1887

Abstract

The binding sites of YihW, an uncharacterized DeoR-family transcription factor (TF) of Escherichia coli K-12, were identified using Genomic SELEX screening at two closely located sites, one inside the spacer between the bidirectional transcription units comprising the yihUTS operon and the yihV gene, and another one upstream of the yihW gene itself. Recently the YihUTS and YihV proteins were identified as catalysing the catabolism of sulfoquinovose (SQ), a hydrolysis product of sulfoquinovosyl diacylglycerol (SQDG) derived from plants and other photosynthetic organisms. Gel shift assay in vitro and reporter assay in vivo indicated that YihW functions as a repressor for all three transcription units. De-repression of the yih operons was found to be under the control of SQ as inducer, but not of lactose, glucose or galactose. Furthermore, a mode of its cooperative DNA binding was suggested for YihW by atomic force microscopy. Hence, as a regulator of the catabolism of SQ, we renamed YihW as CsqR.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000740
2018-10-29
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/165/1/78.html?itemId=/content/journal/micro/10.1099/mic.0.000740&mimeType=html&fmt=ahah

References

  1. Benning C. Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 1998; 49:53–75 [View Article][PubMed]
    [Google Scholar]
  2. Sato N. Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 2004; 117:495–505 [View Article][PubMed]
    [Google Scholar]
  3. Goddard-Borger ED, Williams SJ. Sulfoquinovose in the biosphere: occurrence, metabolism and functions. Biochem J 2017; 474:827–849 [View Article][PubMed]
    [Google Scholar]
  4. Harwood JL, Nicholls RG. The plant sulpholipid- a major component of the sulphur cycle. Biochem Soc Trans 1979; 7:440–447 [View Article][PubMed]
    [Google Scholar]
  5. Sacoman JL, Badish LN, Sharkey TD, Hollingsworth RI. The metabolic and biochemical impact of glucose 6-sulfonate (sulfoquinovose), a dietary sugar, on carbohydrate metabolism. Carbohydr Res 2012; 362:21–29 [View Article][PubMed]
    [Google Scholar]
  6. Roy AB, Ellis AJ, White GF, Harwood JL. Microbial degradation of the plant sulpholipid. Biochem Soc Trans 2000; 28:781–783 [View Article][PubMed]
    [Google Scholar]
  7. Speciale G, Jin Y, Davies GJ, Williams SJ, Goddard-Borger ED. YihQ is a sulfoquinovosidase that cleaves sulfoquinovosyl diacylglyceride sulfolipids. Nat Chem Biol 2016; 12:215–217 [View Article][PubMed]
    [Google Scholar]
  8. Denger K, Weiss M, Felux AK, Schneider A, Mayer C et al. Sulphoglycolysis in Escherichia coli K-12 closes a gap in the biogeochemical sulphur cycle. Nature 2014; 507:114–117 [View Article][PubMed]
    [Google Scholar]
  9. Poolman B, Knol J, van der Does C, Henderson PJ, Liang WJ et al. Cation and sugar selectivity determinants in a novel family of transport proteins. Mol Microbiol 1996; 19:911–922 [View Article][PubMed]
    [Google Scholar]
  10. Saier MH, Reddy VS, Tamang DG, Västermark A. The transporter classification database. Nucleic Acids Res 2014; 42:D251–D258 [View Article][PubMed]
    [Google Scholar]
  11. Denger K, Huhn T, Hollemeyer K, Schleheck D, Cook AM. Sulfoquinovose degraded by pure cultures of bacteria with release of C3-organosulfonates: complete degradation in two-member communities. FEMS Microbiol Lett 2012; 328:39–45 [View Article][PubMed]
    [Google Scholar]
  12. Kaznadzey A, Shelyakin P, Belousova E, Eremina A, Shvyreva U et al. The genes of the sulphoquinovose catabolism in Escherichia coli are also associated with a previously unknown pathway of lactose degradation. Sci Rep 2018; 8:3177 [View Article][PubMed]
    [Google Scholar]
  13. Abayakoon P, Lingford JP, Jin Y, Bengt C, Davies GJ et al. Discovery and characterization of a sulfoquinovose mutarotase using kinetic analysis at equilibrium by exchange spectroscopy. Biochem J 2018; 475:1371–1383 [View Article][PubMed]
    [Google Scholar]
  14. Dartigalongue C, Nikaido H, Raina S. Protein folding in the periplasm in the absence of primary oxidant DsbA: modulation of redox potential in periplasmic space via OmpL porin. Embo J 2000; 19:5980–5988 [View Article][PubMed]
    [Google Scholar]
