A phylogenomic analysis of bacterial helix-turn-helix transcription factors

FEMS Microbiology Reviews

Volumn 33, Issue 2, 2009, Pages 411-429

  Santos, Catarina L ^a,b   Tavares, Fernando ^a,b   Thioulouse, Jean ^c,d   Normand, Philippe ^c,e  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITÉ LYON 1   (France)

^e University of Lyon   (France)

Author keywords

Ecological adaptability; Helix turn helix; Transcriptional regulators

Indexed keywords

HELIX LOOP HELIX PROTEIN;

BACILLUS SUBTILIS; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BIOREMEDIATION; BIOTOPE; DNA TRANSCRIPTION; GENOMICS; INFECTION CONTROL; NEISSERIA GONORRHOEAE; NONHUMAN; PHYLOGENY; PSEUDOMONAS PUTIDA; REVIEW; STAPHYLOCOCCUS AUREUS; XANTHOMONAS;

BACTERIA (MICROORGANISMS);

EID: 60149085847     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2008.00154.x     Document Type: Review

References (94)

1. Ahmed M, Borsch CM, Taylor SS, Vazquez-Laslop N Neyfakh AA (1994) A protein that activates expression of a multidrug efflux transporter upon binding the transporter substrates. J Biol Chem 269 : 28506 28513.
2. Alekshun MN Levy SB (1999) The mar regulon: multiple resistance to antibiotics and other toxic chemicals. Trends Microbiol 7 : 410 413.
3. Aravind L, Anantharaman V, Balaji S, Babu MM Iyer LM (2005) The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 29 : 231 262.
4. Babu MM Aravind L (2006) Adaptive evolution by optimizing expression levels in different environments. Trends Microbiol 14 : 11 14.
5. Berish SA, Subbarao S, Chen CY, Trees DL Morse SA (1993) Identification and cloning of a fur homolog from Neisseria gonorrhoeae. Infect Immun 61 : 4599 4606.
6. Bertani I, Kojic M Venturi V (2001) Regulation of the p-hydroxybenzoic acid hydroxylase gene (pobA) in plant-growth-promoting Pseudomonas putida WCS358. Microbiology 147 : 1611 1620.
7. Bertin PN, Medigue C Normand P (2008) Advances in environmental genomics: towards an integrated view of micro-organisms and ecosystems. Microbiology 154 : 347 359.
8. Campos E, Baldoma L, Aguilar J Badia J (2004) Regulation of expression of the divergent ulaG and ulaABCDEF operons involved in LaAscorbate dissimilation in Escherichia coli. J Bacteriol 186 : 1720 1728.
9. Cavalier-Smith T (2005) Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann Bot (London) 95 : 147 175.
10. Charoenpanich J, Tani A, Moriwaki N, Kimbara K Kawai F (2006) Dual regulation of a polyethylene glycol degradative operon by AraC-type and GalR-type regulators in Sphingopyxis macrogoltabida strain 103. Microbiology 152 : 3025 3034.
11. Chatterjee J, Miyamoto CM, Zouzoulas A, Lang BF, Skouris N Meighen EA (2002) MetR and CRP bind to the Vibrio harveyi lux promoters and regulate luminescence. Mol Microbiol 46 : 101 111.
12. Chattopadhyay MK (2006) Mechanism of bacterial adaptation to low temperature. J Biosci 31 : 157 165.
13. Chen Y Rosen BP (1997) Metalloregulatory properties of the ArsD repressor. J Biol Chem 272 : 14257 14262.
14. Coenye T, Gevers D, Van de Peer Y, Vandamme P Swings J (2005) Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29 : 147 167.
15. D'Amico S, Collins T, Marx JC, Feller G Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7 : 385 389.
16. Dattelbaum JD, Lockatell CV, Johnson DE Mobley HL (2003) UreR, the transcriptional activator of the Proteus mirabilis urease gene cluster is required for urease activity and virulence in experimental urinary tract infections. Infect Immun 71 : 1026 1030.
17. Day WA Maurelli AT (2006) Black holes and antivirulence genes: selection for gene loss as part of the evolution of bacterial pathogens. Evolution of Microbial Pathogens (Seifert HS DiRita VJ, eds), pp. 109 122. ASM Press, Washington, DC.
18. Deming JW (2002) Psychrophiles and polar regions. Curr Opin Microbiol 5 : 301 309.
19. Dethlefsen L, McFall-Ngai M Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449 : 811 818.
20. Egan SM (2002) Growing repertoire of AraC/XylS activators. J Bacteriol 184 : 5529 5532.
