Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors

ABSTRACT Humans purposefully and inadvertently introduce antimicrobial chemicals into buildings, resulting in widespread compounds, including triclosan, triclocarban, and parabens, in indoor dust. Meanwhile, drug-resistant infections continue to increase, raising concerns that buildings function as...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Ashkaan K. Fahimipour, Sarah Ben Maamar, Alexander G. McFarland, Ryan A. Blaustein, Jing Chen, Adam J. Glawe, Jeff Kline, Jessica L. Green, Rolf U. Halden, Kevin Van Den Wymelenberg, Curtis Huttenhower, Erica M. Hartmann
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://doaj.org/article/e37cc68048524abf88b55ec0e851cf40
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:e37cc68048524abf88b55ec0e851cf40
record_format dspace
spelling oai:doaj.org-article:e37cc68048524abf88b55ec0e851cf402021-12-02T19:46:17ZAntimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors10.1128/mSystems.00200-182379-5077https://doaj.org/article/e37cc68048524abf88b55ec0e851cf402018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00200-18https://doaj.org/toc/2379-5077ABSTRACT Humans purposefully and inadvertently introduce antimicrobial chemicals into buildings, resulting in widespread compounds, including triclosan, triclocarban, and parabens, in indoor dust. Meanwhile, drug-resistant infections continue to increase, raising concerns that buildings function as reservoirs of, or even select for, resistant microorganisms. Support for these hypotheses is limited largely since data describing relationships between antimicrobials and indoor microbial communities are scant. We combined liquid chromatography-isotope dilution tandem mass spectrometry with metagenomic shotgun sequencing of dust collected from athletic facilities to characterize relationships between indoor antimicrobial chemicals and microbial communities. Elevated levels of triclosan and triclocarban, but not parabens, were associated with distinct indoor microbiomes. Dust of high triclosan content contained increased Gram-positive species with diverse drug resistance capabilities, whose pangenomes were enriched for genes encoding osmotic stress responses, efflux pump regulation, lipid metabolism, and material transport across cell membranes; such triclosan-associated functional shifts have been documented in laboratory cultures but not yet from buildings. Antibiotic-resistant bacterial isolates were cultured from all but one facility, and resistance often increased in buildings with very high triclosan levels, suggesting links between human encounters with viable drug-resistant bacteria and local biocide conditions. This characterization uncovers complex relationships between antimicrobials and indoor microbiomes: some chemicals elicit effects, whereas others may not, and no single functional or resistance factor explained chemical-microbe associations. These results suggest that anthropogenic chemicals impact microbial systems in or around buildings and their occupants, highlighting an emergent need to identify the most important indoor, outdoor, and host-associated sources of antimicrobial chemical-resistome interactions. IMPORTANCE The ubiquitous use of antimicrobial chemicals may have undesired consequences, particularly on microbes in buildings. This study shows that the taxonomy and function of microbes in indoor dust are strongly associated with antimicrobial chemicals—more so than any other feature of the buildings. Moreover, we identified links between antimicrobial chemical concentrations in dust and culturable bacteria that are cross-resistant to three clinically relevant antibiotics. These findings suggest that humans may be influencing the microbial species and genes that are found indoors through the addition and removal of particular antimicrobial chemicals. Author Video: An author video summary of this article is available.Ashkaan K. FahimipourSarah Ben MaamarAlexander G. McFarlandRyan A. BlausteinJing ChenAdam J. GlaweJeff KlineJessica L. GreenRolf U. HaldenKevin Van Den WymelenbergCurtis HuttenhowerErica M. HartmannAmerican Society for Microbiologyarticleantibiotic resistancemicrobiometriclosanMicrobiologyQR1-502ENmSystems, Vol 3, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic antibiotic resistance
microbiome
triclosan
Microbiology
QR1-502
spellingShingle antibiotic resistance
microbiome
triclosan
Microbiology
QR1-502
Ashkaan K. Fahimipour
Sarah Ben Maamar
Alexander G. McFarland
Ryan A. Blaustein
Jing Chen
Adam J. Glawe
Jeff Kline
Jessica L. Green
Rolf U. Halden
Kevin Van Den Wymelenberg
Curtis Huttenhower
Erica M. Hartmann
Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors
