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Title: Structural and metabolic responses of Staphylococcus aureus biofilms to hyperosmotic and antibiotic stress

Abstract

Biofilms alter their metabolism in response to environmental stress. This study explores the effect of a hyperosmotic agent–antibiotic treatment on the metabolism of Staphylococcus aureus biofilms through the use of nuclear magnetic resonance (NMR) techniques. To determine the metabolic activity of S. aureus, we quantified the concentrations of metabolites in spent medium using high-resolution NMR spectroscopy. Biofilm porosity, thickness, biovolume, and relative diffusion coefficient depth profiles were obtained using NMR microimaging. Dissolved oxygen (DO) concentration was measured to determine the availability of oxygen within the biofilm. Under vancomycin-only treatment, the biofilm communities switched to anaerobic fermentation, as evidenced by high concentrations of formate, acetate, and lactate, and there was no detectable dissolved oxygen in the biofilm. Anaerobic conditions such as fermentation can signify that biofilm is combating antibiotic stress by developing resistance. In addition, we observed the highest consumption of pyruvate, the sole carbon source, under the vancomycin-only treatment. On the other hand, relative effective diffusion coefficients increased under vancomycin-only treatment but decreased under maltodextrin-only and combined treatments. No change was observed in either biofilm thickness or biovolume for biofilms treated with maltodextrin-only or in combination with vancomycin. This indicates that biofilm growth was halted during maltodextrin-only and combined treatments.more » Overall, we demonstrated that the metabolic activity of S. aureus biofilm is affected by hyperosmotic and antibiotic stress.« less

Authors:
 [1];  [1];  [2];  [2];  [1];  [3];  [1]; ORCiD logo [4]
  1. The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman Washington
  2. Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland Washington
  3. Paul G. Allen School for Global Animal Health, Washington State University, Pullman Washington
  4. The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman Washington; Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland Washington; Earth and Biological Sciences Division, Pacific Northwest National Laboratory, Richland Washington
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1438994
Report Number(s):
PNNL-SA-129573
Journal ID: ISSN 0006-3592; 48655
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Biotechnology and Bioengineering; Journal Volume: 115; Journal Issue: 6
Country of Publication:
United States
Language:
English
Subject:
staphylococcus aureus; biofilm; hyperosmotic agent; metabolites; porosity; diffusion coefficient; Environmental Molecular Sciences Laboratory

Citation Formats

Kiamco, Mia M., Mohamed, Abdelrhman, Reardon, Patrick N., Marean-Reardon, Carrie L., Aframehr, Wrya M., Call, Douglas R., Beyenal, Haluk, and Renslow, Ryan S. Structural and metabolic responses of Staphylococcus aureus biofilms to hyperosmotic and antibiotic stress. United States: N. p., 2018. Web. doi:10.1002/bit.26572.
Kiamco, Mia M., Mohamed, Abdelrhman, Reardon, Patrick N., Marean-Reardon, Carrie L., Aframehr, Wrya M., Call, Douglas R., Beyenal, Haluk, & Renslow, Ryan S. Structural and metabolic responses of Staphylococcus aureus biofilms to hyperosmotic and antibiotic stress. United States. doi:10.1002/bit.26572.
Kiamco, Mia M., Mohamed, Abdelrhman, Reardon, Patrick N., Marean-Reardon, Carrie L., Aframehr, Wrya M., Call, Douglas R., Beyenal, Haluk, and Renslow, Ryan S. Sat . "Structural and metabolic responses of Staphylococcus aureus biofilms to hyperosmotic and antibiotic stress". United States. doi:10.1002/bit.26572.
@article{osti_1438994,
title = {Structural and metabolic responses of Staphylococcus aureus biofilms to hyperosmotic and antibiotic stress},
author = {Kiamco, Mia M. and Mohamed, Abdelrhman and Reardon, Patrick N. and Marean-Reardon, Carrie L. and Aframehr, Wrya M. and Call, Douglas R. and Beyenal, Haluk and Renslow, Ryan S.},
abstractNote = {Biofilms alter their metabolism in response to environmental stress. This study explores the effect of a hyperosmotic agent–antibiotic treatment on the metabolism of Staphylococcus aureus biofilms through the use of nuclear magnetic resonance (NMR) techniques. To determine the metabolic activity of S. aureus, we quantified the concentrations of metabolites in spent medium using high-resolution NMR spectroscopy. Biofilm porosity, thickness, biovolume, and relative diffusion coefficient depth profiles were obtained using NMR microimaging. Dissolved oxygen (DO) concentration was measured to determine the availability of oxygen within the biofilm. Under vancomycin-only treatment, the biofilm communities switched to anaerobic fermentation, as evidenced by high concentrations of formate, acetate, and lactate, and there was no detectable dissolved oxygen in the biofilm. Anaerobic conditions such as fermentation can signify that biofilm is combating antibiotic stress by developing resistance. In addition, we observed the highest consumption of pyruvate, the sole carbon source, under the vancomycin-only treatment. On the other hand, relative effective diffusion coefficients increased under vancomycin-only treatment but decreased under maltodextrin-only and combined treatments. No change was observed in either biofilm thickness or biovolume for biofilms treated with maltodextrin-only or in combination with vancomycin. This indicates that biofilm growth was halted during maltodextrin-only and combined treatments. Overall, we demonstrated that the metabolic activity of S. aureus biofilm is affected by hyperosmotic and antibiotic stress.},
doi = {10.1002/bit.26572},
journal = {Biotechnology and Bioengineering},
number = 6,
volume = 115,
place = {United States},
year = {Sat Mar 24 00:00:00 EDT 2018},
month = {Sat Mar 24 00:00:00 EDT 2018}
}