1887

Abstract

The ability of bacteria to deal with diverse environmental changes depends on their repertoire of genes and their ability to regulate their expression. In this process, DNA-binding transcription factors (TFs) have a fundamental role because they affect gene expression positively and/or negatively depending on operator context and ligand-binding status. Here, we show an exhaustive analysis of winged helix–turn–helix domains (wHTHs), a class of DNA-binding TFs. These proteins were identified in high proportions and widely distributed in bacteria, representing around half of the total TFs identified so far. In addition, we evaluated the repertoire of wHTHs in terms of their partner domains (PaDos), identifying a similar trend, as with TFs, i.e. they are abundant and widely distributed in bacteria. Based on the PaDos, we defined three main groups of families: (i) monolithic, those families with little PaDo diversity, such as LysR; (ii) promiscuous, those families with a high PaDo diversity; and (iii) monodomain, with families of small sizes, such as MarR. These findings suggest that PaDos have a very important role in the diversification of regulatory responses in bacteria, probably contributing to their regulatory complexity. Thus, the TFs discriminate over longer regions on the DNA through their diverse DNA-binding domains. On the other hand, the PaDos would allow a great flexibility for transcriptional regulation due to their ability to sense diverse stimuli through a variety of ligand-binding compounds.

Funding
This study was supported by the:
  • Mexican Science and Technology Research Council (CONACYT) (Award 176841)
  • DGAPA-UNAM (Award IN-209511 and IN-217508)
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.050617-0
2011-08-01
2021-07-31
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/8/2308.html?itemId=/content/journal/micro/10.1099/mic.0.050617-0&mimeType=html&fmt=ahah

