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The Evolution of SlyA/RovA Transcription Factors from Repressors to Countersilencers in Enterobacteriaceae.

Will WR, Brzovic P, Le Trong I, Stenkamp RE, Lawrenz MB, Karlinsey JE, Navarre WW, Main-Hester K, Miller VL, Libby SJ, Fang FC
mBio 10 (2019)
Cited: 21 times
EuropePMC logo PMID: 30837332

Abstract

Gene duplication and subsequent evolutionary divergence have allowed conserved proteins to develop unique roles. The MarR family of transcription factors (TFs) has undergone extensive duplication and diversification in bacteria, where they act as environmentally responsive repressors of genes encoding efflux pumps that confer resistance to xenobiotics, including many antimicrobial agents. We have performed structural, functional, and genetic analyses of representative members of the SlyA/RovA lineage of MarR TFs, which retain some ancestral functions, including repression of their own expression and that of divergently transcribed multidrug efflux pumps, as well as allosteric inhibition by aromatic carboxylate compounds. However, SlyA and RovA have acquired the ability to countersilence horizontally acquired genes, which has greatly facilitated the evolution of Enterobacteriaceae by horizontal gene transfer. SlyA/RovA TFs in different species have independently evolved novel regulatory circuits to provide the enhanced levels of expression required for their new role. Moreover, in contrast to MarR, SlyA is not responsive to copper. These observations demonstrate the ability of TFs to acquire new functions as a result of evolutionary divergence of both cis-regulatory sequences and in trans interactions with modulatory ligands.

Articles - 3deu mentioned but not cited (6)

  1. Crystal structures of SlyA protein, a master virulence regulator of Salmonella, in free and DNA-bound states. Dolan KT, Duguid EM, He C. J Biol Chem 286 22178-22185 (2011)
  2. Crystal structure of the zinc-dependent MarR family transcriptional regulator AdcR in the Zn(II)-bound state. Guerra AJ, Dann CE, Giedroc DP. J Am Chem Soc 133 19614-19617 (2011)
  3. Study of PcaV from Streptomyces coelicolor yields new insights into ligand-responsive MarR family transcription factors. Davis JR, Brown BL, Page R, Sello JK. Nucleic Acids Res 41 3888-3900 (2013)
  4. The Evolution of SlyA/RovA Transcription Factors from Repressors to Countersilencers in Enterobacteriaceae. Will WR, Brzovic P, Le Trong I, Stenkamp RE, Lawrenz MB, Karlinsey JE, Navarre WW, Main-Hester K, Miller VL, Libby SJ, Fang FC. mBio 10 e00009-19 (2019)
  5. How Aromatic Compounds Block DNA Binding of HcaR Catabolite Regulator. Kim Y, Joachimiak G, Bigelow L, Babnigg G, Joachimiak A. J Biol Chem 291 13243-13256 (2016)
  6. Letter Amino acid residues involved in inactivation of the Escherichia coli multidrug resistance repressor MarR by salicylate, 2,4-dinitrophenol, and plumbagin. McMurry LM, Levy SB. FEMS Microbiol Lett 349 16-24 (2013)


Reviews citing this publication (2)

  1. How the PhoP/PhoQ System Controls Virulence and Mg2+ Homeostasis: Lessons in Signal Transduction, Pathogenesis, Physiology, and Evolution. Groisman EA, Duprey A, Choi J. Microbiol Mol Biol Rev 85 e0017620 (2021)
  2. The evolution of MarR family transcription factors as counter-silencers in regulatory networks. Will WR, Fang FC. Curr Opin Microbiol 55 1-8 (2020)

Articles citing this publication (13)

  1. Salmonella expresses foreign genes during infection by degrading their silencer. Choi J, Groisman EA. Proc Natl Acad Sci U S A 117 8074-8082 (2020)
  2. Sulfane Sulfur Is a Strong Inducer of the Multiple Antibiotic Resistance Regulator MarR in Escherichia coli. Xu H, Xuan G, Liu H, Xia Y, Xun L. Antioxidants (Basel) 10 1778 (2021)
  3. The MarR-Type Regulator MalR Is Involved in Stress-Responsive Cell Envelope Remodeling in Corynebacterium glutamicum. Hünnefeld M, Persicke M, Kalinowski J, Frunzke J. Front Microbiol 10 1039 (2019)
  4. The MarR-Type Regulator PA3458 Is Involved in Osmoadaptation Control in Pseudomonas aeruginosa. Kotecka K, Kawalek A, Kobylecki K, Bartosik AA. Int J Mol Sci 22 3982 (2021)
  5. The Plant Defense Signal Salicylic Acid Activates the RpfB-Dependent Quorum Sensing Signal Turnover via Altering the Culture and Cytoplasmic pH in the Phytopathogen Xanthomonas campestris. Song K, Chen B, Cui Y, Zhou L, Chan KG, Zhang HY, He YW. mBio 13 e0364421 (2022)
  6. SlyA Transcriptional Regulator Is Not Directly Affected by ppGpp Levels. Bartoli J, Viala JP, Bouveret E. Front Microbiol 11 1856 (2020)
  7. A stress-induced block in dicarboxylate uptake and utilization in Salmonella. Hersch SJ, Radan B, Ilyas B, Lavoie P, Navarre WW. J Bacteriol 203 JB.00487-20 (2021)
  8. Mapping direct and indirect MarA/SoxS/Rob/RamA regulons in Salmonella Typhimurium reveals repression of csgD and biofilm formation. Middlemiss AD, Haycocks JRJ, Stringer AM, Piddock LJV, Wade JT, Grainger DC. Microbiology (Reading) 169 (2023)
  9. The Small RNA MicC Downregulates hilD Translation To Control the Salmonella Pathogenicity Island 1 Type III Secretion System in Salmonella enterica Serovar Typhimurium. Cakar F, Golubeva YA, Vanderpool CK, Slauch JM. J Bacteriol 204 e0037821 (2022)
  10. A Genome-Scale Antibiotic Screen in Serratia marcescens Identifies YdgH as a Conserved Modifier of Cephalosporin and Detergent Susceptibility. Lazarus JE, Warr AR, Westervelt KA, Hooper DC, Waldor MK. Antimicrob Agents Chemother 65 e0078621 (2021)
  11. Biophysical and Biochemical Characterization of the Binding of the MarR-like Transcriptional Regulator Saro_0803 to the nov1 Promotor and Its Inhibition by Resveratrol. He Z, Ke Z, Wang W, Liu Y, Zhang H, Li Y. Biomolecules 13 541 (2023)
  12. Molecular characterization of antimicrobial resistance related genes in E. coli, Salmonella and Klebsiella isolates from broilers in the West Region of Cameroon. Leinyuy JF, Ali IM, Ousenu K, Tume CB. PLoS One 18 e0280150 (2023)
  13. Transcriptome RNA Sequencing Data Set of Differential Gene Expression in Escherichia coli BW25113 Wild-Type and slyA Mutant Strains. Ojo O, Scott D, Iwalokun B, Odetoyin B, Grove A. Microbiol Resour Announc 10 e00294-21 (2021)


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