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Antibiotic-degrading resistance changes bacterial community structure via species-specific responses

Some bacterial resistance mechanisms degrade antibiotics, potentially protecting neighbouring susceptible cells from antibiotic exposure. We do not yet understand how such effects influence bacterial communities of more than two species, which are typical in nature. Here, we used experimental multis...

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Autores principales: Pathak, Ayush, Angst, Daniel C., León-Sampedro, Ricardo, Hall, Alex R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10432403/
https://www.ncbi.nlm.nih.gov/pubmed/37380830
http://dx.doi.org/10.1038/s41396-023-01465-2
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author Pathak, Ayush
Angst, Daniel C.
León-Sampedro, Ricardo
Hall, Alex R.
author_facet Pathak, Ayush
Angst, Daniel C.
León-Sampedro, Ricardo
Hall, Alex R.
author_sort Pathak, Ayush
collection PubMed
description Some bacterial resistance mechanisms degrade antibiotics, potentially protecting neighbouring susceptible cells from antibiotic exposure. We do not yet understand how such effects influence bacterial communities of more than two species, which are typical in nature. Here, we used experimental multispecies communities to test the effects of clinically important pOXA-48-plasmid-encoded resistance on community-level responses to antibiotics. We found that resistance in one community member reduced antibiotic inhibition of other species, but some benefitted more than others. Further experiments with supernatants and pure-culture growth assays showed the susceptible species profiting most from detoxification were those that grew best at degraded antibiotic concentrations (greater than zero, but lower than the starting concentration). This pattern was also observed on agar surfaces, and the same species also showed relatively high survival compared to most other species during the initial high-antibiotic phase. By contrast, we found no evidence of a role for higher-order interactions or horizontal plasmid transfer in community-level responses to detoxification in our experimental communities. Our findings suggest carriage of an antibiotic-degrading resistance mechanism by one species can drastically alter community-level responses to antibiotics, and the identities of the species that profit most from antibiotic detoxification are predicted by their intrinsic ability to survive and grow at changing antibiotic concentrations.
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spelling pubmed-104324032023-08-18 Antibiotic-degrading resistance changes bacterial community structure via species-specific responses Pathak, Ayush Angst, Daniel C. León-Sampedro, Ricardo Hall, Alex R. ISME J Article Some bacterial resistance mechanisms degrade antibiotics, potentially protecting neighbouring susceptible cells from antibiotic exposure. We do not yet understand how such effects influence bacterial communities of more than two species, which are typical in nature. Here, we used experimental multispecies communities to test the effects of clinically important pOXA-48-plasmid-encoded resistance on community-level responses to antibiotics. We found that resistance in one community member reduced antibiotic inhibition of other species, but some benefitted more than others. Further experiments with supernatants and pure-culture growth assays showed the susceptible species profiting most from detoxification were those that grew best at degraded antibiotic concentrations (greater than zero, but lower than the starting concentration). This pattern was also observed on agar surfaces, and the same species also showed relatively high survival compared to most other species during the initial high-antibiotic phase. By contrast, we found no evidence of a role for higher-order interactions or horizontal plasmid transfer in community-level responses to detoxification in our experimental communities. Our findings suggest carriage of an antibiotic-degrading resistance mechanism by one species can drastically alter community-level responses to antibiotics, and the identities of the species that profit most from antibiotic detoxification are predicted by their intrinsic ability to survive and grow at changing antibiotic concentrations. Nature Publishing Group UK 2023-06-29 2023-09 /pmc/articles/PMC10432403/ /pubmed/37380830 http://dx.doi.org/10.1038/s41396-023-01465-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Pathak, Ayush
Angst, Daniel C.
León-Sampedro, Ricardo
Hall, Alex R.
Antibiotic-degrading resistance changes bacterial community structure via species-specific responses
title Antibiotic-degrading resistance changes bacterial community structure via species-specific responses
title_full Antibiotic-degrading resistance changes bacterial community structure via species-specific responses
title_fullStr Antibiotic-degrading resistance changes bacterial community structure via species-specific responses
title_full_unstemmed Antibiotic-degrading resistance changes bacterial community structure via species-specific responses
title_short Antibiotic-degrading resistance changes bacterial community structure via species-specific responses
title_sort antibiotic-degrading resistance changes bacterial community structure via species-specific responses
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10432403/
https://www.ncbi.nlm.nih.gov/pubmed/37380830
http://dx.doi.org/10.1038/s41396-023-01465-2
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