Dissecting the protein architecture of DNA-binding transcription factors in bacteria and archaea Free

Abstract

Gene regulation at the transcriptional level is a central process in all organisms where DNA-binding transcription factors play a fundamental role. This class of proteins binds specifically at DNA sequences, activating or repressing gene expression as a function of the cell’s metabolic status, operator context and ligand-binding status, among other factors, through the DNA-binding domain (DBD). In addition, TFs may contain partner domains (PaDos), which are involved in ligand binding and protein–protein interactions. In this work, we systematically evaluated the distribution, abundance and domain organization of DNA-binding TFs in 799 non-redundant bacterial and archaeal genomes. We found that the distributions of the DBDs and their corresponding PaDos correlated with the size of the genome. We also identified specific combinations between the DBDs and their corresponding PaDos. Within each class of DBDs there are differences in the actual angle formed at the dimerization interface, responding to the presence/absence of ligands and/or crystallization conditions, setting the orientation of the resulting helices and wings facing the DNA. Our results highlight the importance of PaDos as central elements that enhance the diversity of regulatory functions in all bacterial and archaeal organisms, and our results also demonstrate the role of PaDos in sensing diverse signal compounds. The highly specific interactions between DBDs and PaDos observed in this work, together with our structural analysis highlighting the difficulty in predicting both inter-domain geometry and quaternary structure, suggest that these systems appeared once and evolved with diverse duplication events in all the analysed organisms.

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2017-08-01
2024-03-30
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References

  1. Martínez-Antonio A, Janga SC, Salgado H, Collado-Vides J. Internal-sensing machinery directs the activity of the regulatory network in Escherichia coli. Trends Microbiol 2006; 14:22–27 [View Article][PubMed]
    [Google Scholar]
  2. Miroslavova NS, Busby SJW. Structure of bacterial promoters. Biochem Soc Symp 2006; 10:1–10 [CrossRef]
    [Google Scholar]
  3. Wall ME, Hlavacek WS, Savageau MA. Design of gene circuits: lessons from bacteria. Nat Rev Genet 2004; 5:34–42 [View Article][PubMed]
    [Google Scholar]
  4. Madan Babu M, Teichmann SA. Evolution of transcription factors and the gene regulatory network in Escherichia coli. Nucleic Acids Res 2003; 31:1234–1244 [View Article][PubMed]
    [Google Scholar]
  5. Charoensawan V, Wilson D, Teichmann SA. Genomic repertoires of DNA-binding transcription factors across the tree of life. Nucleic Acids Res 2010; 38:7364–7377 [View Article][PubMed]
    [Google Scholar]
  6. Rivera-Gómez N, Segovia L, Pérez-Rueda E. Diversity and distribution of transcription factors: their partner domains play an important role in regulatory plasticity in bacteria. Microbiology 2011; 157:2308–2318 [View Article][PubMed]
    [Google Scholar]
  7. Schreiter ER, Drennan CL. Ribbon-helix-helix transcription factors: variations on a theme. Nat Rev Microbiol 2007; 5:710–720 [View Article][PubMed]
    [Google Scholar]
  8. Martínez-Núñez MA, Poot-Hernandez AC, Rodríguez-Vázquez K, Perez-Rueda E. Increments and duplication events of enzymes and transcription factors influence metabolic and regulatory diversity in prokaryotes. PLoS One 2013; 8:e69707 [View Article][PubMed]
    [Google Scholar]
  9. Wilson D, Charoensawan V, Kummerfeld SK, Teichmann SA. DBD-taxonomically broad transcription factor predictions: new content and functionality. Nucleic Acids Res 2008; 36:D88–D92 [View Article][PubMed]
    [Google Scholar]
  10. Gama-Castro S, Jiménez-Jacinto V, Peralta-Gil M, Santos-Zavaleta A, Peñaloza-Spinola MI et al. RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and textpresso navigation. Nucleic Acids Res 2008; 36:D120–D124 [View Article][PubMed]
    [Google Scholar]
