1887

Abstract

Genomic SELEX screening was performed to identify the binding sites of YiaU, an uncharacterized LysR family transcription factor, on the K-12 genome. Five high-affinity binding targets of YiaU were identified, all of which were involved in the structures of the bacterial cell surface such as outer and inner membrane proteins, and lipopolysaccharides. Detailed and analyses suggest that YiaU activates these target genes. To gain insight into the effects of YiaU on physiological properties, we used phenotype microarrays, biofilm screening assays and the sensitivity against serum complement analysed using a deletion mutant or YiaU expression strain. Together, these results suggest that the YiaU regulon confers resistance to some antibiotics, and increases biofilm formation and complement sensitivity. We propose renaming YiaU as CsuR (regulator of cell surface).

Funding
This study was supported by the:
  • Japan Society for the Promotion of Science (Award 25430173)
    • Principle Award Recipient: AkiraISHIHAMA
  • Japan Society for the Promotion of Science (Award 18310133)
    • Principle Award Recipient: AkiraISHIHAMA
  • Japan Society for the Promotion of Science (Award 19K06618)
    • Principle Award Recipient: TomohiroShimada
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001166
2022-04-19
2024-10-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/168/4/mic001166.html?itemId=/content/journal/micro/10.1099/mic.0.001166&mimeType=html&fmt=ahah