References

  1. Aravind L., Koonin E. V. ( 1999). DNA-binding proteins and evolution of transcription regulation in the archaea. Nucleic Acids Res 27:4658–4670 [View Article][PubMed]
    [Google Scholar]
  2. Aravind L., Anantharaman V., Balaji S., Babu M. M., Iyer L. M. ( 2005). The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 29:231–262[PubMed]
    [Google Scholar]
  3. Baumbach J. ( 2007). CoryneRegNet 4.0 – a reference database for corynebacterial gene regulatory networks. BMC Bioinformatics 8:429 [View Article][PubMed]
    [Google Scholar]
  4. Bengtsson B. O. ( 2004). Modelling the evolution of genomes with integrated external and internal functions. J Theor Biol 231:271–278 [View Article][PubMed]
    [Google Scholar]
  5. Brennan R. G. ( 1993). The winged-helix DNA-binding motif: another helix–turn–helix takeoff. Cell 74:773–776 [View Article][PubMed]
    [Google Scholar]
  6. Brennan R. G., Matthews B. W. ( 1989a). The helix–turn–helix DNA binding motif. J Biol Chem 264:1903–1906[PubMed]
    [Google Scholar]
  7. Brennan R. G., Matthews B. W. ( 1989b). Structural basis of DNA-protein recognition. Trends Biochem Sci 14:286–290 [View Article][PubMed]
    [Google Scholar]
  8. Brown J. H., Gupta V. K., Li B. L., Milne B. T., Restrepo C., West G. B. ( 2002). The fractal nature of nature: power laws, ecological complexity and biodiversity. Philos Trans R Soc Lond B Biol Sci 357:619–626 [View Article][PubMed]
    [Google Scholar]
  9. Browning D. F., Busby S. J. ( 2004). The regulation of bacterial transcription initiation. Nat Rev Microbiol 2:57–65 [View Article][PubMed]
    [Google Scholar]
  10. Busenlehner L. S., Pennella M. A., Giedroc D. P. ( 2003). The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol Rev 27:131–143 [View Article][PubMed]
    [Google Scholar]
  11. Changizi M. A. ( 2001). Universal scaling laws for hierarchical complexity in languages, organisms, behaviors and other combinatorial systems. J Theor Biol 211:277–295 [View Article][PubMed]
    [Google Scholar]
  12. Coulson R. M., Enright A. J., Ouzounis C. A. ( 2001). Transcription-associated protein families are primarily taxon-specific. Bioinformatics 17:95–97 [View Article][PubMed]
    [Google Scholar]
  13. Croft L. J., Lercher M. J., Gagen M. J., Mattick J. S. ( 2003). Is prokaryotic complexity limited by accelerated growth in regulatory overhead. Genome Biol 5:P2 [View Article]
    [Google Scholar]
  14. Eisen M. B., Spellman P. T., Brown P. O., Botstein D. ( 1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868 [View Article][PubMed]
    [Google Scholar]
  15. Ellison D. W., Miller V. L. ( 2006). Regulation of virulence by members of the MarR/SlyA family. Curr Opin Microbiol 9:153–159 [View Article][PubMed]
    [Google Scholar]
  16. Even S., Burguière P., Auger S., Soutourina O., Danchin A., Martin-Verstraete I. ( 2006). Global control of cysteine metabolism by CymR in Bacillus subtilis . J Bacteriol 188:2184–2197 [View Article][PubMed]
    [Google Scholar]
  17. Finn R. D., Tate J., Mistry J., Coggill P. C., Sammut S. J., Hotz H. R., Ceric G., Forslund K., Eddy S. R. et al. ( 2008). The Pfam protein families database. Nucleic Acids Res 36:Database issueD281–D288 [View Article][PubMed]
    [Google Scholar]
  18. Fischer B., Rummel G., Aldridge P., Jenal U. ( 2002). The FtsH protease is involved in development, stress response and heat shock control in Caulobacter crescentus . Mol Microbiol 44:461–478 [View Article][PubMed]
    [Google Scholar]
  19. Gama-Castro S., Jiménez-Jacinto V., Peralta-Gil M., Santos-Zavaleta A., Peñaloza-Spinola M. I., Contreras-Moreira B., Segura-Salazar J., Muñiz-Rascado L., Martínez-Flores I. et al. ( 2008). RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. Nucleic Acids Res 36:Database issueD120–D124 [View Article][PubMed]
    [Google Scholar]
  20. Gollnick P., Babitzke P., Antson A., Yanofsky C. ( 2005). Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis . Annu Rev Genet 39:47–68 [View Article][PubMed]
    [Google Scholar]
  21. Gruber T. M., Gross C. A. ( 2003). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466 [View Article][PubMed]
    [Google Scholar]
  22. Hernández-Montes G., Díaz-Mejía J. J., Pérez-Rueda E., Segovia L. ( 2008). The hidden universal distribution of amino acid biosynthetic networks: a genomic perspective on their origins and evolution. Genome Biol 9:R95 [View Article][PubMed]
    [Google Scholar]
  23. Ishihama A. ( 2000). Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54:499–518 [View Article][PubMed]
    [Google Scholar]
  24. Janga S. C., Moreno-Hagelsieb G. ( 2004). Conservation of adjacency as evidence of paralogous operons. Nucleic Acids Res 32:5392–5397 [View Article][PubMed]
    [Google Scholar]
  25. Janga S. C., Pérez-Rueda E. ( 2009). Plasticity of transcriptional machinery in bacteria is increased by the repertoire of regulatory families. Comput Biol Chem 33:261–268 [View Article][PubMed]
    [Google Scholar]
  26. Körner H., Sofia H. J., Zumft W. G. ( 2003). Phylogeny of the bacterial superfamily of Crp–Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 27:559–592 [View Article][PubMed]
    [Google Scholar]
  27. Kummerfeld S. K., Teichmann S. A. ( 2006). DBD: a transcription factor prediction database. Nucleic Acids Res 34:Database issueD74–D81 [View Article][PubMed]
    [Google Scholar]
  28. Lespinet O., Wolf Y. I., Koonin E. V., Aravind L. ( 2002). The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12:1048–1059 [View Article][PubMed]
    [Google Scholar]
  29. Levine M., Tjian R. ( 2003). Transcription regulation and animal diversity. Nature 424:147–151 [View Article][PubMed]
    [Google Scholar]
  30. Lynch M. ( 2006). Streamlining and simplification of microbial genome architecture. Annu Rev Microbiol 60:327–349 [View Article][PubMed]