  11. Sierro N, Makita Y, de Hoon M, Nakai K. DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res 2008; 36:D93–D96 [View Article][PubMed]
    [Google Scholar]
  12. Wilson D, Pethica R, Zhou Y, Talbot C, Vogel C et al. SUPERFAMILY-sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res 2009; 37:D380–D386 [View Article][PubMed]
    [Google Scholar]
  13. Saeed AI, Sharov V, White J, Li J, Liang W et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003; 34:374–378[PubMed]
    [Google Scholar]
  14. R Development Core Team A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna, Austria: R Core Team; 2011 pp. 409
    [Google Scholar]
  15. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996; 14:33–38 [View Article][PubMed]
    [Google Scholar]
  16. Galán-Vásquez E, Sánchez-Osorio I, Martínez-Antonio A. Transcription factors exhibit differential conservation in bacteria with reduced genomes. PLoS One 2016; 11:e0146901 [View Article][PubMed]
    [Google Scholar]
  17. Zhao W, Zhong Y, Yuan H, Wang J, Zheng H et al. Complete genome sequence of the rifamycin SV-producing Amycolatopsis mediterranei U32 revealed its genetic characteristics in phylogeny and metabolism. Cell Res 2010; 20:1096–1108 [View Article][PubMed]
    [Google Scholar]
  18. Gough J, Chothia C. SUPERFAMILY: HMMs representing all proteins of known structure. SCOP sequence searches, alignments and genome assignments. Nucleic Acids Res 2002; 30:268–272 [View Article][PubMed]
    [Google Scholar]
  19. Gotfredsen M, Gerdes K. The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Mol Microbiol 1998; 29:1065–1076 [View Article][PubMed]
    [Google Scholar]
  20. Itzkovitz S, Tlusty T, Alon U. Coding limits on the number of transcription factors. BMC Genomics 2006; 7:239 [View Article][PubMed]
    [Google Scholar]
  21. Ravcheev DA, Khoroshkin MS, Laikova ON, Tsoy OV, Sernova NV et al. Comparative genomics and evolution of regulons of the LacI-family transcription factors. Front Microbiol 2014; 5:1 [View Article][PubMed]
    [Google Scholar]
  22. Martínez-Hackert E, Stock AM. Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 1997; 269:301–312 [View Article][PubMed]
    [Google Scholar]
  23. Guédon E, Jamet E, Renault P. Gene regulation in Lactococcus lactis: the gap between predicted and characterized regulators. Antonie van Leeuwenhoek 2002; 82:93–112 [View Article][PubMed]
    [Google Scholar]
  24. Armenta-Medina D, Segovia L, Perez-Rueda E. Comparative genomics of nucleotide metabolism: a tour to the past of the three cellular domains of life. BMC Genomics 2014; 15:800–816 [View Article][PubMed]
    [Google Scholar]
  25. Poot-Hernandez AC, Rodriguez-Vazquez K, Perez-Rueda E. The alignment of enzymatic steps reveals similar metabolic pathways and probable recruitment events in Gammaproteobacteria. BMC Genomics 2015; 16:1–14 [View Article][PubMed]
    [Google Scholar]
  26. Weissbach H, Brot N. Regulation of methionine synthesis in Escherichia coli. Mol Microbiol 1991; 5:1593–1597 [View Article][PubMed]
    [Google Scholar]
  27. Coles M, Djuranovic S, Söding J, Frickey T, Koretke K et al. AbrB-like transcription factors assume a swapped hairpin fold that is evolutionarily related to double-psi β barrels. Structure 2005; 13:919–928 [View Article][PubMed]
    [Google Scholar]
  28. Bobay BG, Andreeva A, Mueller GA, Cavanagh J, Murzin AG. Revised structure of the AbrB N-terminal domain unifies a diverse superfamily of putative DNA-binding proteins. FEBS Lett 2005; 579:5669–5674 [View Article][PubMed]
    [Google Scholar]
  29. Adams MA, Udell CM, Pal GP, Jia Z. MraZ from Escherichia coli: cloning, purification, crystallization and preliminary X-ray analysis. Acta Crystallogr Sect F Struct Biol Cryst Commun 2005; 61:378–380 [View Article][PubMed]
    [Google Scholar]
  30. Vaughn JL, Feher V, Naylor S, Strauch MA, Cavanagh J. Novel DNA binding domain and genetic regulation model of Bacillus subtilis transition state regulator abrB. Nat Struct Biol 2000; 7:1139–1146 [View Article][PubMed]
    [Google Scholar]
  31. Perederina A, Svetlov V, Vassylyeva MN, Tahirov TH, Yokoyama S et al. Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription. Cell 2004; 118:297–309 [View Article][PubMed]
    [Google Scholar]
