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

Journal Article · · Biotechnology and Bioengineering
DOI:https://doi.org/10.1002/bit.26572· OSTI ID:1438994
 [1];  [1];  [2];  [2];  [1];  [3];  [1];  [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

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.

Research Organization:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Organization:
USDOE
DOE Contract Number:
AC05-76RL01830
OSTI ID:
1438994
Report Number(s):
PNNL-SA-129573; 48655
Journal Information:
Biotechnology and Bioengineering, Vol. 115, Issue 6; ISSN 0006-3592
Publisher:
Wiley
Country of Publication:
United States
Language:
English

References (42)

Effect of Oxygen on Glucose Metabolism: Utilization of Lactate in Staphylococcus Aureus as Revealed by In Vivo NMR Studies journal March 2013
Regulation of electron transfer processes affects phototrophic mat structure and activity journal September 2015
In vivo activity of vancomycin combined with colistin against multidrug-resistant strains of Acinetobacter baumannii in a Galleria mellonella model journal October 2015
How antibiotics kill bacteria: from targets to networks journal May 2010
Mechanism of Aminoglycoside Antibiotic Resistance in Anaerobic Bacteria: Clostridium perfringens and Bacteroides fragilis journal January 1979
Bacterial Drug Tolerance under Clinical Conditions Is Governed by Anaerobic Adaptation but not Anaerobic Respiration journal July 2014
Biofilms in chronic wounds journal January 2008
Clinical Approach to Wounds: D??bridement and Wound Bed Preparation Including the Use of Dressings and Wound-Healing Adjuvants journal January 2006
Contributions of Antibiotic Penetration, Oxygen Limitation, and Low Metabolic Activity to Tolerance of Pseudomonas aeruginosa Biofilms to Ciprofloxacin and Tobramycin journal January 2003
Metabolic regulation of antibiotic resistance journal September 2011
In situ effective diffusion coefficient profiles in live biofilms using pulsed-field gradient nuclear magnetic resonance journal April 2010
Rapid depletion of dissolved oxygen in 96-well microtiter plate Staphylococcus epidermidis biofilm assays promotes biofilm development and is influenced by inoculum cell concentration journal August 2009
Synergy between oxacillin and manuka honey sensitizes methicillin-resistant Staphylococcus aureus to oxacillin journal March 2012
Oxygen Limitation Contributes to Antibiotic Tolerance of Pseudomonas aeruginosa in Biofilms journal June 2004
Influence of Iron and Aeration on Staphylococcus aureus Growth, Metabolism, and Transcription journal April 2014
A novel metabolomic approach used for the comparison of Staphylococcus aureus planktonic cells and biofilm samples journal March 2016
Anaerobic Gene Expression in Staphylococcus aureus journal March 2007
In situ nuclear magnetic resonance microimaging of live biofilms in a microchannel journal January 2017
Anaerobic Conditions Induce Expression of Polysaccharide Intercellular Adhesin in Staphylococcus aureus and Staphylococcus epidermidis journal June 2001
Effect of osmotic pressure on membrane energy-linked functions in Escherichia coli journal January 1991
Metabolic profiling of Staphylococcus aureus cultivated under aerobic and anaerobic conditions with 1 H NMR-based nontargeted analysis journal June 2012
Intracellular Organic Osmolytes: Function and Regulation journal February 2008
Antibiotic-specific differences in the response of Staphylococcus aureus to treatment with antimicrobials combined with manuka honey journal January 2015
Diffusion in biofilms respiring on electrodes journal January 2013
Surgical Treatment of the Infected Diabetic Foot journal August 2004
Vancomycin and maltodextrin affect structure and activity of Staphylococcus aureus biofilms : Vancomycin and Maltodextrin Affect Biofilms journal September 2015
Comparative Activities of Daptomycin, Linezolid, and Tigecycline against Catheter-Related Methicillin-Resistant Staphylococcus Bacteremic Isolates Embedded in Biofilm journal March 2007
NMRPipe: A multidimensional spectral processing system based on UNIX pipes journal November 1995
A real-life clinical evaluation of a next-generation antimicrobial dressing on acute and chronic wounds journal January 2015
Bactericidal Action of Daptomycin against Stationary-Phase and Nondividing Staphylococcus aureus Cells journal October 2007
Managing biofilm by using dressings journal June 2015
Apolipoprotein B Is an Innate Barrier against Invasive Staphylococcus aureus Infection journal December 2008
Staphylococcus aureus in the House Fly: Temporospatial Fate of Bacteria and Expression of the Antimicrobial Peptide defensin journal January 2013
Fitness Cost of VanA-Type Vancomycin Resistance in Methicillin-Resistant Staphylococcus aureus journal March 2009
Colonization of Epidermal Tissue by Staphylococcus aureus Produces Localized Hypoxia and Stimulates Secretion of Antioxidant and Caspase-14 Proteins journal May 2015
Compensation of the Metabolic Costs of Antibiotic Resistance by Physiological Adaptation in Escherichia coli journal May 2013
Electron Donors Supporting Growth and Electroactivity of Geobacter sulfurreducens Anode Biofilms journal November 2011
Regular debridement is the main tool for maintaining a healthy wound bed in most chronic wounds journal February 2009
Transcriptional Activation of the Staphylococcus aureus putP Gene by Low-Proline-High Osmotic Conditions and during Infection of Murine and Human Tissues journal December 2005
Antibiotic resistance and its cost: is it possible to reverse resistance? journal March 2010
Mathematical modeling of dormant cell formation in growing biofilm journal May 2015
Improving Antibiotic Activity against Wound Pathogens with Manuka Honey In Vitro journal September 2012