Burkholderiaceae and multidrug resistance genes are key players in resistome development in a germfree soil model

Yuping Cao, Yigal Achmon, Sima Yaron*, Bupe A. Siame, Ka Yin Leung*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish
Article numbere00988-21
JournalmSystems
Volume6
Issue number6
Early online date1 Dec 2021
DOIs
StatePublished - Dec 2021

Keywords

  • Germfree soil
  • Metagenomics
  • Microbiome
  • Multidrug resistance genes
  • Resistome

Fingerprint

Dive into the research topics of 'Burkholderiaceae and multidrug resistance genes are key players in resistome development in a germfree soil model'. Together they form a unique fingerprint.

Cite this