Intrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride

ABSTRACT Pharmaceutical products that are contaminated with Burkholderia cepacia complex (BCC) bacteria may pose serious consequences to vulnerable patients. Benzyldimethylalkylammonium chloride (BZK) cationic surfactants are extensively used in medical applications and have been implicated in the c...

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Autores principales: Youngbeom Ahn, Jeong Myeong Kim, Ohgew Kweon, Seong-Jae Kim, Richard C. Jones, Kellie Woodling, Gonçalo Gamboa da Costa, John J. LiPuma, David Hussong, Bernard S. Marasa, Carl E. Cerniglia
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:0f299cf8a8184489aefea2deec489ba02021-11-15T15:50:15ZIntrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride10.1128/mBio.01716-162150-7511https://doaj.org/article/0f299cf8a8184489aefea2deec489ba02016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01716-16https://doaj.org/toc/2150-7511ABSTRACT Pharmaceutical products that are contaminated with Burkholderia cepacia complex (BCC) bacteria may pose serious consequences to vulnerable patients. Benzyldimethylalkylammonium chloride (BZK) cationic surfactants are extensively used in medical applications and have been implicated in the coselection of antimicrobial resistance. The ability of BCC to degrade BZK, tetradecyldimethylbenzylammonium chloride (C14BDMA-Cl), dodecyldimethylbenzylammonium chloride (C12BDMA-Cl), decyldimethylbenzylammonium chloride (C10BDMA-Cl), hexyldimethylbenzylammonium chloride, and benzyltrimethylammonium chloride was determined by incubation in 1/10-diluted tryptic soy broth (TSB) to determine if BCC bacteria have the ability to survive and inactivate these disinfectants. With BZK, C14BDMA-Cl, and C12BDMA-Cl, inhibition of the growth of 20 BCC strains was observed in disinfectant solutions that ranged from 64 to 256 µg/ml. The efflux pump inhibitor carbonyl cyanide m-chlorophenylhydrazone increased the sensitivity of bacteria to 64 µg/ml BZK. The 20 BCC strains grew well in 1/10-diluted TSB medium with BZK, C12BDMA-Cl, and C10BDMA-Cl; they absorbed and degraded the compounds in 7 days. Formation of benzyldimethylamine and benzylmethylamine as the initial metabolites suggested that the cleavage of the C alkyl-N bond occurred as the first step of BZK degradation by BCC bacteria. Proteomic data confirmed the observed efflux activity and metabolic inactivation via biodegradation in terms of BZK resistance of BCC bacteria, which suggests that the two main resistance mechanisms are intrinsic and widespread. IMPORTANCE Benzyldimethylalkylammonium chloride is commonly used as an antiseptic in the United States. Several recent microbial outbreaks were linked to antiseptics that were found to contain strains of the Burkholderia cepacia complex. Burkholderia species survived in antiseptics, possibly because of the degradation of antiseptic molecules or regulation of relevant gene expression. In this study, we assessed the efflux pump and the potential of B. cepacia complex bacteria to degrade benzyldimethylalkylammonium chloride and improved our understanding of the resistance mechanisms, by using proteomic and metabolic information. To our knowledge, this is the first systematic report of the intrinsic mechanisms of B. cepacia complex strain resistance to benzyldimethylalkylammonium chloride, based on the metabolic and proteomic evidence for efflux pumps and the complete biodegradation of benzyldimethylalkylammonium chloride.Youngbeom AhnJeong Myeong KimOhgew KweonSeong-Jae KimRichard C. JonesKellie WoodlingGonçalo Gamboa da CostaJohn J. LiPumaDavid HussongBernard S. MarasaCarl E. CernigliaAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 6 (2016)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Youngbeom Ahn
Jeong Myeong Kim
Ohgew Kweon
Seong-Jae Kim
Richard C. Jones
Kellie Woodling
Gonçalo Gamboa da Costa
John J. LiPuma
David Hussong
Bernard S. Marasa
Carl E. Cerniglia
Intrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride
description ABSTRACT Pharmaceutical products that are contaminated with Burkholderia cepacia complex (BCC) bacteria may pose serious consequences to vulnerable patients. Benzyldimethylalkylammonium chloride (BZK) cationic surfactants are extensively used in medical applications and have been implicated in the coselection of antimicrobial resistance. The ability of BCC to degrade BZK, tetradecyldimethylbenzylammonium chloride (C14BDMA-Cl), dodecyldimethylbenzylammonium chloride (C12BDMA-Cl), decyldimethylbenzylammonium chloride (C10BDMA-Cl), hexyldimethylbenzylammonium chloride, and benzyltrimethylammonium chloride was determined by incubation in 1/10-diluted tryptic soy broth (TSB) to determine if BCC bacteria have the ability to survive and inactivate these disinfectants. With BZK, C14BDMA-Cl, and C12BDMA-Cl, inhibition of the growth of 20 BCC strains was observed in disinfectant solutions that ranged from 64 to 256 µg/ml. The efflux pump inhibitor carbonyl cyanide m-chlorophenylhydrazone increased the sensitivity of bacteria to 64 µg/ml BZK. The 20 BCC strains grew well in 1/10-diluted TSB medium with BZK, C12BDMA-Cl, and C10BDMA-Cl; they absorbed and degraded the compounds in 7 days. Formation of benzyldimethylamine and benzylmethylamine as the initial metabolites suggested that the cleavage of the C alkyl-N bond occurred as the first step of BZK degradation by BCC bacteria. Proteomic data confirmed the observed efflux activity and metabolic inactivation via biodegradation in terms of BZK resistance of BCC bacteria, which suggests that the two main resistance mechanisms are intrinsic and widespread. IMPORTANCE Benzyldimethylalkylammonium chloride is commonly used as an antiseptic in the United States. Several recent microbial outbreaks were linked to antiseptics that were found to contain strains of the Burkholderia cepacia complex. Burkholderia species survived in antiseptics, possibly because of the degradation of antiseptic molecules or regulation of relevant gene expression. In this study, we assessed the efflux pump and the potential of B. cepacia complex bacteria to degrade benzyldimethylalkylammonium chloride and improved our understanding of the resistance mechanisms, by using proteomic and metabolic information. To our knowledge, this is the first systematic report of the intrinsic mechanisms of B. cepacia complex strain resistance to benzyldimethylalkylammonium chloride, based on the metabolic and proteomic evidence for efflux pumps and the complete biodegradation of benzyldimethylalkylammonium chloride.
format article
author Youngbeom Ahn
Jeong Myeong Kim
Ohgew Kweon
Seong-Jae Kim
Richard C. Jones
Kellie Woodling
Gonçalo Gamboa da Costa
John J. LiPuma
David Hussong
Bernard S. Marasa
Carl E. Cerniglia
author_facet Youngbeom Ahn
Jeong Myeong Kim
Ohgew Kweon
Seong-Jae Kim
Richard C. Jones
Kellie Woodling
Gonçalo Gamboa da Costa
John J. LiPuma
David Hussong
Bernard S. Marasa
Carl E. Cerniglia
author_sort Youngbeom Ahn
title Intrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride
title_short Intrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride
title_full Intrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride
title_fullStr Intrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride
title_full_unstemmed Intrinsic Resistance of <named-content content-type="genus-species">Burkholderia cepacia</named-content> Complex to Benzalkonium Chloride
title_sort intrinsic resistance of <named-content content-type="genus-species">burkholderia cepacia</named-content> complex to benzalkonium chloride
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/0f299cf8a8184489aefea2deec489ba0
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