4.5 Article

Insights into conjugative transfer of antibiotic resistance genes affected by soil minerals

Journal

EUROPEAN JOURNAL OF SOIL SCIENCE
Volume 72, Issue 3, Pages 1143-1153

Publisher

WILEY
DOI: 10.1111/ejss.13004

Keywords

antimicrobial resistance; conjugative transfer frequency; membrane permeability; minerals; oxidative stress response; ROS formation

Categories

Funding

  1. Royal Society-Newton Advanced Fellowship [NAF \R1\191017]
  2. National Key Research Program of China [2016YFD0800206]
  3. National Natural Science Foundation of China: General Project [41877029]
  4. National Natural Science Foudation of China: International (Region) Cooperation and Exchange Project [41961130383]
  5. Wuhan Science and Technology Bureau [2019020701011469]
  6. Royal Society
  7. National Natural Science Foundation of China

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This study explores the impact of soil minerals on the conjugative transfer of antibiotic resistance genes, demonstrating that birnessite induces a concentration-dependent increase in conjugative transfer. The mechanisms underlying this phenomenon include the formation of reactive oxygen species, increased membrane permeability, and altered gene expression. These findings provide evidence for the role of birnessite in the dissemination of antibiotic resistance.
Widespread antibiotic resistance genes (ARGs) have caused critical threats to public health on a global scale. Soil, composed mainly of minerals, acts as a source of resistance determinants, playing a considerable role in the development and dissemination of ARGs. The great abundance of ARGs in the soil environment raises concern about the effect of minerals on the spread of ARGs. Herein, the horizontal transfer of a model plasmid pMP2463 containing ARGs fromEscherichia coliS17-1 toPseudomonas putidaKT2440 was monitored following exposure to four common soil minerals, namely, kaolinite, montmorillonite, goethite and birnessite. Birnessite resulted in concentration-dependent increases in conjugative transfer of plasmid pMP2463 by 1.3-4.3 fold, compared with that in the control group. However, no obvious laws were found in the change of conjugative transfer rate at different concentrations of kaolinite and montmorillonite. As for goethite, the conjugative transfer rate increased firstly and then decreased as the concentration increased. The possible mechanisms underlying birnessite-induced conjugative transfer of plasmid were explored; birnessite is capable of initiating intracellular reactive oxygen species (ROS) formation, inducing the oxidative stress response. Additionally, birnessite notably facilitated the mRNA expression of the outer membrane protein genes, which contributed to cellular membrane pore formation and horizontal gene transfer, and altered the mRNA expression of conjugative-related genes that are responsible for conjugative transfer of mobile genetic elements between bacteria. This study triggers questions regarding the potential role of soil minerals in the global dissemination of antimicrobial resistance and provides insights into the interactions between bacteria and minerals in the natural soil environment. Highlights The effect of soil minerals on conjugative transfer of ARGs was explored. Birnessite induced the concentration-dependent increase of conjugative transfer. Mechanisms underlying ROS formation, membrane permeability increase, gene expression alteration were revealed. Our results provide evidence for the effect of birnessite on antibiotic resistance dissemination.

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