Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communities

The effects of sub-minimum inhibitory concentrations (sub-MICs) of antibiotics on aquatic environments is not yet fully understood. Here, we explore these effects by employing a replicated microcosm system fed with river water where biofilm communities were continuously exposed over an eight-week pe...

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Main Authors: Gabriela Flores-Vargas, Darren R. Korber, Jordyn Bergsveinson
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1194952/full
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author Gabriela Flores-Vargas
Darren R. Korber
Jordyn Bergsveinson
author_facet Gabriela Flores-Vargas
Darren R. Korber
Jordyn Bergsveinson
author_sort Gabriela Flores-Vargas
collection DOAJ
description The effects of sub-minimum inhibitory concentrations (sub-MICs) of antibiotics on aquatic environments is not yet fully understood. Here, we explore these effects by employing a replicated microcosm system fed with river water where biofilm communities were continuously exposed over an eight-week period to sub-MIC exposure (1/10, 1/50, and 1/100 MIC) to a mix of common antibiotics (ciprofloxacin, streptomycin, and oxytetracycline). Biofilms were examined using a structure–function approach entailing microscopy and metagenomic techniques, revealing details on the microbiome, resistome, virulome, and functional prediction. A comparison of three commonly used microbiome and resistome databases was also performed. Differences in biofilm architecture were observed between sub-MIC antibiotic treatments, with an overall reduction of extracellular polymeric substances and autotroph (algal and cyanobacteria) and protozoan biomass, particularly at the 1/10 sub-MIC condition. While metagenomic analyses demonstrated that microbial diversity was lowest at the sub-MIC 1/10 antibiotic treatment, resistome diversity was highest at sub-MIC 1/50. This study also notes the importance of benchmarking analysis tools and careful selection of reference databases, given the disparity in detected antimicrobial resistance genes (ARGs) identity and abundance across methods. Ultimately, the most detected ARGs in sub-MICs exposed biofilms were those that conferred resistance to aminoglycosides, tetracyclines, β-lactams, sulfonamides, and trimethoprim. Co-occurrence of microbiome and resistome features consistently showed a relationship between Proteobacteria genera and aminoglycoside ARGs. Our results support the hypothesis that constant exposure to sub-MICs antibiotics facilitate the transmission and promote prevalence of antibiotic resistance in riverine biofilms communities, and additionally shift overall microbial community metabolic function.
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spelling doaj.art-7a26cbc89d5c4fea94562d252da7f5382023-08-01T09:14:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-08-011410.3389/fmicb.2023.11949521194952Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communitiesGabriela Flores-Vargas0Darren R. Korber1Jordyn Bergsveinson2Food and Bioproduct Sciences, University of Saskatchewan, Saskatoon, SK, CanadaFood and Bioproduct Sciences, University of Saskatchewan, Saskatoon, SK, CanadaWatershed Hydrology and Ecology Research Division, Environment and Climate Change Canada, Saskatoon, SK, CanadaThe effects of sub-minimum inhibitory concentrations (sub-MICs) of antibiotics on aquatic environments is not yet fully understood. Here, we explore these effects by employing a replicated microcosm system fed with river water where biofilm communities were continuously exposed over an eight-week period to sub-MIC exposure (1/10, 1/50, and 1/100 MIC) to a mix of common antibiotics (ciprofloxacin, streptomycin, and oxytetracycline). Biofilms were examined using a structure–function approach entailing microscopy and metagenomic techniques, revealing details on the microbiome, resistome, virulome, and functional prediction. A comparison of three commonly used microbiome and resistome databases was also performed. Differences in biofilm architecture were observed between sub-MIC antibiotic treatments, with an overall reduction of extracellular polymeric substances and autotroph (algal and cyanobacteria) and protozoan biomass, particularly at the 1/10 sub-MIC condition. While metagenomic analyses demonstrated that microbial diversity was lowest at the sub-MIC 1/10 antibiotic treatment, resistome diversity was highest at sub-MIC 1/50. This study also notes the importance of benchmarking analysis tools and careful selection of reference databases, given the disparity in detected antimicrobial resistance genes (ARGs) identity and abundance across methods. Ultimately, the most detected ARGs in sub-MICs exposed biofilms were those that conferred resistance to aminoglycosides, tetracyclines, β-lactams, sulfonamides, and trimethoprim. Co-occurrence of microbiome and resistome features consistently showed a relationship between Proteobacteria genera and aminoglycoside ARGs. Our results support the hypothesis that constant exposure to sub-MICs antibiotics facilitate the transmission and promote prevalence of antibiotic resistance in riverine biofilms communities, and additionally shift overall microbial community metabolic function.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1194952/fullantibioticsantibiotic resistancebiofilmsenvironmental resistomemicrobiomesub-MIC
spellingShingle Gabriela Flores-Vargas
Darren R. Korber
Jordyn Bergsveinson
Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communities
Frontiers in Microbiology
antibiotics
antibiotic resistance
biofilms
environmental resistome
microbiome
sub-MIC
title Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communities
title_full Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communities
title_fullStr Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communities
title_full_unstemmed Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communities
title_short Sub-MIC antibiotics influence the microbiome, resistome and structure of riverine biofilm communities
title_sort sub mic antibiotics influence the microbiome resistome and structure of riverine biofilm communities
topic antibiotics
antibiotic resistance
biofilms
environmental resistome
microbiome
sub-MIC
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1194952/full
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AT jordynbergsveinson submicantibioticsinfluencethemicrobiomeresistomeandstructureofriverinebiofilmcommunities