21. Egland PG Harwood CS (1999) BadR, a new MarR family member, regulates anaerobic benzoate degradation by Rhodopseudomonas palustris in concert with AadR, an Fnr family member. J Bacteriol 181 : 2102 2109.
22. Escolar L, Perez-Martin J de Lorenzo V (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181 : 6223 6229.
23. Ferluga S, Bigirimana J, Höfte M Venturi V (2007) A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol Plant Pathol 8 : 529 538.
24. Ferrandez A, Minambres B, Garcia B, Olivera ER, Luengo JM, Garcia JL Diaz E (1998) Catabolism of phenylacetic acid in Escherichia coli. Characterization of a new aerobic hybrid pathway. J Biol Chem 273 : 25974 25986.
25. Frota CC, Papavinasasundaram KG, Davis EO Colston MJ (2004) The AraC family transcriptional regulator Rv1931c plays a role in the virulence of Mycobacterium tuberculosis. Infect Immun 72 : 5483 5486.
26. Fuqua C Greenberg EP (1998) Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1 : 183 189.
27. Fuqua C, Winans SC Greenberg EP (1996) Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol 50 : 727 751.
28. Gallegos MT, Schleif R, Bairoch A, Hofmann K Ramos JL (1997) Arac/XylS family of transcriptional regulators. Microbiol Mol Biol R 61 : 393 410.
29. Galvao TC de Lorenzo V (2006) Transcriptional regulators a la carte: engineering new effector specificities in bacterial regulatory proteins. Curr Opin Biotech 17 : 34 42.
30. Godsey MH, Zheleznova Heldwein EE Brennan RG (2002) Structural biology of bacterial multidrug resistance gene regulators. J Biol Chem 277 : 40169 40172.
31. Gold B, Rodriguez GM, Marras SA, Pentecost M Smith I (2001) The Mycobacterium tuberculosis IdeR is a dual functional regulator that controls transcription of genes involved in iron acquisition, iron storage and survival in macrophages. Mol Microbiol 42 : 851 865.
32. Guazzaroni ME, Krell T, Felipe A, Ruiz R, Meng C, Zhang X, Gallegos MT Ramos JL (2005) The multidrug efflux regulator TtgV recognizes a wide range of structurally different effectors in solution and complexed with target DNA: evidence from isothermal titration calorimetry. J Biol Chem 280 : 20887 20893.
33. Haine V, Sinon A, Van Steen F, Rousseau S, Dozot M, Lestrate P, Lambert C, Letesson JJ De Bolle X (2005) Systematic targeted mutagenesis of Brucella melitensis 16M reveals a major role for GntR regulators in the control of virulence. Infect Immun 73 : 5578 5586.
34. Haine V, Dozot M, Dornand J, Letesson JJ De Bolle X (2006) NnrA is required for full virulence and regulates several Brucella melitensis denitrification genes. J Bacteriol 188 : 1615 1619.
35. Hanssler E, Muller T, Jessberger N, Volzke A, Plassmeier J, Kalinowski J, Kramer R Burkovski A (2007) FarR, a putative regulator of amino acid metabolism in Corynebacterium glutamicum. Appl Microbiol Biotechnol 76 : 625 632.
36. Hantke K (1981) Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182 : 288 292.
37. Hentschel U, Steinert M Hacker J (2000) Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol 8 : 226 231.
38. Hobman JL, Wilkie J Brown NL (2005) A design for life: prokaryotic metal-binding MerR family regulators. Biometals 18 : 429 436.
39. Hoskisson PA, Rigali S, Fowler K, Findlay KC Buttner MJ (2006) DevA, a GntR-like transcriptional regulator required for development in Streptomyces coelicolor. J Bacteriol 188 : 5014 5023.
40. Iriti M Faoro F (2007) Review of innate and specific immunity in plants and animals. Mycopathologia 164 : 57 64.
41. Joshi MV, Bignell DR, Johnson EG, Sparks JP, Gibson DM Loria R (2007) The AraC/XylS regulator TxtR modulates thaxtomin biosynthesis and virulence in Streptomyces scabies. Mol Microbiol 66 : 633 642.
42. Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S Givskov M (2005) The LuxR receptor: the sites of interaction with quorum-sensing signals and inhibitors. Microbiology 151 : 3589 3602.
43. Kohn WD, Mant CT Hodges RS (1997) Alpha-helical protein assembly motifs. J Biol Chem 272 : 2583 2586.
