Arginine deiminase in Staphylococcus epidermidis functions to augment biofilm maturation through pH homeostasis

J. K. Lindgren, Vinai Chittezham Thomas, M. E. Olson, S. S. Chaudhari, Austin S Nuxoll, C. R. Schaeffer, K. E. Lindgren, J. Jones, Matthew C Zimmerman, P. M. Dunman, Kenneth W Bayles, Paul D Fey

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

Allelic replacement mutants were constructed within arginine deiminase (arcA1 and arcA2) to assess the function of the arginine deiminase (ADI) pathway in organic acid resistance and biofilm formation of Staphylococcus epidermidis 1457. A growth-dependent acidification assay (pH ̃5.0 to ̃5.2) determined that strain 1457 devoid of arginine deiminase activity (1457 ΔADI) was significantly less viable than the wild type following depletion of glucose and in the presence of arginine. However, no difference in viability was noted for individual 1457 ΔarcA1 (native) or ΔarcA2 (arginine catabolic mobile element [ACME]-derived) mutants, suggesting that the native and ACME-derived ADIs are compensatory in S. epidermidis. Furthermore, flow cytometry and electron paramagnetic resonance spectroscopy results suggested that organic acid stress resulted in oxidative stress that could be partially rescued by the iron chelator dipyridyl. Collectively, these results suggest that formation of hydroxyl radicals is partially responsible for cell death via organic acid stress and that ADI-derived ammonia functions to counteract this acid stress. Finally, static biofilm assays determined that viability, ammonia synthesis, and pH were reduced in strain 1457 ΔADI following 120 h of growth in comparison to strain 1457 and the arcA1 and arcA2 single mutants. It is hypothesized that ammonia synthesis via the ADI pathway is important to reduce pH stress in specific microniches that contain high concentrations of organic acids.

Original languageEnglish (US)
Pages (from-to)2277-2289
Number of pages13
JournalJournal of bacteriology
Volume196
Issue number12
DOIs
StatePublished - 2014

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Staphylococcus epidermidis
Biofilms
Homeostasis
Acids
Ammonia
Arginine
Electron Spin Resonance Spectroscopy
Chelating Agents
Growth
Hydroxyl Radical
arginine deiminase
Spectrum Analysis
Flow Cytometry
Oxidative Stress
Cell Death
Iron
Glucose
Autosomal Recessive Cerebellar Ataxia Type 1

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Arginine deiminase in Staphylococcus epidermidis functions to augment biofilm maturation through pH homeostasis. / Lindgren, J. K.; Chittezham Thomas, Vinai; Olson, M. E.; Chaudhari, S. S.; Nuxoll, Austin S; Schaeffer, C. R.; Lindgren, K. E.; Jones, J.; Zimmerman, Matthew C; Dunman, P. M.; Bayles, Kenneth W; Fey, Paul D.

In: Journal of bacteriology, Vol. 196, No. 12, 2014, p. 2277-2289.

Research output: Contribution to journalArticle

Lindgren, J. K. ; Chittezham Thomas, Vinai ; Olson, M. E. ; Chaudhari, S. S. ; Nuxoll, Austin S ; Schaeffer, C. R. ; Lindgren, K. E. ; Jones, J. ; Zimmerman, Matthew C ; Dunman, P. M. ; Bayles, Kenneth W ; Fey, Paul D. / Arginine deiminase in Staphylococcus epidermidis functions to augment biofilm maturation through pH homeostasis. In: Journal of bacteriology. 2014 ; Vol. 196, No. 12. pp. 2277-2289.
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