  15. Pérez-Rueda E, Collado-Vides J. The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Res 2000; 28:1838–1847 [View Article][PubMed]
    [Google Scholar]
  16. Elgrably-Weiss M, Schlosser-Silverman E, Rosenshine I, Altuvia S. DeoT, a DeoR-type transcriptional regulator of multiple target genes. FEMS Microbiol Lett 2006; 254:141–148 [View Article][PubMed]
    [Google Scholar]
  17. Ge B, Liu Y, Liu B, Zhao W, Zhang K. Characterization of novel DeoR-family member from the Streptomyces ahygroscopicus strain CK-15 that acts as a repressor of morphological development. Appl Microbiol Biotechnol 2016; 100:8819–8828 [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 USA 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; 2:2006.0008 [View Article][PubMed]
    [Google Scholar]
  23. Burton NA, Johnson MD, Antczak P, Robinson A, Lund PA. Novel aspects of the acid response network of E. coli K-12 are revealed by a study of transcriptional dynamics. J Mol Biol 2010; 401:726–742 [View Article][PubMed]
    [Google Scholar]
  24. Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R et al. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 2005; 280:1448–1456 [View Article][PubMed]
    [Google Scholar]
  25. Shimada T, Fujita N, Yamamoto K, Ishihama A. Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS One 2011; 6:e20081 [View Article][PubMed]
    [Google Scholar]
  26. Teramoto J, Yoshimura SH, Takeyasu K, Ishihama A. A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions. Nucleic Acids Res 2010; 38:3605–3618 [View Article][PubMed]
    [Google Scholar]
  27. Ogasawara H, Ishida Y, Yamada K, Yamamoto K, Ishihama A. PdhR (pyruvate dehydrogenase complex regulator) controls the respiratory electron transport system in Escherichia coli. J Bacteriol 2007; 189:5534–5541 [View Article][PubMed]
    [Google Scholar]
  28. 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]
  29. Blouin K, Walker SG, Smit J, Turner R. Characterization of In Vivo Reporter Systems for Gene Expression and Biosensor Applications Based on luxAB Luciferase Genes. Appl Environ Microbiol 1996; 62:2013–2021[PubMed]
    [Google Scholar]
  30. Yamanaka Y, Oshima T, Ishihama A, Yamamoto K. Characterization of the YdeO regulon in Escherichia coli. PLoS One 2014; 9:e111962 [View Article][PubMed]
    [Google Scholar]
  31. Uchihashi T, Kodera N, Ando T. Guide to video recording of structure dynamics and dynamic processes of proteins by high-speed atomic force microscopy. Nat Protoc 2012; 7:1193–1206 [View Article][PubMed]
    [Google Scholar]
  32. Shimada T, Ogasawara H, Ishihama A. Single-target regulators form a minor group of transcription factors in Escherichia coli K-12. Nucleic Acids Res 2018; 46:3921–3936 [View Article][PubMed]
    [Google Scholar]
  33. 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]
  34. Lim CJ, Lee SY, Teramoto J, Ishihama A, Yan J. The nucleoid-associated protein Dan organizes chromosomal DNA through rigid nucleoprotein filament formation in E. coli during anoxia. Nucleic Acids Res 2013; 41:746–753 [View Article][PubMed]
    [Google Scholar]
  35. Shimada T, Katayama Y, Kawakita S, Ogasawara H, Nakano M et al. A novel regulator RcdA of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli. Microbiologyopen 2012; 1:381–394 [View Article][PubMed]
    [Google Scholar]
  36. Sugino H, Usui T, Shimada T, Nakano M, Ogasawara H et al. A structural sketch of RcdA, a transcription factor controlling the master regulator of biofilm formation. FEBS Lett 2017; 591:2019–2031 [View Article][PubMed]
    [Google Scholar]
  37. Felux AK, Spiteller D, Klebensberger J, Schleheck D. Entner-Doudoroff pathway for sulfoquinovose degradation in Pseudomonas putida SQ1. Proc Natl Acad Sci USA 2015; 112:E4298E4305 [View Article][PubMed]
    [Google Scholar]
  38. Shimada T, Momiyama E, Yamanaka Y, Watanabe H, Yamamoto K et al. Regulatory role of XynR (YagI) in catabolism of xylonate in Escherichia coli K-12. FEMS Microbiol Lett 2017; 364: [View Article][PubMed]
    [Google Scholar]
  39. 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]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000740
Loading
/content/journal/micro/10.1099/mic.0.000740
Loading

Data & Media loading...

Supplements

Supplementary File 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