44. Korner H, Sofia HJ Zumft WG (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.
45. Kotelnikova EA, Makeev VJ Gelfand MS (2005) Evolution of transcription factor DNA binding sites. Gene 347 : 255 263.
46. Kreft J Vazquez-Boland JA (2001) Regulation of virulence genes in Listeria. Int J Med Microbiol 291 : 145 157.
47. Kuroda M, Hayashi H Ohta T (1999) Chromosome-determined zinc-responsible operon czr in Staphylococcus aureus strain 912. Microbiol Immunol 43 : 115 125.
48. Lawrence JG (2006) Studying evolution using genome sequence data. Evolution of Microbial Pathogens (Seifert HS DiRita VJ, eds), pp. 11 33. ASM Press, Washington, DC.
49. Letunic I, Copley RR, Pils B, Pinkert S, Schultz J Bork P (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34 : D257 D260.
50. Liu G, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G Wei Y (2006) Targeted alterations in iron homeostasis underlie plant defense responses. J Cell Sci 120 : 596 605.
51. Lopez O, Morera C, Miranda-Rios J, Girard L, Romero D Soberon M (2001) Regulation of gene expression in response to oxygen in Rhizobium etli: role of FnrN in fixNOQP expression and in symbiotic nitrogen fixation. J Bacteriol 183 : 6999 7006.
52. Lozada-Chavez I, Janga SC Collado-Vides J (2006) Bacterial regulatory networks are extremely flexible in evolution. Nucleic Acids Res 34 : 3434 3445.
53. Martinez-Antonio A Collado-Vides J (2003) Identifying global regulators in transcriptional regulatory networks in bacteria. Curr Opin Microbiol 6 : 482 489.
54. Mole BM, Baltrus DA, Dangl JL Grant SR (2007) Global virulence regulation networks in phytopathogenic bacteria. Trends in Microbiol 15 : 363 371.
55. Munson GP, Holcomb LG Scott JR (2001) Novel group of virulence activators within the AraC family that are not restricted to upstream binding sites. Infect Immun 69 : 186 193.
56. Nurnberger T, Brunner F, Kemmerling B Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198 : 249 266.
57. Ofria C, Adami C Collier TC (2003) Selective pressures on genomes in molecular evolution. J Theor Biol 222 : 477 483.
58. Oram DM, Avdalovic A Holmes RK (2004) Analysis of genes that encode DtxR-like transcriptional regulators in pathogenic and saprophytic corynebacterial species. Infect Immun 72 : 1885 1895.
59. Outten FW, Outten CE O'Halloran TV (2000) Metalloregulatory systems at the interface between bacterial metal homeostasis and resistance. Bacterial Stress Responses (Storz G Hengge-Aronis R, eds), pp. 145 157. ASM Press, Washington, DC.
60. Perrenoud A Sauer U (2005) Impact of global transcriptional regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on glucose catabolism in Escherichia coli. J Bacteriol 187 : 3171 3179.
61. Pomposiello PJ Demple B (2001) Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19 : 109 114.
62. Providenti MA Wyndham RC (2001) Identification and functional characterization of CbaR, a MarR-like modulator of the cbaABC-encoded chlorobenzoate catabolism pathway. Appl Environ Microbiol 67 : 3530 3541.
63. Pym AS, Domenech P, Honore N, Song J, Deretic V Cole ST (2001) Regulation of catalase-peroxidase (KatG) expression, isoniazid sensitivity and virulence by furA of Mycobacterium tuberculosis. Mol Microbiol 40 : 879 889.
64. Ranea JA (2006) Genome evolution: micro(be)-economics. Heredity 96 : 337 338.
65. Rasmussen TB Givskov M (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296 : 149 161.
66. Rea RB, Gahan CG Hill C (2004) Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect Immun 72 : 717 727.
67. Ren J, Sainsbury S, Combs SE, Capper RG, Jordan PW, Berrow NS, Stammers DK, Saunders NJ Owens RJ (2007) The structure and transcriptional analysis of a global regulator from Neisseria meningitidis. J Biol Chem 282 : 14655 14664.
68. Roberts RJ (2004) Identifying protein function - a call for community action. PLOS Biol 2 : 293.
69. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK Smith I (2002) ideR, An essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 70 : 3371 3381.
