech, Thomas R., Troiano, Julianne M., Melby, Eric S., Lohse, Samuel E., Hu, Dehong, Chrisler, William B., Murphy, Catherine J., Orr, Galya, Geiger, Franz M., Haynes, Christy L., and Pedersen, Joel A. Fri . "Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes". United States. https://doi.org/10.1021/acs.est.5b01841. https://www.osti.gov/servlets/purl/1221471.
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@article{osti_1221471,
title = {Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes},
author = {Jacobson, Kurt H. and Gunsolus, Ian L. and Kuech, Thomas R. and Troiano, Julianne M. and Melby, Eric S. and Lohse, Samuel E. and Hu, Dehong and Chrisler, William B. and Murphy, Catherine J. and Orr, Galya and Geiger, Franz M. and Haynes, Christy L. and Pedersen, Joel A.},
abstractNote = {We report that design of nanomedicines and nanoparticle-based antimicrobial and antifouling formulations, and assessment of the potential implications of nanoparticle release into the environment require understanding nanoparticle interaction with bacterial surfaces. Here we demonstrate electrostatically driven association of functionalized nanoparticles with lipopolysaccharides of Gram-negative bacterial outer membranes and find that lipopolysaccharide structure influences the extent and location of binding relative to the lipid-solution interface. By manipulating the lipopolysaccharide content in Shewanella oneidensis outer membranes, we observed electrostatically driven interaction of cationic gold nanoparticles with the lipopolysaccharide-containing leaflet. We probed this interaction by quartz crystal microbalance with dissipation monitoring (QCM-D) and second harmonic generation (SHG) using solid-supported lipopolysaccharide-containing bilayers. Association of cationic nanoparticles increased with lipopolysaccharide content, while no association of anionic nanoparticles was observed. The harmonic-dependence of QCM-D measurements suggested that a population of the cationic nanoparticles was held at a distance from the outer leaflet-solution interface of bilayers containing smooth lipopolysaccharides (those bearing a long O-polysaccharide). Additionally, smooth lipopolysaccharides held the bulk of the associated cationic particles outside of the interfacial zone probed by SHG. Lastly, our results demonstrate that positively charged nanoparticles are more likely to interact with Gram-negative bacteria than are negatively charged particles, and this interaction occurs primarily through lipopolysaccharides.},
doi = {10.1021/acs.est.5b01841},
journal = {Environmental Science and Technology},
number = 17,
volume = 49,
place = {United States},
year = {Fri Jul 24 00:00:00 EDT 2015},
month = {Fri Jul 24 00:00:00 EDT 2015}
}
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https://doi.org/10.1021/acs.est.5b01841
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