A Bacterial Pathogen Senses Host Mannose to Coordinate Virulence

Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida, an important fish pathogen...

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Published iniScience Vol. 20; pp. 310 - 323
Main Authors Wei, Lifan, Qiao, Haoxian, Sit, Brandon, Yin, Kaiyu, Yang, Guanhua, Ma, Ruiqing, Ma, Jiabao, Yang, Chun, Yao, Jun, Ma, Yue, Xiao, Jingfan, Liu, Xiaohong, Zhang, Yuanxing, Waldor, Matthew K., Wang, Qiyao
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 25.10.2019
Elsevier
Subjects
Fish Culture
Microbiology
Pathogenic Organism
Microbiology
Pathogenic Organism
Fish Culture
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Abstract Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida, an important fish pathogen, to quantify the fitness of insertion mutants for intracellular growth in macrophages and in turbot (Scophthalmus maximus). These screens identified EvrA, a transcription activator that induces expression of esrB, a key virulence regulator. EvrA is directly bound and activated by mannose-6-phosphate (man-6P) derived from actively imported mannose. Mutants lacking EvrA or expressing an EvrA unable to bind man-6P were similarly attenuated in turbot. Exogenously added mannose promoted E. piscicida virulence, and high levels of mannose were detected in fish tissue. Together, these observations reveal that binding of a host-derived sugar to a transcription factor can facilitate pathogen sensing of the host environment and trigger virulence programs. [Display omitted] •An E. piscicida defined mutant library is generated and analyzed in vitro and in vivo•EvrA is a key transcriptional activator of the known virulence regulator esrB•EvrA is directly bound and activated by mannose-6-phosphate from imported mannose•Extracellular mannose augments E. piscicida virulence in an evrA-dependent manner Pathogenic Organism; Microbiology; Fish Culture
AbstractList Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida, an important fish pathogen, to quantify the fitness of insertion mutants for intracellular growth in macrophages and in turbot (Scophthalmus maximus). These screens identified EvrA, a transcription activator that induces expression of esrB, a key virulence regulator. EvrA is directly bound and activated by mannose-6-phosphate (man-6P) derived from actively imported mannose. Mutants lacking EvrA or expressing an EvrA unable to bind man-6P were similarly attenuated in turbot. Exogenously added mannose promoted E. piscicida virulence, and high levels of mannose were detected in fish tissue. Together, these observations reveal that binding of a host-derived sugar to a transcription factor can facilitate pathogen sensing of the host environment and trigger virulence programs. : Pathogenic Organism; Microbiology; Fish Culture Subject Areas: Pathogenic Organism, Microbiology, Fish Culture
Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida, an important fish pathogen, to quantify the fitness of insertion mutants for intracellular growth in macrophages and in turbot (Scophthalmus maximus). These screens identified EvrA, a transcription activator that induces expression of esrB, a key virulence regulator. EvrA is directly bound and activated by mannose-6-phosphate (man-6P) derived from actively imported mannose. Mutants lacking EvrA or expressing an EvrA unable to bind man-6P were similarly attenuated in turbot. Exogenously added mannose promoted E. piscicida virulence, and high levels of mannose were detected in fish tissue. Together, these observations reveal that binding of a host-derived sugar to a transcription factor can facilitate pathogen sensing of the host environment and trigger virulence programs.Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida, an important fish pathogen, to quantify the fitness of insertion mutants for intracellular growth in macrophages and in turbot (Scophthalmus maximus). These screens identified EvrA, a transcription activator that induces expression of esrB, a key virulence regulator. EvrA is directly bound and activated by mannose-6-phosphate (man-6P) derived from actively imported mannose. Mutants lacking EvrA or expressing an EvrA unable to bind man-6P were similarly attenuated in turbot. Exogenously added mannose promoted E. piscicida virulence, and high levels of mannose were detected in fish tissue. Together, these observations reveal that binding of a host-derived sugar to a transcription factor can facilitate pathogen sensing of the host environment and trigger virulence programs.
Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida, an important fish pathogen, to quantify the fitness of insertion mutants for intracellular growth in macrophages and in turbot (Scophthalmus maximus). These screens identified EvrA, a transcription activator that induces expression of esrB, a key virulence regulator. EvrA is directly bound and activated by mannose-6-phosphate (man-6P) derived from actively imported mannose. Mutants lacking EvrA or expressing an EvrA unable to bind man-6P were similarly attenuated in turbot. Exogenously added mannose promoted E. piscicida virulence, and high levels of mannose were detected in fish tissue. Together, these observations reveal that binding of a host-derived sugar to a transcription factor can facilitate pathogen sensing of the host environment and trigger virulence programs.
Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida , an important fish pathogen, to quantify the fitness of insertion mutants for intracellular growth in macrophages and in turbot ( Scophthalmus maximus ). These screens identified EvrA, a transcription activator that induces expression of esrB , a key virulence regulator. EvrA is directly bound and activated by mannose-6-phosphate (man-6P) derived from actively imported mannose. Mutants lacking EvrA or expressing an EvrA unable to bind man-6P were similarly attenuated in turbot. Exogenously added mannose promoted E. piscicida virulence, and high levels of mannose were detected in fish tissue. Together, these observations reveal that binding of a host-derived sugar to a transcription factor can facilitate pathogen sensing of the host environment and trigger virulence programs. • An E. piscicida defined mutant library is generated and analyzed in vitro and in vivo • EvrA is a key transcriptional activator of the known virulence regulator esrB • EvrA is directly bound and activated by mannose-6-phosphate from imported mannose • Extracellular mannose augments E. piscicida virulence in an evrA -dependent manner Pathogenic Organism; Microbiology; Fish Culture
Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such signals has proved difficult. We generated a genome-scale defined transposon mutant library in Edwardsiella piscicida, an important fish pathogen, to quantify the fitness of insertion mutants for intracellular growth in macrophages and in turbot (Scophthalmus maximus). These screens identified EvrA, a transcription activator that induces expression of esrB, a key virulence regulator. EvrA is directly bound and activated by mannose-6-phosphate (man-6P) derived from actively imported mannose. Mutants lacking EvrA or expressing an EvrA unable to bind man-6P were similarly attenuated in turbot. Exogenously added mannose promoted E. piscicida virulence, and high levels of mannose were detected in fish tissue. Together, these observations reveal that binding of a host-derived sugar to a transcription factor can facilitate pathogen sensing of the host environment and trigger virulence programs. [Display omitted] •An E. piscicida defined mutant library is generated and analyzed in vitro and in vivo•EvrA is a key transcriptional activator of the known virulence regulator esrB•EvrA is directly bound and activated by mannose-6-phosphate from imported mannose•Extracellular mannose augments E. piscicida virulence in an evrA-dependent manner Pathogenic Organism; Microbiology; Fish Culture
Author Ma, Yue
Yang, Chun
Yao, Jun
Zhang, Yuanxing
Yang, Guanhua
Waldor, Matthew K.
Ma, Ruiqing
Ma, Jiabao
Yin, Kaiyu
Qiao, Haoxian
Xiao, Jingfan
Sit, Brandon
Liu, Xiaohong
Wei, Lifan
Wang, Qiyao
AuthorAffiliation 6 State Key Laboratory of Genetic Engineering, Department of Physiology and Biophysics, School of Life Sciences, Fudan University, Shanghai, 200433, China
7 Institutes of Biomedical Sciences, Fudan University, Shanghai, 200433, China
2 Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
3 Shanghai Engineering Research Center of Maricultured Animal Vaccines, Shanghai 200237, China
4 Division of Infectious Diseases, Brigham and Women's Hospital and Harvard Medical School, Boston, MA 02115, USA
1 State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China
5 Howard Hughes Medical Institute, Boston, MA 02115, USA
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Keywords Microbiology
Pathogenic Organism
Fish Culture
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– reference: 38784014 - iScience. 2024 May 20;27(6):110004
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Snippet Bacterial pathogens are thought to activate expression of virulence genes upon detection of host-associated cues, but identification of the nature of such...
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SubjectTerms Fish Culture
Microbiology
Pathogenic Organism
Title A Bacterial Pathogen Senses Host Mannose to Coordinate Virulence
URI https://dx.doi.org/10.1016/j.isci.2019.09.028
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