Broad-spectrum tolerance to disinfectant-mediated bacterial killing due to mutation of the PheS aminoacyl tRNA synthetase

M Miaomiao Chen R Runbo Cui (State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University) S Shouqiang Hong (State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University) W Weiwei Zhu (Division of Plant Science and Technology, University of Missouri) Q Qiong Yang (State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University) J Jiahao Li Z Zihan Nie (State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University) X Xue Zhang Y Yanghui Ye (Minister of Education Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Institute of Molecular Enzymology, School of Biology and Basic Medical Sciences, Soochow University) Y Yunxin Xue (State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University) D Dai Wang (State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University) Y Yuzhi Hong (Minister of Education Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Institute of Molecular Enzymology, School of Biology and Basic Medical Sciences, Soochow University) K Karl Drlica (Public Health Research Institute and Department of Microbiology, Biochemistry & Molecular Genetics, New Jersey Medical School, Rutgers University) J Jianjun Niu (Center of Clinical Laboratory, Zhongshan Hospital, School of Medicine, Xiamen University) X Xilin Zhao (State Key Laboratory and Institute of Elemento-Organic Chemistry, Frontiers Science Center for New Organic Matter, Haihe Laboratory of Sustainable Chemical Transformations, College of Chemistry, Nankai University, 94 Weijin Road, Tianjin 300071, China)

Abstract

Disinfectants are essential tools for controlling infectious diseases and maintaining sterile conditions in many medical and food-industry settings. Recent work revealed that a deficiency in the carbohydrate phosphotransferase system (PTS) confers pan-tolerance to killing by diverse disinfectant types through its interaction with the cAMP-CRP regulatory network. The present work characterized a pan-tolerance mutant obtained by enrichment using phenol as a lethal probe and an Escherichia coli PTS null mutant as a parental strain. The resulting super-pan-tolerant mutant, which harbored an F158C substitution in PheS, inhibited bacterial killing by multiple disinfectant classes with surprisingly little effect on antimicrobial lethality. The PheS substitution, which was expected to lower substrate recognition efficiency and result in deacylated tRNA phe occupying the ribosomal A site, activated relA expression and synthesis of ppGpp, even in the absence of disinfectant exposure. ppGpp, along with DksA, increased RpoS function by activating promoters of dsrA and iraP , two genes whose products increase the expression and stability of RpoS. Subsequently, RpoS upregulated the expression of genes encoding a universal stress protein (UspB) and an oxidative stress peroxidase (KatE), which preconditioned bacteria to better survive a variety of disinfectants. Disinfectant-mediated accumulation of reactive oxygen species (ROS) and bacterial killing were abolished/reduced by exogenous dimethyl sulfoxide and by a PheS F158C substitution up-regulating genes encoding ROS-detoxifying enzymes ( katE, sodA, oxyR, ahpC ). These data identify a pheS mutation-triggered, ppGpp-stimulated transcriptional regulatory cascade that negates biocide-mediated lethality, thereby tying the stringent response to protection from ROS-mediated biocide lethality.

Article Details

Volume / Issue Vol. 122, Issue 6
Published February 11, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (15)

M

Miaomiao Chen

R

Runbo Cui

State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University

S

Shouqiang Hong

State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University

W

Weiwei Zhu

Division of Plant Science and Technology, University of Missouri

Q

Qiong Yang

State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University

J

Jiahao Li

Z

Zihan Nie

State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University

X

Xue Zhang

Y

Yanghui Ye

Minister of Education Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Institute of Molecular Enzymology, School of Biology and Basic Medical Sciences, Soochow University

Y

Yunxin Xue

State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University

D

Dai Wang

State Key Laboratory of Vaccines for Infectious Diseases, Xiang-An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University

Y

Yuzhi Hong

Minister of Education Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Institute of Molecular Enzymology, School of Biology and Basic Medical Sciences, Soochow University

K

Karl Drlica

Public Health Research Institute and Department of Microbiology, Biochemistry & Molecular Genetics, New Jersey Medical School, Rutgers University

J

Jianjun Niu

Center of Clinical Laboratory, Zhongshan Hospital, School of Medicine, Xiamen University

X

Xilin Zhao

State Key Laboratory and Institute of Elemento-Organic Chemistry, Frontiers Science Center for New Organic Matter, Haihe Laboratory of Sustainable Chemical Transformations, College of Chemistry, Nankai University, 94 Weijin Road, Tianjin 300071, China