    [Google Scholar]
  31. Lynch M., Conery J. S. ( 2003). The origins of genome complexity. Science 302:1401–1404 [View Article][PubMed]
    [Google Scholar]
  32. Madan Babu M., Teichmann S. A. ( 2003). Evolution of transcription factors and the gene regulatory network in Escherichia coli . Nucleic Acids Res 31:1234–1244 [View Article][PubMed]
    [Google Scholar]
  33. Madan Babu M., Teichmann S. A., Aravind L. ( 2006). Evolutionary dynamics of prokaryotic transcriptional regulatory networks. J Mol Biol 358:614–633 [View Article][PubMed]
    [Google Scholar]
  34. Maddocks S. E., Oyston P. C. ( 2008). Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154:3609–3623 [View Article][PubMed]
    [Google Scholar]
  35. Martínez-Antonio A., Janga S. C., Salgado H., Collado-Vides J. ( 2006). Internal-sensing machinery directs the activity of the regulatory network in Escherichia coli . Trends Microbiol 14:22–27 [View Article][PubMed]
    [Google Scholar]
  36. Martínez-Núñez M. A., Pérez-Rueda E., Gutiérrez-Ríos R. M., Merino E. ( 2010). New insights into the regulatory networks of paralogous genes in bacteria. Microbiology 156:14–22 [View Article][PubMed]
    [Google Scholar]
  37. Merino E., Yanofsky C. ( 2005). Transcription attenuation: a highly conserved regulatory strategy used by bacteria. Trends Genet 21:260–264 [View Article][PubMed]
    [Google Scholar]
  38. Miroslavova N. S., Busby S. J. ( 2006). Investigations of the modular structure of bacterial promoters. Biochem Soc Symp731–10[PubMed]
    [Google Scholar]
  39. Moreno-Campuzano S., Janga S. C., Pérez-Rueda E. ( 2006). Identification and analysis of DNA-binding transcription factors in Bacillus subtilis and other Firmicutes – a genomic approach. BMC Genomics 7:147 [View Article][PubMed]
    [Google Scholar]
  40. Oliynyk M., Samborskyy M., Lester J. B., Mironenko T., Scott N., Dickens S., Haydock S. F., Leadlay P. F. ( 2007). Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL23338. Nat Biotechnol 25:447–453 [View Article][PubMed]
    [Google Scholar]
  41. Pennella M. A., Giedroc D. P. ( 2005). Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators. Biometals 18:413–428 [View Article][PubMed]
    [Google Scholar]
  42. Peres C. M., Harwood C. S. ( 2006). BadM is a transcriptional repressor and one of three regulators that control benzoyl coenzyme A reductase gene expression in Rhodopseudomonas palustris. J Bacteriol 188:8662–8665 [View Article][PubMed]
    [Google Scholar]
  43. Pérez-Rueda E., Collado-Vides J. ( 2001). Common history at the origin of the position–function correlation in transcriptional regulators in archaea and bacteria. J Mol Evol 53:172–179 [View Article][PubMed]
    [Google Scholar]
  44. Pérez-Rueda E., Janga S. C. ( 2010). Identification and genomic analysis of transcription factors in archaeal genomes exemplifies their functional architecture and evolutionary origin. Mol Biol Evol 27:1449–1459 [View Article][PubMed]
    [Google Scholar]
  45. Pérez-Rueda E., Collado-Vides J., Segovia L. ( 2004). Phylogenetic distribution of DNA-binding transcription factors in bacteria and archaea. Comput Biol Chem 28:341–350 [View Article][PubMed]
    [Google Scholar]
  46. Pérez-Rueda E., Janga S. C., Martínez-Antonio A. ( 2009). Scaling relationship in the gene content of transcriptional machinery in bacteria. Mol Biosyst 5:1494–1501 [View Article][PubMed]
    [Google Scholar]
  47. Rigali S., Derouaux A., Giannotta F., Dusart J. ( 2002). Subdivision of the helix–turn–helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J Biol Chem 277:12507–12515 [View Article][PubMed]
    [Google Scholar]
  48. Rigali S., Schlicht M., Hoskisson P., Nothaft H., Merzbacher M., Joris B., Titgemeyer F. ( 2004). Extending the classification of bacterial transcription factors beyond the helix–turn–helix motif as an alternative approach to discover new cis/trans relationships. Nucleic Acids Res 32:3418–3426 [View Article][PubMed]
    [Google Scholar]
  49. Rodionov D. A., Dubchak I., Arkin A., Alm E., Gelfand M. S. ( 2004). Reconstruction of regulatory and metabolic pathways in metal-reducing delta-proteobacteria. Genome Biol 5:R90 [View Article][PubMed]
    [Google Scholar]
  50. Shimoni Y., Altuvia S., Margalit H., Biham O. ( 2009). Stochastic analysis of the SOS response in Escherichia coli . PLoS ONE 4:e5363 [View Article][PubMed]
    [Google Scholar]
  51. Sierro N., Makita Y., de Hoon M., Nakai K. ( 2008). DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res 36:Database issueD93–D96 [View Article][PubMed]
    [Google Scholar]
  52. Taraban M., Zhan H., Whitten A. E., Langley D. B., Matthews K. S., Swint-Kruse L., Trewhella J. ( 2008). Ligand-induced conformational changes and conformational dynamics in the solution structure of the lactose repressor protein. J Mol Biol 376:466–481 [View Article][PubMed]
    [Google Scholar]
  53. Tordai H., Nagy A., Farkas K., Bányai L., Patthy L. ( 2005). Modules, multidomain proteins and organismic complexity. FEBS J 272:5064–5078 [View Article][PubMed]
    [Google Scholar]
  54. van Nimwegen E. ( 2003). Scaling laws in the functional content of genomes. Trends Genet 19:479–484 [View Article][PubMed]
    [Google Scholar]
  55. Wall M. E., Hlavacek W. S., Savageau M. A. ( 2004). Design of gene circuits: lessons from bacteria. Nat Rev Genet 5:34–42 [View Article][PubMed]
    [Google Scholar]
  56. West G. B., Brown J. H. ( 2005). The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592 [View Article][PubMed]
    [Google Scholar]
  57. Wösten M. M. ( 1998). Eubacterial sigma-factors. FEMS Microbiol Rev 22:127–150 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.050617-0
Loading
/content/journal/micro/10.1099/mic.0.050617-0
Loading

Data & Media loading...

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