description ABSTRACT Humans purposefully and inadvertently introduce antimicrobial chemicals into buildings, resulting in widespread compounds, including triclosan, triclocarban, and parabens, in indoor dust. Meanwhile, drug-resistant infections continue to increase, raising concerns that buildings function as reservoirs of, or even select for, resistant microorganisms. Support for these hypotheses is limited largely since data describing relationships between antimicrobials and indoor microbial communities are scant. We combined liquid chromatography-isotope dilution tandem mass spectrometry with metagenomic shotgun sequencing of dust collected from athletic facilities to characterize relationships between indoor antimicrobial chemicals and microbial communities. Elevated levels of triclosan and triclocarban, but not parabens, were associated with distinct indoor microbiomes. Dust of high triclosan content contained increased Gram-positive species with diverse drug resistance capabilities, whose pangenomes were enriched for genes encoding osmotic stress responses, efflux pump regulation, lipid metabolism, and material transport across cell membranes; such triclosan-associated functional shifts have been documented in laboratory cultures but not yet from buildings. Antibiotic-resistant bacterial isolates were cultured from all but one facility, and resistance often increased in buildings with very high triclosan levels, suggesting links between human encounters with viable drug-resistant bacteria and local biocide conditions. This characterization uncovers complex relationships between antimicrobials and indoor microbiomes: some chemicals elicit effects, whereas others may not, and no single functional or resistance factor explained chemical-microbe associations. These results suggest that anthropogenic chemicals impact microbial systems in or around buildings and their occupants, highlighting an emergent need to identify the most important indoor, outdoor, and host-associated sources of antimicrobial chemical-resistome interactions. IMPORTANCE The ubiquitous use of antimicrobial chemicals may have undesired consequences, particularly on microbes in buildings. This study shows that the taxonomy and function of microbes in indoor dust are strongly associated with antimicrobial chemicals—more so than any other feature of the buildings. Moreover, we identified links between antimicrobial chemical concentrations in dust and culturable bacteria that are cross-resistant to three clinically relevant antibiotics. These findings suggest that humans may be influencing the microbial species and genes that are found indoors through the addition and removal of particular antimicrobial chemicals. Author Video: An author video summary of this article is available.
format article
author Ashkaan K. Fahimipour
Sarah Ben Maamar
Alexander G. McFarland
Ryan A. Blaustein
Jing Chen
Adam J. Glawe
Jeff Kline
Jessica L. Green
Rolf U. Halden
Kevin Van Den Wymelenberg
Curtis Huttenhower
Erica M. Hartmann
author_facet Ashkaan K. Fahimipour
Sarah Ben Maamar
Alexander G. McFarland
Ryan A. Blaustein
Jing Chen
Adam J. Glawe
Jeff Kline
Jessica L. Green
Rolf U. Halden
Kevin Van Den Wymelenberg
Curtis Huttenhower
Erica M. Hartmann
author_sort Ashkaan K. Fahimipour
title Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors
title_short Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors
title_full Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors
title_fullStr Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors
title_full_unstemmed Antimicrobial Chemicals Associate with Microbial Function and Antibiotic Resistance Indoors
title_sort antimicrobial chemicals associate with microbial function and antibiotic resistance indoors
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/e37cc68048524abf88b55ec0e851cf40
work_keys_str_mv AT ashkaankfahimipour antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT sarahbenmaamar antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT alexandergmcfarland antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT ryanablaustein antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT jingchen antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT adamjglawe antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT jeffkline antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT jessicalgreen antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT rolfuhalden antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT kevinvandenwymelenberg antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT curtishuttenhower antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
AT ericamhartmann antimicrobialchemicalsassociatewithmicrobialfunctionandantibioticresistanceindoors
_version_ 1718376056008736768