Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations
Surface disinfectants are regularly used in prophylactic and infection control measures. Concern has been raised whether residues of sub-inhibitory disinfectant concentrations may constitute a selective pressure and could contribute to the development of strains which are tolerant and/or resistant t...
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| Format: | Article |
| Language: | English |
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Elsevier
2020-06-01
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| Series: | Heliyon |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2405844020309142 |
| _version_ | 1818217872319578112 |
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| author | Stephanie Speck Cindy Wenke Andrea T. Feßler Johannes Kacza Franziska Geber Anissa D. Scholtzek Dennis Hanke Inga Eichhorn Stefan Schwarz Maciej Rosolowski Uwe Truyen |
| author_facet | Stephanie Speck Cindy Wenke Andrea T. Feßler Johannes Kacza Franziska Geber Anissa D. Scholtzek Dennis Hanke Inga Eichhorn Stefan Schwarz Maciej Rosolowski Uwe Truyen |
| author_sort | Stephanie Speck |
| collection | DOAJ |
| description | Surface disinfectants are regularly used in prophylactic and infection control measures. Concern has been raised whether residues of sub-inhibitory disinfectant concentrations may constitute a selective pressure and could contribute to the development of strains which are tolerant and/or resistant to biocides including antibiotics. The current study investigated whether Staphylococcus (S.) aureus ATCC® 29213™ and ATCC® 6538™ would change their growth characteristics and antimicrobial susceptibility profiles after prolonged treatment with sub-inhibitory concentrations of sodium hypochlorite (NaOCl). NaOCl is a fast-acting disinfectant with a broad-spectrum activity, inexpensive and widely used in healthcare and the food production industry. Minimum inhibitory concentration (MIC) for NaOCl was determined by broth macrodilution according to the guidelines for disinfectant efficacy testing provided by the German Veterinary Medical Society. Serial passages after 24 h and 72 h, respectively, in defined sub-inhibitory concentrations of NaOCl resulted in a number of phenotypic variants. Two of these variants, derived from S. aureus ATCC® 29213™, showed elevated MICs of oxacillin and were considered as in vitro-generated borderline oxacillin-resistant S. aureus (BORSA). Transmission electron microscopy revealed a significantly thickened cell wall in these isolates, a phenomenon that has also been described for Listeria monocytogenes after low-level exposure to NaOCl. Whole genome sequencing revealed an early stop codon in the gene coding for the GdpP protein and thereby abolishing the function of this gene. GdpP represents a phosphodiesterase that regulates gene expression, and loss of function of the GdpP protein has been described in association with borderline oxacillin resistance. Our findings suggest that a mutation in the GdpP protein gene and morphological changes of the cell wall were induced by repeated exposure to sub-lethal NaOCl concentrations, and most likely accounted for a BORSA phenotype in two variants derived from S. aureus ATCC® 29213™. |
| first_indexed | 2024-12-12T07:14:46Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 2405-8440 |
| language | English |
| last_indexed | 2024-12-12T07:14:46Z |
| publishDate | 2020-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Heliyon |
| spelling | doaj.art-5c54dde00d294ca68acbb44bf186b9f02022-12-22T00:33:33ZengElsevierHeliyon2405-84402020-06-0166e04070Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrationsStephanie Speck0Cindy Wenke1Andrea T. Feßler2Johannes Kacza3Franziska Geber4Anissa D. Scholtzek5Dennis Hanke6Inga Eichhorn7Stefan Schwarz8Maciej Rosolowski9Uwe Truyen10Institute of Animal Hygiene and Veterinary Public Health, University of Leipzig, Leipzig, Germany; Corresponding author.Institute of Animal Hygiene and Veterinary Public Health, University of Leipzig, Leipzig, GermanyInstitute of Microbiology and Epizootics, Centre of Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyBioImaging Core Facility, VMF/SIKT, University of Leipzig, Leipzig, GermanyInstitute of Animal Hygiene and Veterinary Public Health, University of Leipzig, Leipzig, GermanyInstitute of Microbiology and Epizootics, Centre of Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyInstitute of Microbiology and Epizootics, Centre of Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyInstitute of Microbiology and Epizootics, Centre of Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyInstitute of Microbiology and Epizootics, Centre of Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyInstitute for Medical Informatics, Statistics and Epidemiology (IMISE), University of Leipzig, Leipzig, GermanyInstitute of Animal Hygiene and Veterinary Public Health, University of Leipzig, Leipzig, GermanySurface disinfectants are regularly used in prophylactic and infection control measures. Concern has been raised whether residues of sub-inhibitory disinfectant concentrations may constitute a selective pressure and could contribute to the development of strains which are tolerant and/or resistant to biocides including antibiotics. The current study investigated whether Staphylococcus (S.) aureus ATCC® 29213™ and ATCC® 6538™ would change their growth characteristics and antimicrobial susceptibility profiles after prolonged treatment with sub-inhibitory concentrations of sodium hypochlorite (NaOCl). NaOCl is a fast-acting disinfectant with a broad-spectrum activity, inexpensive and widely used in healthcare and the food production industry. Minimum inhibitory concentration (MIC) for NaOCl was determined by broth macrodilution according to the guidelines for disinfectant efficacy testing provided by the German Veterinary Medical Society. Serial passages after 24 h and 72 h, respectively, in defined sub-inhibitory concentrations of NaOCl resulted in a number of phenotypic variants. Two of these variants, derived from S. aureus ATCC® 29213™, showed elevated MICs of oxacillin and were considered as in vitro-generated borderline oxacillin-resistant S. aureus (BORSA). Transmission electron microscopy revealed a significantly thickened cell wall in these isolates, a phenomenon that has also been described for Listeria monocytogenes after low-level exposure to NaOCl. Whole genome sequencing revealed an early stop codon in the gene coding for the GdpP protein and thereby abolishing the function of this gene. GdpP represents a phosphodiesterase that regulates gene expression, and loss of function of the GdpP protein has been described in association with borderline oxacillin resistance. Our findings suggest that a mutation in the GdpP protein gene and morphological changes of the cell wall were induced by repeated exposure to sub-lethal NaOCl concentrations, and most likely accounted for a BORSA phenotype in two variants derived from S. aureus ATCC® 29213™.http://www.sciencedirect.com/science/article/pii/S2405844020309142MicrobiologyAntibiotic resistant bacteriaAntimicrobialBacteriologyHealth sciencesStaphylococcus |
| spellingShingle | Stephanie Speck Cindy Wenke Andrea T. Feßler Johannes Kacza Franziska Geber Anissa D. Scholtzek Dennis Hanke Inga Eichhorn Stefan Schwarz Maciej Rosolowski Uwe Truyen Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations Heliyon Microbiology Antibiotic resistant bacteria Antimicrobial Bacteriology Health sciences Staphylococcus |
| title | Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations |
| title_full | Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations |
| title_fullStr | Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations |
| title_full_unstemmed | Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations |
| title_short | Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations |
| title_sort | borderline resistance to oxacillin in staphylococcus aureus after treatment with sub lethal sodium hypochlorite concentrations |
| topic | Microbiology Antibiotic resistant bacteria Antimicrobial Bacteriology Health sciences Staphylococcus |
| url | http://www.sciencedirect.com/science/article/pii/S2405844020309142 |
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