Cargando…

Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model

Assembly of a resistome in parallel with the establishment of a microbial community is not well understood. Germfree models can reveal microbiota interactions and shed light on bacterial colonization and resistance development under antibiotic pressure. In this study, we exposed germfree soil (GS),...

Descripción completa

Detalles Bibliográficos
Autores principales: Cao, Yuping, Achmon, Yigal, Yaron, Sima, Siame, Bupe A., Leung, Ka Yin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8562478/
https://www.ncbi.nlm.nih.gov/pubmed/34726494
http://dx.doi.org/10.1128/mSystems.00988-21
_version_ 1784593267684278272
author Cao, Yuping
Achmon, Yigal
Yaron, Sima
Siame, Bupe A.
Leung, Ka Yin
author_facet Cao, Yuping
Achmon, Yigal
Yaron, Sima
Siame, Bupe A.
Leung, Ka Yin
author_sort Cao, Yuping
collection PubMed
description Assembly of a resistome in parallel with the establishment of a microbial community is not well understood. Germfree models can reveal microbiota interactions and shed light on bacterial colonization and resistance development under antibiotic pressure. In this study, we exposed germfree soil (GS), GS with diluted nontreated soil (DS), and nontreated soil (NS) to various concentrations of tetracycline (TET) in a nongermfree environment for 10 weeks, followed by 2 weeks of exposure to water. High-throughput sequencing was used to profile bacterial communities and antibiotic resistance genes (ARGs) in the soils. The initial bacterial loads were found to shape the profiles of bacterial communities and the resistomes. GS and DS treated with TET and the same soils left untreated had similar profiles, whereas NS showed different profiles. Soils with the same initial bacterial loads had their profiles shifted by TET treatment. Multidrug resistance (MDR) genes were the most abundant ARG types in all soils, with multidrug efflux pump genes being the discriminatory ARGs in GS regardless of different TET treatments and in GS, DS, and NS after TET. Furthermore, MDR genes were significantly enriched by TET treatment. In contrast, tetracycline resistance genes were either absent or low in relative abundance. The family Burkholderiaceae was predominant in all soils (except in NS treated with water) and was positively selected for by TET treatment. Most importantly, Burkholderiaceae were the primary carrier of ARGs, including MDR genes. IMPORTANCE This is the first study to examine how resistomes develop and evolve using GS. GS can be used to study the colonization and establishment of bacterial communities under antibiotic selection. Surprisingly, MDR genes were the main ARGs detected in GS, and TET treatments did not positively select for specific tetracycline resistance genes. Additionally, Burkholderiaceae were the key bacterial hosts for MDR genes in the current GS model under the conditions investigated. These results show that the family Burkholderiaceae underpins the development of resistome and serves as a source of ARGs. The ease of establishment of Burkholderiaceae and MDR genes in soils has serious implications for human health, since these bacteria are versatile and ubiquitous in the environment.
format Online
Article
Text
id pubmed-8562478
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-85624782021-11-04 Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model Cao, Yuping Achmon, Yigal Yaron, Sima Siame, Bupe A. Leung, Ka Yin mSystems Research Article Assembly of a resistome in parallel with the establishment of a microbial community is not well understood. Germfree models can reveal microbiota interactions and shed light on bacterial colonization and resistance development under antibiotic pressure. In this study, we exposed germfree soil (GS), GS with diluted nontreated soil (DS), and nontreated soil (NS) to various concentrations of tetracycline (TET) in a nongermfree environment for 10 weeks, followed by 2 weeks of exposure to water. High-throughput sequencing was used to profile bacterial communities and antibiotic resistance genes (ARGs) in the soils. The initial bacterial loads were found to shape the profiles of bacterial communities and the resistomes. GS and DS treated with TET and the same soils left untreated had similar profiles, whereas NS showed different profiles. Soils with the same initial bacterial loads had their profiles shifted by TET treatment. Multidrug resistance (MDR) genes were the most abundant ARG types in all soils, with multidrug efflux pump genes being the discriminatory ARGs in GS regardless of different TET treatments and in GS, DS, and NS after TET. Furthermore, MDR genes were significantly enriched by TET treatment. In contrast, tetracycline resistance genes were either absent or low in relative abundance. The family Burkholderiaceae was predominant in all soils (except in NS treated with water) and was positively selected for by TET treatment. Most importantly, Burkholderiaceae were the primary carrier of ARGs, including MDR genes. IMPORTANCE This is the first study to examine how resistomes develop and evolve using GS. GS can be used to study the colonization and establishment of bacterial communities under antibiotic selection. Surprisingly, MDR genes were the main ARGs detected in GS, and TET treatments did not positively select for specific tetracycline resistance genes. Additionally, Burkholderiaceae were the key bacterial hosts for MDR genes in the current GS model under the conditions investigated. These results show that the family Burkholderiaceae underpins the development of resistome and serves as a source of ARGs. The ease of establishment of Burkholderiaceae and MDR genes in soils has serious implications for human health, since these bacteria are versatile and ubiquitous in the environment. American Society for Microbiology 2021-11-02 /pmc/articles/PMC8562478/ /pubmed/34726494 http://dx.doi.org/10.1128/mSystems.00988-21 Text en Copyright © 2021 Cao et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Cao, Yuping
Achmon, Yigal
Yaron, Sima
Siame, Bupe A.
Leung, Ka Yin
Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model
title Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model
title_full Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model
title_fullStr Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model
title_full_unstemmed Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model
title_short Burkholderiaceae and Multidrug Resistance Genes Are Key Players in Resistome Development in a Germfree Soil Model
title_sort burkholderiaceae and multidrug resistance genes are key players in resistome development in a germfree soil model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8562478/
https://www.ncbi.nlm.nih.gov/pubmed/34726494
http://dx.doi.org/10.1128/mSystems.00988-21
work_keys_str_mv AT caoyuping burkholderiaceaeandmultidrugresistancegenesarekeyplayersinresistomedevelopmentinagermfreesoilmodel
AT achmonyigal burkholderiaceaeandmultidrugresistancegenesarekeyplayersinresistomedevelopmentinagermfreesoilmodel
AT yaronsima burkholderiaceaeandmultidrugresistancegenesarekeyplayersinresistomedevelopmentinagermfreesoilmodel
AT siamebupea burkholderiaceaeandmultidrugresistancegenesarekeyplayersinresistomedevelopmentinagermfreesoilmodel
AT leungkayin burkholderiaceaeandmultidrugresistancegenesarekeyplayersinresistomedevelopmentinagermfreesoilmodel