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Biotechnology

Unprotonated Short-Chain Alkylamines Inhibit Staphylolytic Activity of Lysostaphin in a Wall Teichoic Acid-Dependent Manner

Xia Wu, Seok Joon Kwon, Domyoung Kim, Jian Zha, Mauricio Mora-Pale, Jonathan S. Dordick
Robert M. Kelly, Editor
Xia Wu
Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
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Seok Joon Kwon
Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
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Domyoung Kim
Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
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Jian Zha
Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
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Mauricio Mora-Pale
Global Home Care Early Research and Formula Fundamentals (MX-GTC), Colgate-Palmolive, Colonia Granada, Mexico City, Mexico
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Jonathan S. Dordick
Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USADepartment of Chemical and Biological Engineering, Department of Biomedical Engineering, and Department of Biology, Rensselaer Polytechnic Institute, Troy, New York, USA
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Robert M. Kelly
North Carolina State University
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DOI: 10.1128/AEM.00693-18
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ABSTRACT

Lysostaphin (Lst) is a potent bacteriolytic enzyme that kills Staphylococcus aureus, a common bacterial pathogen of humans and animals. With high activity against both planktonic cells and biofilms, Lst has the potential to be used in industrial products, such as commercial cleansers, for decontamination. However, Lst is inhibited in the presence of monoethanolamine (MEA), a chemical widely used in cleaning solutions and pharmaceuticals, and the underlying mechanism of inhibition remains unknown. In this study, we examined the cell binding and killing capabilities of Lst against S. aureus ATCC 6538 in buffered salt solution with MEA at different pH values (7.5 to 10.5) and discovered that only the unprotonated form of MEA inhibited Lst binding to the cell surface, leading to low Lst activity, despite retention of its secondary structure. This reduced enzyme activity could be largely recovered via a reduction in wall teichoic acid (WTA) biosynthesis through tunicamycin treatment, indicating that the suppression of Lst activity was dependent on the presence and amount of WTA. We propose that the decreased cell binding and killing capabilities of Lst are associated with the influence of uncharged MEA on the conformation of WTA. A similar effect was confirmed with other short-chain alkylamines. This study offers new insight into the impact of short-chain alkylamines on both Lst and WTA structure and function and provides guidance for the application of Lst in harsh environments.

IMPORTANCE Lysostaphin (Lst) effectively and selectively kills Staphylococcus aureus, the bacterial culprit of many hospital- and community-acquired skin and respiratory infections and food poisoning. Lst has been investigated in animal models and clinical trials, industrial formulations, and environmental settings. Here, we studied the mechanistic basis of the inhibitory effect of alkylamines, such as monoethanolamine (MEA), a widely used chemical in commercial detergents, on Lst activity, for the potential incorporation of Lst in disinfectant solutions. We have found that protonated MEA has little influence on Lst activity, while unprotonated MEA prevents Lst from binding to S. aureus cells and hence dramatically decreases the enzyme's bacteriolytic efficacy. Following partial removal of the wall teichoic acid, an important component of the bacterial cell envelope, the inhibitory effect of unprotonated MEA on Lst is reduced. This phenomenon can be extended to other short-chain alkylamines. This mechanistic report of the impact of alkylamines on Lst functionality will help guide future applications of Lst in disinfection and decontamination of health-related commercial products.

FOOTNOTES

    • Received 24 March 2018.
    • Accepted 1 May 2018.
    • Accepted manuscript posted online 4 May 2018.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.00693-18.

  • Copyright © 2018 American Society for Microbiology.

All Rights Reserved.

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Unprotonated Short-Chain Alkylamines Inhibit Staphylolytic Activity of Lysostaphin in a Wall Teichoic Acid-Dependent Manner
Xia Wu, Seok Joon Kwon, Domyoung Kim, Jian Zha, Mauricio Mora-Pale, Jonathan S. Dordick
Appl. Environ. Microbiol. Jul 2018, 84 (14) e00693-18; DOI: 10.1128/AEM.00693-18

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Unprotonated Short-Chain Alkylamines Inhibit Staphylolytic Activity of Lysostaphin in a Wall Teichoic Acid-Dependent Manner
Xia Wu, Seok Joon Kwon, Domyoung Kim, Jian Zha, Mauricio Mora-Pale, Jonathan S. Dordick
Appl. Environ. Microbiol. Jul 2018, 84 (14) e00693-18; DOI: 10.1128/AEM.00693-18
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KEYWORDS

Staphylococcus aureus
lysostaphin
peptidoglycan
tunicamycin
unprotonated amine
wall teichoic acids

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