Evolutionary rewiring and reprogramming of bacterial transcription regulation

Journal of Genetics and Genomics

Volumn 38, Issue 7, 2011, Pages 279-288

  Wang, Li ^a,b   Wang, Fang Fang ^a,b,c   Qian, Wei ^a,b  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b National Plant Gene Research Center   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Evo Devo; Molecular evolution; Reprogramming; Rewiring; Transcription regulation

Indexed keywords

BACTERIAL GENE; BACTERIUM; EVOLUTION; GENE DUPLICATION; HORIZONTAL GENE TRANSFER; HUMAN; MICROORGANISM; NONHUMAN; REVIEW; TRANSCRIPTION REGULATION;

ADAPTATION, BIOLOGICAL; BACTERIA; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENETIC SPECIATION; GENOME, BACTERIAL; RECOMBINATION, GENETIC; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS);

EID: 79960469948     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2011.06.001     Document Type: Review

References (78)

1. Alon U. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 2007, 8:450-461.
2. Andersson D.I., Hughes D. Gene amplification and adaptive evolution in bacteria. Annu. Rev. Genet. 2009, 43:167-195.
3. Artsimovitch I., Landick R. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc. Natl. Acad. Sci. USA 2000, 97:7090-7095.
4. Bailey M.J., Hughes C., Koronakis V. RfaH and the ops element, components of a novel system controlling bacterial transcription elongation. Mol. Microbiol. 1997, 26:845-851.
5. Belogurov G.A., Mooney R.A., Svetlov V., Landick R., Artsimovitch I. Functional specialization of transcription elongation factors. EMBO J. 2009, 28:112-122.
6. Belogurov G.A., Vassylyeva M.N., Svetlov V., Klyuyev S., Grishin N.V., Vassylyev D.G., Artsimovitch I. Structural basis for converting a general transcription factor into an operon-specific virulence regulator. Mol. Cell 2007, 26:117-129.
7. Bijlsma J.J., Groisman E.A. The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol. Microbiol. 2005, 57:85-96.
8. Booth L.N., Tuch B.B., Johnson A.D. Intercalation of a new tier of transcription regulation into an ancient circuit. Nature 2010, 468:959-963.
9. Boto L. Horizontal gene transfer in evolution: facts and challenges. Proc. Biol. Sci. 2010, 277:819-827.
10. Britten R.J., Davidson E.H. Gene regulation for higher cells: a theory. Science 1969, 165:349-357.
11. Browning D.F., Busby S.J. The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2004, 2:57-65.
12. Cardinale C.J., Washburn R.S., Tadigotla V.R., Brown L.M., Gottesman M.E., Nudler E. Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 2008, 320:935-938.
13. Carroll S.B. Evolution at two levels: on genes and form. PLoS Biol. 2005, 3:e245.
14. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36.
15. Checa S.K., Espariz M., Audero M.E., Botta P.E., Spinelli S.V., Soncini F.C. Bacterial sensing of and resistance to gold salts. Mol. Microbiol. 2007, 63:1307-1318.
16. Cooper T.F., Remold S.K., Lenski R.E., Schneider D. Expression profiles reveal parallel evolution of epistatic interactions involving the CRP regulon in Escherichia coli. PLoS Genet. 2008, 4:e35.
17. Craven S.H., Neidle E.L. Double trouble: medical implications of genetic duplication and amplification in bacteria. Future Microbiol. 2007, 2:309-321.
18. Darwin C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life 1859, John Murray, London. first ed.
19. de Hoon M.J., Eichenberger P., Vitkup D. Hierarchical evolution of the bacterial sporulation network. Curr. Biol. 2010, 20:R735-R745.
20. Dean A.M., Thornton J.W. Mechanistic approaches to the study of evolution: the functional synthesis. Nat. Rev. Genet. 2007, 8:675-688.
21. Dowell R.D. Transcription factor binding variation in the evolution of gene regulation. Trends Genet. 2010, 26:468-475.
22. Fass E., Groisman E.A. Control of Salmonella pathogenicity island-2 gene expression. Curr. Opin. Microbiol. 2009, 12:199-204.
23. Feng X., Oropeza R., Kenney L.J. Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol. Microbiol. 2003, 48:1131-1143.
24. Feschotte C. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 2008, 9:397-405.
25. Gehring W.J., Ikeo K. Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet. 1999, 15:371-377.
26. Gelfand M.S. Evolution of transcriptional regulatory networks in microbial genomes. Curr. Opin. Struct. Biol. 2006, 16:420-429.
27. Gevers D., Vandepoele K., Simillon C., Van de Peer Y. Gene duplication and biased functional retention of paralogs in bacterial genomes. Trends Microbiol. 2004, 12:148-154.
28. Groisman E.A., Mouslim C. Sensing by bacterial regulatory systems in host and non-host environments. Nat. Rev. Microbiol. 2006, 4:705-709.
29. Gunn J.S., Lim K.B., Krueger J., Kim K., Guo L., Hackett M., Miller S.I. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 1998, 27:1171-1182.
30. Hale C.R., Zhao P., Olson S., Duff M.O., Graveley B.R., Wells L., Terns R.M., Terns M.P. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 2009, 139:945-956.
