Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>

ABSTRACT Subminimal inhibitory concentrations of antibiotics have been shown to induce bacterial biofilm formation. Few studies have investigated antibiotic-induced biofilm formation in Staphylococcus aureus, an important human pathogen. Our goal was to measure S. aureus biofilm formation in the pre...

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Autores principales:	Jeffrey B. Kaplan, Era A. Izano, Prerna Gopal, Michael T. Karwacki, Sangho Kim, Jeffrey L. Bose, Kenneth W. Bayles, Alexander R. Horswill
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cbeec9a045684a409c51fa8ca80fe88b
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spelling	oai:doaj.org-article:cbeec9a045684a409c51fa8ca80fe88b2021-11-15T15:39:09ZLow Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>10.1128/mBio.00198-122150-7511https://doaj.org/article/cbeec9a045684a409c51fa8ca80fe88b2012-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00198-12https://doaj.org/toc/2150-7511ABSTRACT Subminimal inhibitory concentrations of antibiotics have been shown to induce bacterial biofilm formation. Few studies have investigated antibiotic-induced biofilm formation in Staphylococcus aureus, an important human pathogen. Our goal was to measure S. aureus biofilm formation in the presence of low levels of β-lactam antibiotics. Fifteen phylogenetically diverse methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-sensitive S. aureus (MSSA) strains were employed. Methicillin, ampicillin, amoxicillin, and cloxacillin were added to cultures at concentrations ranging from 0× to 1× MIC. Biofilm formation was measured in 96-well microtiter plates using a crystal violet binding assay. Autoaggregation was measured using a visual test tube settling assay. Extracellular DNA was quantitated using agarose gel electrophoresis. All four antibiotics induced biofilm formation in some strains. The amount of biofilm induction was as high as 10-fold and was inversely proportional to the amount of biofilm produced by the strain in the absence of antibiotics. MRSA strains of lineages USA300, USA400, and USA500 exhibited the highest levels of methicillin-induced biofilm induction. Biofilm formation induced by low-level methicillin was inhibited by DNase. Low-level methicillin also induced DNase-sensitive autoaggregation and extracellular DNA release. The biofilm induction phenotype was absent in a strain deficient in autolysin (atl). Our findings demonstrate that subminimal inhibitory concentrations of β-lactam antibiotics significantly induce autolysin-dependent extracellular DNA release and biofilm formation in some strains of S. aureus. IMPORTANCE The widespread use of antibiotics as growth promoters in agriculture may expose bacteria to low levels of the drugs. The aim of this study was to investigate the effects of low levels of antibiotics on bacterial autoaggregation and biofilm formation, two processes that have been shown to foster genetic exchange and antibiotic resistance. We found that low levels of β-lactam antibiotics, a class commonly used in both clinical and agricultural settings, caused significant autoaggregation and biofilm formation by the important human pathogen Staphylococcus aureus. Both processes were dependent on cell lysis and release of DNA into the environment. The effect was most pronounced among multidrug-resistant strains known as methicillin-resistant S. aureus (MRSA). These results may shed light on the recalcitrance of some bacterial infections to antibiotic treatment in clinical settings and the evolution of antibiotic-resistant bacteria in agricultural settings.Jeffrey B. KaplanEra A. IzanoPrerna GopalMichael T. KarwackiSangho KimJeffrey L. BoseKenneth W. BaylesAlexander R. HorswillAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 4 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Jeffrey B. Kaplan Era A. Izano Prerna Gopal Michael T. Karwacki Sangho Kim Jeffrey L. Bose Kenneth W. Bayles Alexander R. Horswill Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>
description	ABSTRACT Subminimal inhibitory concentrations of antibiotics have been shown to induce bacterial biofilm formation. Few studies have investigated antibiotic-induced biofilm formation in Staphylococcus aureus, an important human pathogen. Our goal was to measure S. aureus biofilm formation in the presence of low levels of β-lactam antibiotics. Fifteen phylogenetically diverse methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-sensitive S. aureus (MSSA) strains were employed. Methicillin, ampicillin, amoxicillin, and cloxacillin were added to cultures at concentrations ranging from 0× to 1× MIC. Biofilm formation was measured in 96-well microtiter plates using a crystal violet binding assay. Autoaggregation was measured using a visual test tube settling assay. Extracellular DNA was quantitated using agarose gel electrophoresis. All four antibiotics induced biofilm formation in some strains. The amount of biofilm induction was as high as 10-fold and was inversely proportional to the amount of biofilm produced by the strain in the absence of antibiotics. MRSA strains of lineages USA300, USA400, and USA500 exhibited the highest levels of methicillin-induced biofilm induction. Biofilm formation induced by low-level methicillin was inhibited by DNase. Low-level methicillin also induced DNase-sensitive autoaggregation and extracellular DNA release. The biofilm induction phenotype was absent in a strain deficient in autolysin (atl). Our findings demonstrate that subminimal inhibitory concentrations of β-lactam antibiotics significantly induce autolysin-dependent extracellular DNA release and biofilm formation in some strains of S. aureus. IMPORTANCE The widespread use of antibiotics as growth promoters in agriculture may expose bacteria to low levels of the drugs. The aim of this study was to investigate the effects of low levels of antibiotics on bacterial autoaggregation and biofilm formation, two processes that have been shown to foster genetic exchange and antibiotic resistance. We found that low levels of β-lactam antibiotics, a class commonly used in both clinical and agricultural settings, caused significant autoaggregation and biofilm formation by the important human pathogen Staphylococcus aureus. Both processes were dependent on cell lysis and release of DNA into the environment. The effect was most pronounced among multidrug-resistant strains known as methicillin-resistant S. aureus (MRSA). These results may shed light on the recalcitrance of some bacterial infections to antibiotic treatment in clinical settings and the evolution of antibiotic-resistant bacteria in agricultural settings.
format	article
author	Jeffrey B. Kaplan Era A. Izano Prerna Gopal Michael T. Karwacki Sangho Kim Jeffrey L. Bose Kenneth W. Bayles Alexander R. Horswill
author_facet	Jeffrey B. Kaplan Era A. Izano Prerna Gopal Michael T. Karwacki Sangho Kim Jeffrey L. Bose Kenneth W. Bayles Alexander R. Horswill
author_sort	Jeffrey B. Kaplan
title	Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_short	Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_full	Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_fullStr	Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_full_unstemmed	Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>
title_sort	low levels of β-lactam antibiotics induce extracellular dna release and biofilm formation in <named-content content-type="genus-species">staphylococcus aureus</named-content>
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/cbeec9a045684a409c51fa8ca80fe88b
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Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in <named-content content-type="genus-species">Staphylococcus aureus</named-content>

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