70. Rolff J (2007) Why did the acquired immune system of vertebrates evolve? Dev Comp Immunol 31 : 476 482.
71. Rosinski JA Atchley WR (1999) Molecular evolution of helix-turn-helix proteins. J Mol Evol 49 : 301 309.
72. Rouquette C, Harmon JB Shafer WM (1999) Induction of the mtrCDE-encoded efflux pump system of Neisseria gonorrhoeae requires MtrA, an AraC-like protein. Mol Microbiol 33 : 651 658.
73. Santos C, Vieira J, Tavares F, Benson D, Tisa L, Berry A, Moradas-Ferreira P Normand P (2008) On the nature of fur evolution: a phylogenetic approach in Actinobacteria. BMC Evol Biol 8 : 185.
74. Shevchik VE Hugouvieux-Cotte-Pattat N (2003) PaeX, a second pectin acetylesterase of Erwinia chrysanthemi 3937. J Bacteriol 185 : 3091 3100.
75. Slobodkin AI (2005) Thermophilic microbial metal reduction. Mikrobiologiia 74 : 581 595.
76. Smidt H, Van Leest M, van der Oost J de Vos WM (2000) Transcriptional regulation of the cpr gene cluster in ortho-chlorophenol-respiring Desulfitobacterium dehalogenans. J Bacteriol 182 : 5683 5691.
77. Soutourina O, Kolb A, Krin E, Laurent-Winter C, Rimsky S, Danchin A Bertin P (1999) Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181 : 7500 7508.
78. Thomson NR, Crow MA, McGowan SJ, Cox A Salmond GP (2000) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36 : 539 556.
79. Tolmasky ME, Wertheimer AM, Actis LA Crosa JH (1994) Characterization of the Vibrio anguillarum fur gene: role in regulation of expression of the FatA outer membrane protein and catechols. J Bacteriol 176 : 213 220.
80. Trindade MI, Abratt VR Reid SJ (2003) Induction of sucrose utilization genes from Bifidobacterium lactis by sucrose and raffinose. Appl Environ Microbiol 69 : 24 32.
81. Tropel D van der Meer JR (2004) Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol Mol Biol Rev 68 : 474 500.
82. Tsoi TV, Plotnikova EG, Cole JR, Guerin WF, Bagdasarian M Tiedje JM (1999) Cloning, expression, and nucleotide sequence of the Pseudomonas aeruginosa 142 ohb genes coding for oxygenolytic ortho dehalogenation of halobenzoates. Appl Environ Microbiol 65 : 2151 2162.
83. Ulrich LE, Koonin EV Zhulin IB (2005) One-component systems dominate signal transduction in prokaryotes. Trends Microbiol 13 : 52 56.
84. van Delden C, Comte R Bally AM (2001) Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J Bacteriol 183 : 5376 5384.
85. Van Houdt R, Givskov M Michiels CW (2007a) Quorum sensing in Serratia. FEMS Microbiol Rev 31 : 407 424.
86. Van Houdt R, Moons P, Aertsen A, Jansen A, Vanoirbeek K, Daykin M, Williams P Michiels CW (2007b) Characterization of a luxI/luxR-type quorum sensing system and N-acyl-homoserine lactone-dependent regulation of exo-enzyme and antibacterial component production in Serratia plymuthica RVH1. Res Microbiol 158 : 150 158.
87. von Mering C, Hugenholtz P, Raes J, Tringe SG, Doerks T, Jensen LJ, Ward N Bork P (2007) Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315 : 1126 1130.
88. Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58 : 236 244.
89. Wilmes P Bond PL (2006) Metaproteomics: studying functional gene expression in microbial ecosystems. Trends Microbiol 14 : 92 97.
90. Yokoyama K, Ishijima SA, Clowney L, Koike H, Aramaki H, Tanaka C, Makino K Suzuki M (2006) Feast/famine regulatory proteins (FFRPs): Escherichia coli Lrp, AsnC and related archaeal transcription factors. FEMS Microbiol Rev 30 : 89 108.
91. Zhang Z, Gosset G, Barabote R, Gonzalez CS, Cuevas WA Saier MH Jr. (2005) Functional interactions between the carbon and iron utilization regulators, Crp and Fur, in Escherichia coli. J Bacteriol 187 : 980 990.
92. Zheng H, Zhong Z, Lai X, Chen WX, Li S Zhu J (2006) A LuxR/LuxI-type quorum-sensing system in a plant bacterium, Mesorhizobium tianshanense, controls symbiotic nodulation. J Bacteriol 188 : 1943 1949.
93. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. P Natl Acad Sci USA 99 : 3129 3134.
94. Zipfel C Felix G (2005) Plants and animals: a different taste for microbes? Curr Opin Plant Biol 8 : 353 360.