References

  1. Lai Y, Rosenshine I, Leong JM, Frankel G. Intimate host attachment: enteropathogenic and enterohaemorrhagic Escherichia coli. Cell Microbiol 2013; 15:1796–1808 [View Article] [PubMed]
    [Google Scholar]
  2. Nan B, McBride MJ, Chen J, Zusman DR, Oster G. Bacteria that glide with helical tracks. Curr Biol 2014; 24:R169–73 [View Article] [PubMed]
    [Google Scholar]
  3. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 2003; 67:593–656 [View Article] [PubMed]
    [Google Scholar]
  4. Raetz CRH, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem 2002; 71:635–700 [View Article] [PubMed]
    [Google Scholar]
  5. Gan L, Chen S, Jensen GJ. Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci U S A 2008; 105:18953–18957 [View Article] [PubMed]
    [Google Scholar]
  6. Rollauer SE, Sooreshjani MA, Noinaj N, Buchanan SK. Outer membrane protein biogenesis in Gram-negative bacteria. Philos Trans R Soc Lond B Biol Sci 2015; 370:20150023 [View Article] [PubMed]
    [Google Scholar]
  7. Wimley WC. The versatile beta-barrel membrane protein. Curr Opin Struct Biol 2003; 13:404–411 [View Article] [PubMed]
    [Google Scholar]
  8. Miot M, Betton J-M. Protein quality control in the bacterial periplasm. Microb Cell Fact 2004; 3:4 [View Article] [PubMed]
    [Google Scholar]
  9. Daley DO, Rapp M, Granseth E, Melén K, Drew D et al. Global topology analysis of the Escherichia coli inner membrane proteome. Science 2005; 308:1321–1323 [View Article] [PubMed]
    [Google Scholar]
  10. Luirink J, Yu Z, Wagner S, de Gier J-W. Biogenesis of inner membrane proteins in Escherichia coli. Biochim Biophys Acta 2012; 1817:965–976 [View Article] [PubMed]
    [Google Scholar]
  11. Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJW. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci U S A 2005; 102:17693–17698 [View Article] [PubMed]
    [Google Scholar]
  12. Kahramanoglou C, Seshasayee ASN, Prieto AI, Ibberson D, Schmidt S et al. Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res 2011; 39:2073–2091 [View Article] [PubMed]
    [Google Scholar]
  13. Rhee HS, Pugh BF. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 2011; 147:1408–1419 [View Article] [PubMed]
    [Google Scholar]
  14. Ishihama A. Prokaryotic genome regulation: a revolutionary paradigm. Proc Jpn Acad Ser B Phys Biol Sci 2012; 88:485–508 [View Article] [PubMed]
    [Google Scholar]
  15. Ishihama A, Shimada T, Yamazaki Y. Transcription profile of Escherichia coli: genomic SELEX search for regulatory targets of transcription factors. Nucleic Acids Res 2016; 44:2058–2074 [View Article] [PubMed]
    [Google Scholar]
  16. Ishihama A et al. The Nucleoid: an Overview. In Böck A, Curtiss I, Kaper JB, Karp PD, Neidhardt FC. eds EcoSal—Escherichia Coli and Salmonella: Cellular and Molecular Biology Washington, DC: ASM Press; 2009
    [Google Scholar]
  17. Ishihama A, Kori A, Koshio E, Yamada K, Maeda H et al. Intracellular concentrations of 65 species of transcription factors with known regulatory functions in Escherichia coli. J Bacteriol 2014; 196:2718–2727 [View Article] [PubMed]
    [Google Scholar]
  18. Shimada T, Fujita N, Maeda M, Ishihama A. Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells 2005; 10:907–918 [View Article] [PubMed]
    [Google Scholar]
  19. Shimada T, Ogasawara H, Ishihama A. Genomic SELEX screening of regulatory targets of Escherichia coli transcription factors. Methods Mol Biol 2018; 1837:49–69 [View Article] [PubMed]
    [Google Scholar]
  20. Jishage M, Ishihama A. Variation in RNA polymerase sigma subunit composition within different stocks of Escherichia coli W3110. J Bacteriol 1997; 179:959–963 [View Article] [PubMed]
    [Google Scholar]
  21. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000; 97:6640–6645 [View Article] [PubMed]
    [Google Scholar]
  22. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. Construction of Escherichia coli K‐12 in‐frame, single‐gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2: [View Article] [PubMed]
    [Google Scholar]
  23. Shimada T, Ishihama A, Busby SJW, Grainger DC. The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res 2008; 36:3950–3955 [View Article] [PubMed]
    [Google Scholar]
  24. Shimada T, Bridier A, Briandet R, Ishihama A. Novel roles of LeuO in transcription regulation of E. coli genome: antagonistic interplay with the universal silencer H-NS. Mol Microbiol 2011; 82:378–397 [View Article] [PubMed]
    [Google Scholar]
  25. Anzai T, Imamura S, Ishihama A, Shimada T. Expanded roles of pyruvate-sensing PdhR in transcription regulation of the Escherichia coli K-12 genome: fatty acid catabolism and cell motility. Microb Genom 2020; 6:mgen000442 [View Article]
    [Google Scholar]
  26. Shimada T, Saito N, Maeda M, Tanaka K, Ishihama A. Expanded roles of leucine-responsive regulatory protein in transcription regulation of the Escherichia coli genome: Genomic SELEX screening of the regulation targets. Microb Genom 2015; 1:e000001 [View Article] [PubMed]
    [Google Scholar]
  27. Bochner BR. Global phenotypic characterization of bacteria. FEMS Microbiol Rev 2009; 33:191–205 [View Article]
    [Google Scholar]
  28. Ogasawara H, Ishizuka T, Hotta S, Aoki M, Shimada T et al. Novel regulators of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli K-12. Microbiology 2020; 166:880–890 [View Article] [PubMed]
    [Google Scholar]
  29. Liu YF, Yan JJ, Lei HY, Teng CH, Wang MC et al. Loss of outer membrane protein C in Escherichia coli contributes to both antibiotic resistance and escaping antibody-dependent bactericidal activity. Infect Immun 2012; 80:1815–1822 [View Article] [PubMed]
    [Google Scholar]
  30. Shimada T, Furuhata S, Ishihama A. Whole set of constitutive promoters for RpoN sigma factor and the regulatory role of its enhancer protein NtrC in Escherichia coli K-12. Microb Genom 2021; 7:000653 [View Article] [PubMed]
    [Google Scholar]
  31. Heesterbeek DAC, Angelier ML, Harrison RA, Rooijakkers SHM. Complement and bacterial infections: from molecular mechanisms to therapeutic applications. J Innate Immun 2018; 10:455–464 [View Article] [PubMed]
    [Google Scholar]
  32. Miskinyte M, Sousa A, Ramiro RS, de Sousa JAM, Kotlinowski J et al. The genetic basis of Escherichia coli pathoadaptation to macrophages. PLoS Pathog 2013; 9:e1003802 [View Article] [PubMed]
    [Google Scholar]
  33. Proença JT, Barral DC, Gordo I. Commensal-to-pathogen transition: One-single transposon insertion results in two pathoadaptive traits in Escherichia coli -macrophage interaction. Sci Rep 2017; 7:4504 [View Article] [PubMed]
    [Google Scholar]
  34. Biesecker S, Nicastro L, Wilson R, Tükel Ç. The functional amyloid curli protects Escherichia coli against complement-mediated bactericidal activity. Biomolecules 2018; 8:5 [View Article] [PubMed]
    [Google Scholar]
  35. Gao Y, Lim HG, Verkler H, Szubin R, Quach D et al. Unraveling the functions of uncharacterized transcription factors in Escherichia coli using ChIP-exo. Nucleic Acids Res 2021; 49:9696–9710 [View Article] [PubMed]
    [Google Scholar]
  36. Noinaj N, Fairman JW, Buchanan SK. The crystal structure of BamB suggests interactions with BamA and its role within the BAM complex. J Mol Biol 2011; 407:248–260 [View Article] [PubMed]
    [Google Scholar]
  37. Vinson HM, Gautam A, Olet S, Gibbs PS, Barigye R. Molecular analysis of porin gene transcription in heterogenotypic multidrug-resistant Escherichia coli isolates from scouring calves. J Antimicrob Chemother 2010; 65:1926–1935 [View Article] [PubMed]
    [Google Scholar]
  38. Hu Y, Coates ARM. Transposon mutagenesis identifies genes which control antimicrobial drug tolerance in stationary-phase Escherichia coli. FEMS Microbiol Lett 2005; 243:117–124 [View Article] [PubMed]
    [Google Scholar]
  39. Han MJ, Lee SH. An efficient bacterial surface display system based on a novel outer membrane anchoring element from the Escherichia coli protein YiaT. FEMS Microbiol Lett 2015; 362:1–7 [View Article] [PubMed]
    [Google Scholar]
  40. Abbas AK, Lichtman AH, Pillai S. Cellular and Molecular Immunology 2010 pp 272–288
    [Google Scholar]
  41. Rubirés X, Saigi F, Piqué N, Climent N, Merino S et al. A gene (wbbL) from Serratia marcescens N28b (O4) complements the rfb-50 mutation of Escherichia coli K-12 derivatives. J Bacteriol 1997; 179:7581–7586 [View Article] [PubMed]
    [Google Scholar]
  42. Maddocks SE, Oyston PCF. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology (Reading) 2008; 154:3609–3623 [View Article] [PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.001166
Loading
/content/journal/micro/10.1099/mic.0.001166
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error