  32. Furman R, Sevostyanova A, Artsimovitch I. Transcription initiation factor DksA has diverse effects on RNA chain elongation. Nucleic Acids Res 2012; 40:3392–3402 [View Article][PubMed]
    [Google Scholar]
  33. Bignell C, Thomas CM. The bacterial ParA–ParB partitioning proteins. J Biotechnol 2001; 91:1–34 [View Article][PubMed]
    [Google Scholar]
  34. Lehnen D, Blumer C, Polen T, Wackwitz B, Wendisch VF et al. LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol Microbiol 2002; 45:521–532 [View Article][PubMed]
    [Google Scholar]
  35. Sharp FC, Sperandio V. QseA directly activates transcription of LEE1 in enterohemorrhagic Escherichia coli. Infect Immun 2007; 75:2432–2440 [View Article][PubMed]
    [Google Scholar]
  36. Huber H, Hohn MJ, Stetter KO, Rachel R. The phylum Nanoarchaeota: present knowledge and future perspectives of a unique form of life. Res Microbiol 2003; 154:165–171 [View Article][PubMed]
    [Google Scholar]
  37. Merhej V, Royer-Carenzi M, Pontarotti P, Raoult D. Massive comparative genomic analysis reveals convergent evolution of specialized bacteria. Biol Direct 2009; 4:13 [View Article][PubMed]
    [Google Scholar]
  38. Stingl U, Radek R, Yang H, Brune A. “Endomicrobia”: cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes. Appl Environ Microbiol 2005; 71:1473–1479 [View Article][PubMed]
    [Google Scholar]
  39. Podar M, Makarova KS, Graham DE, Wolf YI, Koonin EV et al. Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park. Biol Direct 2013; 8:9 [View Article][PubMed]
    [Google Scholar]
  40. Caetano-Anollés G, Wang M, Caetano-Anollés D, Mittenthal JE. The origin, evolution and structure of the protein world. Biochem J 2009; 417:621–637 [View Article][PubMed]
    [Google Scholar]
  41. Santero E, Hoover TR, North AK, Berger DK, Porter SC et al. Role of integration host factor in stimulating transcription from the sigma 54-dependent nifH promoter. J Mol Biol 1992; 227:602–620 [View Article][PubMed]
    [Google Scholar]
  42. Busby S, Ebright RH. Transcription activation by catabolite activator protein (CAP). J Mol Biol 1999; 293:199–213 [View Article][PubMed]
    [Google Scholar]
  43. Körner H, Sofia HJ, Zumft WG. Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 2003; 27:559–592 [View Article][PubMed]
    [Google Scholar]
  44. Rafferty JA, Elder RH, Watson AJ, Cawkwell L, Potter PM et al. Isolation and partial characterisation of a Chinese hamster O6-alkylguanine-DNA alkyltransferase cDNA. Nucleic Acids Res 1992; 20:1891–1895 [View Article][PubMed]
    [Google Scholar]
  45. Zhang D, Kiyatkin A, Bolin JT, Low PS. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3 crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood 2008; 96:2925–2933
    [Google Scholar]
  46. Bateman A. The SIS domain: a phosphosugar-binding domain. Trends Biochem Sci 1999; 24:94–95 [View Article][PubMed]
    [Google Scholar]
  47. Barragán MJ, Blázquez B, Zamarro MT, Mancheño JM, García JL et al. BzdR, a repressor that controls the anaerobic catabolism of benzoate in Azoarcus sp. CIB, is the first member of a new subfamily of transcriptional regulators. J Biol Chem 2005; 280:10683–10694 [View Article][PubMed]
    [Google Scholar]
  48. Kulinska A, Czeredys M, Hayes F, Jagura-Burdzy G. Genomic and functional characterization of the modular broad-host-range RA3 plasmid, the archetype of the IncU group. Appl Environ Microbiol 2008; 74:4119–4132 [View Article][PubMed]
    [Google Scholar]
  49. Kohl M, Wiese S, Warscheid B. Cytoscape: software for visualization and analysis of biological networks; 2011291–303
  50. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [View Article][PubMed]
    [Google Scholar]
  51. Fukami-Kobayashi K, Tateno Y, Nishikawa K. Parallel evolution of ligand specificity between LacI/GalR family repressors and periplasmic sugar-binding proteins. Mol Biol Evol 2003; 20:267–277 [View Article][PubMed]
    [Google Scholar]
  52. Ranea JA, Buchan DW, Thornton JM, Orengo CA. Evolution of protein superfamilies and bacterial genome size. J Mol Biol 2004; 336:871–887 [View Article][PubMed]
    [Google Scholar]
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