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Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease

Rationale: Long-term antibiotic use for managing chronic respiratory disease is increasing; however, the role of the airway resistome and its relationship to host microbiomes remains unknown. Objectives: To evaluate airway resistomes and relate them to host and environmental microbiomes using ultrad...

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Autores principales: Mac Aogáin, Micheál, Lau, Kenny J. X., Cai, Zhao, Kumar Narayana, Jayanth, Purbojati, Rikky W., Drautz-Moses, Daniela I., Gaultier, Nicolas E., Jaggi, Tavleen K., Tiew, Pei Yee, Ong, Thun How, Siyue Koh, Mariko, Lim Yick Hou, Albert, Abisheganaden, John A., Tsaneva-Atanasova, Krasimira, Schuster, Stephan C., Chotirmall, Sanjay H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Thoracic Society 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397787/
https://www.ncbi.nlm.nih.gov/pubmed/32320621
http://dx.doi.org/10.1164/rccm.201911-2202OC
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author Mac Aogáin, Micheál
Lau, Kenny J. X.
Cai, Zhao
Kumar Narayana, Jayanth
Purbojati, Rikky W.
Drautz-Moses, Daniela I.
Gaultier, Nicolas E.
Jaggi, Tavleen K.
Tiew, Pei Yee
Ong, Thun How
Siyue Koh, Mariko
Lim Yick Hou, Albert
Abisheganaden, John A.
Tsaneva-Atanasova, Krasimira
Schuster, Stephan C.
Chotirmall, Sanjay H.
author_facet Mac Aogáin, Micheál
Lau, Kenny J. X.
Cai, Zhao
Kumar Narayana, Jayanth
Purbojati, Rikky W.
Drautz-Moses, Daniela I.
Gaultier, Nicolas E.
Jaggi, Tavleen K.
Tiew, Pei Yee
Ong, Thun How
Siyue Koh, Mariko
Lim Yick Hou, Albert
Abisheganaden, John A.
Tsaneva-Atanasova, Krasimira
Schuster, Stephan C.
Chotirmall, Sanjay H.
author_sort Mac Aogáin, Micheál
collection PubMed
description Rationale: Long-term antibiotic use for managing chronic respiratory disease is increasing; however, the role of the airway resistome and its relationship to host microbiomes remains unknown. Objectives: To evaluate airway resistomes and relate them to host and environmental microbiomes using ultradeep metagenomic shotgun sequencing. Methods: Airway specimens from 85 individuals with and without chronic respiratory disease (severe asthma, chronic obstructive pulmonary disease, and bronchiectasis) were subjected to metagenomic sequencing to an average depth exceeding 20 million reads. Respiratory and device-associated microbiomes were evaluated on the basis of taxonomical classification and functional annotation including the Comprehensive Antibiotic Resistance Database to determine airway resistomes. Co-occurrence networks of gene–microbe association were constructed to determine potential microbial sources of the airway resistome. Paired patient-inhaler metagenomes were compared (n = 31) to assess for the presence of airway–environment overlap in microbiomes and/or resistomes. Measurements and Main Results: Airway metagenomes exhibit taxonomic and metabolic diversity and distinct antimicrobial resistance patterns. A “core” airway resistome dominated by macrolide but with high prevalence of β-lactam, fluoroquinolone, and tetracycline resistance genes exists and is independent of disease status or antibiotic exposure. Streptococcus and Actinomyces are key potential microbial reservoirs of macrolide resistance including the ermX, ermF, and msrD genes. Significant patient-inhaler overlap in airway microbiomes and their resistomes is identified where the latter may be a proxy for airway microbiome assessment in chronic respiratory disease. Conclusions: Metagenomic analysis of the airway reveals a core macrolide resistome harbored by the host microbiome.
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spelling pubmed-73977872020-08-03 Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease Mac Aogáin, Micheál Lau, Kenny J. X. Cai, Zhao Kumar Narayana, Jayanth Purbojati, Rikky W. Drautz-Moses, Daniela I. Gaultier, Nicolas E. Jaggi, Tavleen K. Tiew, Pei Yee Ong, Thun How Siyue Koh, Mariko Lim Yick Hou, Albert Abisheganaden, John A. Tsaneva-Atanasova, Krasimira Schuster, Stephan C. Chotirmall, Sanjay H. Am J Respir Crit Care Med Original Articles Rationale: Long-term antibiotic use for managing chronic respiratory disease is increasing; however, the role of the airway resistome and its relationship to host microbiomes remains unknown. Objectives: To evaluate airway resistomes and relate them to host and environmental microbiomes using ultradeep metagenomic shotgun sequencing. Methods: Airway specimens from 85 individuals with and without chronic respiratory disease (severe asthma, chronic obstructive pulmonary disease, and bronchiectasis) were subjected to metagenomic sequencing to an average depth exceeding 20 million reads. Respiratory and device-associated microbiomes were evaluated on the basis of taxonomical classification and functional annotation including the Comprehensive Antibiotic Resistance Database to determine airway resistomes. Co-occurrence networks of gene–microbe association were constructed to determine potential microbial sources of the airway resistome. Paired patient-inhaler metagenomes were compared (n = 31) to assess for the presence of airway–environment overlap in microbiomes and/or resistomes. Measurements and Main Results: Airway metagenomes exhibit taxonomic and metabolic diversity and distinct antimicrobial resistance patterns. A “core” airway resistome dominated by macrolide but with high prevalence of β-lactam, fluoroquinolone, and tetracycline resistance genes exists and is independent of disease status or antibiotic exposure. Streptococcus and Actinomyces are key potential microbial reservoirs of macrolide resistance including the ermX, ermF, and msrD genes. Significant patient-inhaler overlap in airway microbiomes and their resistomes is identified where the latter may be a proxy for airway microbiome assessment in chronic respiratory disease. Conclusions: Metagenomic analysis of the airway reveals a core macrolide resistome harbored by the host microbiome. American Thoracic Society 2020-08-01 2020-08-01 /pmc/articles/PMC7397787/ /pubmed/32320621 http://dx.doi.org/10.1164/rccm.201911-2202OC Text en Copyright © 2020 by the American Thoracic Society http://creativecommons.org/licenses/by-nc-nd/4.0/ This article is open access and distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives License 4.0 (http://creativecommons.org/licenses/by-nc-nd/4.0/). For commercial usage and reprints, please contact Diane Gern (dgern@thoracic.org).
spellingShingle Original Articles
Mac Aogáin, Micheál
Lau, Kenny J. X.
Cai, Zhao
Kumar Narayana, Jayanth
Purbojati, Rikky W.
Drautz-Moses, Daniela I.
Gaultier, Nicolas E.
Jaggi, Tavleen K.
Tiew, Pei Yee
Ong, Thun How
Siyue Koh, Mariko
Lim Yick Hou, Albert
Abisheganaden, John A.
Tsaneva-Atanasova, Krasimira
Schuster, Stephan C.
Chotirmall, Sanjay H.
Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease
title Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease
title_full Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease
title_fullStr Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease
title_full_unstemmed Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease
title_short Metagenomics Reveals a Core Macrolide Resistome Related to Microbiota in Chronic Respiratory Disease
title_sort metagenomics reveals a core macrolide resistome related to microbiota in chronic respiratory disease
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397787/
https://www.ncbi.nlm.nih.gov/pubmed/32320621
http://dx.doi.org/10.1164/rccm.201911-2202OC
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