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The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance

The TonB system is generally considered as an energy transporting device for the absorption of nutrients. Our recent study showed that deletion of this system caused a significantly increased sensitivity of Aeromonas hydrophila to the macrolides erythromycin and roxithromycin, but had no effect on o...

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Autores principales: Dong, Yuhao, Li, Qing, Geng, Jinzhu, Cao, Qing, Zhao, Dan, Jiang, Mingguo, Li, Shougang, Lu, Chengping, Liu, Yongjie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8082627/
https://www.ncbi.nlm.nih.gov/pubmed/33926565
http://dx.doi.org/10.1186/s13567-021-00934-w
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author Dong, Yuhao
Li, Qing
Geng, Jinzhu
Cao, Qing
Zhao, Dan
Jiang, Mingguo
Li, Shougang
Lu, Chengping
Liu, Yongjie
author_facet Dong, Yuhao
Li, Qing
Geng, Jinzhu
Cao, Qing
Zhao, Dan
Jiang, Mingguo
Li, Shougang
Lu, Chengping
Liu, Yongjie
author_sort Dong, Yuhao
collection PubMed
description The TonB system is generally considered as an energy transporting device for the absorption of nutrients. Our recent study showed that deletion of this system caused a significantly increased sensitivity of Aeromonas hydrophila to the macrolides erythromycin and roxithromycin, but had no effect on other classes of antibiotics. In this study, we found the sensitivity of ΔtonB123 to all macrolides tested revealed a 8- to 16-fold increase compared with the wild-type (WT) strain, but this increase was not related with iron deprivation caused by tonB123 deletion. Further study demonstrated that the deletion of tonB123 did not damage the integrity of the bacterial membrane but did hinder the function of macrolide efflux. Compared with the WT strain, deletion of macA(2)B(2), one of two ATP-binding cassette (ABC) types of the macrolide efflux pump, enhanced the sensitivity to the same levels as those of ΔtonB123. Interestingly, the deletion of macA(2)B(2) in the ΔtonB123 mutant did not cause further increase in sensitivity to macrolide resistance, indicating that the macrolide resistance afforded by the MacA(2)B(2) pump was completely abrogated by tonB123 deletion. In addition, macA(2)B(2) expression was not altered in the ΔtonB123 mutant, indicating that any influence of TonB on MacA(2)B(2)-mediated macrolide resistance was at the pump activity level. In conclusion, inactivation of the TonB system significantly compromises the resistance of A. hydrophila to macrolides, and the mechanism of action is related to the function of MacA(2)B(2)-mediated macrolide efflux. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-021-00934-w.
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spelling pubmed-80826272021-04-29 The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance Dong, Yuhao Li, Qing Geng, Jinzhu Cao, Qing Zhao, Dan Jiang, Mingguo Li, Shougang Lu, Chengping Liu, Yongjie Vet Res Research Article The TonB system is generally considered as an energy transporting device for the absorption of nutrients. Our recent study showed that deletion of this system caused a significantly increased sensitivity of Aeromonas hydrophila to the macrolides erythromycin and roxithromycin, but had no effect on other classes of antibiotics. In this study, we found the sensitivity of ΔtonB123 to all macrolides tested revealed a 8- to 16-fold increase compared with the wild-type (WT) strain, but this increase was not related with iron deprivation caused by tonB123 deletion. Further study demonstrated that the deletion of tonB123 did not damage the integrity of the bacterial membrane but did hinder the function of macrolide efflux. Compared with the WT strain, deletion of macA(2)B(2), one of two ATP-binding cassette (ABC) types of the macrolide efflux pump, enhanced the sensitivity to the same levels as those of ΔtonB123. Interestingly, the deletion of macA(2)B(2) in the ΔtonB123 mutant did not cause further increase in sensitivity to macrolide resistance, indicating that the macrolide resistance afforded by the MacA(2)B(2) pump was completely abrogated by tonB123 deletion. In addition, macA(2)B(2) expression was not altered in the ΔtonB123 mutant, indicating that any influence of TonB on MacA(2)B(2)-mediated macrolide resistance was at the pump activity level. In conclusion, inactivation of the TonB system significantly compromises the resistance of A. hydrophila to macrolides, and the mechanism of action is related to the function of MacA(2)B(2)-mediated macrolide efflux. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-021-00934-w. BioMed Central 2021-04-29 2021 /pmc/articles/PMC8082627/ /pubmed/33926565 http://dx.doi.org/10.1186/s13567-021-00934-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Dong, Yuhao
Li, Qing
Geng, Jinzhu
Cao, Qing
Zhao, Dan
Jiang, Mingguo
Li, Shougang
Lu, Chengping
Liu, Yongjie
The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance
title The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance
title_full The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance
title_fullStr The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance
title_full_unstemmed The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance
title_short The TonB system in Aeromonas hydrophila NJ-35 is essential for MacA(2)B(2) efflux pump-mediated macrolide resistance
title_sort tonb system in aeromonas hydrophila nj-35 is essential for maca(2)b(2) efflux pump-mediated macrolide resistance
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8082627/
https://www.ncbi.nlm.nih.gov/pubmed/33926565
http://dx.doi.org/10.1186/s13567-021-00934-w
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