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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Autores principales: Aimee K. Murray, Lihong Zhang, Xiaole Yin, Tong Zhang, Angus Buckling, Jason Snape, William H. Gaze
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Lenguaje:EN
Publicado: American Society for Microbiology 2018
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Acceso en línea:https://doaj.org/article/3faf00ab7c0540de97293cb46f4a7d5a
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spelling 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)
institution DOAJ
collection DOAJ
language EN
topic antibiotic resistance
evolution
metagenomics
microbial ecology
Microbiology
QR1-502
spellingShingle 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 AT aimeekmurray novelinsightsintoselectionforantibioticresistanceincomplexmicrobialcommunities
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