Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities
ABSTRACT Recent research has demonstrated that selection for antibiotic resistance occurs at very low antibiotic concentrations in single-species experiments, but the relevance of these findings when species are embedded in complex microbial communities is unclear. We show that the strength of selec...
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American Society for Microbiology
2018
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oai:doaj.org-article:3faf00ab7c0540de97293cb46f4a7d5a2021-11-15T16:00:15ZNovel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities10.1128/mBio.00969-182150-7511https://doaj.org/article/3faf00ab7c0540de97293cb46f4a7d5a2018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00969-18https://doaj.org/toc/2150-7511ABSTRACT Recent research has demonstrated that selection for antibiotic resistance occurs at very low antibiotic concentrations in single-species experiments, but the relevance of these findings when species are embedded in complex microbial communities is unclear. We show that the strength of selection for naturally occurring resistance alleles in a complex community remains constant from low subinhibitory to above clinically relevant concentrations. Selection increases with antibiotic concentration before reaching a plateau where selection remains constant over a 2-order-magnitude concentration range. This is likely to be due to cross protection of the susceptible bacteria in the community following rapid extracellular antibiotic degradation by the resistant population, shown experimentally through a combination of chemical quantification and bacterial growth experiments. Metagenome and 16S rRNA analyses of sewage-derived bacterial communities evolved under cefotaxime exposure show preferential enrichment for blaCTX-M genes over all other beta-lactamase genes, as well as positive selection and co-selection for antibiotic resistant, opportunistic pathogens. These findings have far-reaching implications for our understanding of the evolution of antibiotic resistance, by challenging the long-standing assumption that selection occurs in a dose-dependent manner. IMPORTANCE Antibiotic resistance is one of the greatest global issues facing society. Still, comparatively little is known about selection for resistance at very low antibiotic concentrations. We show that the strength of selection for clinically important resistance genes within a complex bacterial community can remain constant across a large antibiotic concentration range (wide selective space). Therefore, largely understudied ecological compartments could be just as important as clinical environments for selection of antibiotic resistance.Aimee K. MurrayLihong ZhangXiaole YinTong ZhangAngus BucklingJason SnapeWilliam H. GazeAmerican Society for Microbiologyarticleantibiotic resistanceevolutionmetagenomicsmicrobial ecologyMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018) |
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antibiotic resistance evolution metagenomics microbial ecology Microbiology QR1-502 |
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antibiotic resistance evolution metagenomics microbial ecology Microbiology QR1-502 Aimee K. Murray Lihong Zhang Xiaole Yin Tong Zhang Angus Buckling Jason Snape William H. Gaze Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities |
description |
ABSTRACT Recent research has demonstrated that selection for antibiotic resistance occurs at very low antibiotic concentrations in single-species experiments, but the relevance of these findings when species are embedded in complex microbial communities is unclear. We show that the strength of selection for naturally occurring resistance alleles in a complex community remains constant from low subinhibitory to above clinically relevant concentrations. Selection increases with antibiotic concentration before reaching a plateau where selection remains constant over a 2-order-magnitude concentration range. This is likely to be due to cross protection of the susceptible bacteria in the community following rapid extracellular antibiotic degradation by the resistant population, shown experimentally through a combination of chemical quantification and bacterial growth experiments. Metagenome and 16S rRNA analyses of sewage-derived bacterial communities evolved under cefotaxime exposure show preferential enrichment for blaCTX-M genes over all other beta-lactamase genes, as well as positive selection and co-selection for antibiotic resistant, opportunistic pathogens. These findings have far-reaching implications for our understanding of the evolution of antibiotic resistance, by challenging the long-standing assumption that selection occurs in a dose-dependent manner. IMPORTANCE Antibiotic resistance is one of the greatest global issues facing society. Still, comparatively little is known about selection for resistance at very low antibiotic concentrations. We show that the strength of selection for clinically important resistance genes within a complex bacterial community can remain constant across a large antibiotic concentration range (wide selective space). Therefore, largely understudied ecological compartments could be just as important as clinical environments for selection of antibiotic resistance. |
format |
article |
author |
Aimee K. Murray Lihong Zhang Xiaole Yin Tong Zhang Angus Buckling Jason Snape William H. Gaze |
author_facet |
Aimee K. Murray Lihong Zhang Xiaole Yin Tong Zhang Angus Buckling Jason Snape William H. Gaze |
author_sort |
Aimee K. Murray |
title |
Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities |
title_short |
Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities |
title_full |
Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities |
title_fullStr |
Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities |
title_full_unstemmed |
Novel Insights into Selection for Antibiotic Resistance in Complex Microbial Communities |
title_sort |
novel insights into selection for antibiotic resistance in complex microbial communities |
publisher |
American Society for Microbiology |
publishDate |
2018 |
url |
https://doaj.org/article/3faf00ab7c0540de97293cb46f4a7d5a |
work_keys_str_mv |
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_version_ |
1718426961158602752 |