31. Herpin A., Braasch I., Kraeussling M., Schmidt C., Thoma E.C., Nakamura S., Tanaka M., Schartl M. Transcriptional rewiring of the sex determining dmrt1 gene duplicate by transposable elements. PLoS Genet. 2010, 6:e1000844.
32. Hoekstra H.E., Coyne J.A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 2007, 61:995-1016.
33. Jackson R.W., Johnson L.J., Clarke S.R., Arnold D.L. Bacterial pathogen evolution: breaking news. Trends Genet. 2010, 27:32-40.
34. Jordan I.K., Rogozin I.B., Glazko G.V., Koonin E.V. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 2003, 19:68-72.
35. Juhas M., van der Meer J.R., Gaillard M., Harding R.M., Hood D.W., Crook D.W. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol. Rev. 2009, 33:376-393.
36. Kato A., Mitrophanov A.Y., Groisman E.A. A connector of two-component regulatory systems promotes signal amplification and persistence of expression. Proc. Natl. Acad. Sci. USA 2007, 104:12063-12068.
37. Koonin E.V., Makarova K.S., Aravind L. Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 2001, 55:709-742.
38. Kunarso G., Chia N.Y., Jeyakani J., Hwang C., Lu X., Chan Y.S., Ng H.H., Bourque G. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 2010, 42:631-634.
39. Lind P.A., Tobin C., Berg O.G., Kurland C.G., Andersson D.I. Compensatory gene amplification restores fitness after inter-species gene replacements. Mol. Microbiol. 2010, 75:1078-1089.
40. Lozada-Chavez I., Janga S.C., Collado-Vides J. Bacterial regulatory networks are extremely flexible in evolution. Nucleic Acids Res. 2006, 34:3434-3445.
41. Lucchini S., Rowley G., Goldberg M.D., Hurd D., Harrison M., Hinton J.C. H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog. 2006, 2:e81.
42. Luque I., Andujar A., Jia L., Zabulon G., de Marsac N.T., Flores E., Houmard J. Regulated expression of glutamyl-tRNA synthetase is directed by a mobile genetic element in the cyanobacterium Tolypothrix sp. PCC 7601. Mol. Microbiol. 2006, 60:1276-1288.
43. Mandel M.J., Wollenberg M.S., Stabb E.V., Visick K.L., Ruby E.G. A single regulatory gene is sufficient to alter bacterial host range. Nature 2009, 458:215-218.
44. Martinez-Nunez M.A., Perez-Rueda E., Gutierrez-Rios R.M., Merino E. New insights into the regulatory networks of paralogous genes in bacteria. Microbiology 2010, 156:14-22.
45. Ng W.L., Bassler B.L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 2009, 43:197-222.
46. Ochman H., Lawrence J.G., Groisman E.A. Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405:299-304.
47. Ohno S. Evolution by Gene Duplication 1970, Springer, Berlin.
48. Osborne S.E., Walthers D., Tomljenovic A.M., Mulder D.T., Silphaduang U., Duong N., Lowden M.J., Wickham M.E., Waller R.F., Kenney L.J., Coombes B.K. Pathogenic adaptation of intracellular bacteria by rewiring a cis-regulatory input function. Proc. Natl. Acad. Sci. USA 2009, 106:3982-3987.
49. Paytubi S., Madrid C., Forns N., Nieto J.M., Balsalobre C., Uhlin B.E., Juarez A. YdgT, the Hha paralogue in Escherichia coli, forms heteromeric complexes with H-NS and StpA. Mol. Microbiol. 2004, 54:251-263.
50. Perez Audero M.E., Podoroska B.M., Ibanez M.M., Cauerhff A., Checa S.K., Soncini F.C. Target transcription binding sites differentiate two groups of MerR-monovalent metal ion sensors. Mol. Microbiol. 2010, 78:853-865.
51. Perez J.C., Groisman E.A. Transcription factor function and promoter architecture govern the evolution of bacterial regulons. Proc. Natl. Acad. Sci. USA 2009, 106:4319-4324.
52. Perez J.C., Groisman E.A. Evolution of transcriptional regulatory circuits in bacteria. Cell 2009, 138:233-244.
53. Perez J.C., Latifi T., Groisman E.A. Overcoming H-NS-mediated transcriptional silencing of horizontally acquired genes by the PhoP and SlyA proteins in Salmonella enterica. J. Biol. Chem. 2008, 283:10773-10783.
54. 2+ homeostasis. PLoS Genet. 2009, 5:e1000428.
55. Peter I.S., Davidson E.H. Evolution of gene regulatory networks controlling body plan development. Cell 2011, 144:970-985.
56. Petersen C., Moller L.B., Valentin-Hansen P. The cryptic adenine deaminase gene of Escherichia coli. Silencing by the nucleoid-associated DNA-binding protein, H-NS, and activation by insertion elements. J. Biol. Chem. 2002, 277:31373-31380.
57. Pontel L.B., Audero M.E., Espariz M., Checa S.K., Soncini F.C. GolS controls the response to gold by the hierarchical induction of Salmonella-specific genes that include a CBA efflux-coding operon. Mol. Microbiol. 2007, 66:814-825.
58. Price M.N., Dehal P.S., Arkin A.P. Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol. 2008, 9:R4.
59. Qian W., Han Z.J., He C. Two-component signal transduction systems of Xanthomonas spp.: a lesson from genomics. Mol. Plant Microbe Interact. 2008, 21:151-161.
60. E stress response in related genomes. PLoS Biol. 2006, 4:e2.
61. Rodionov D.A., Mironov A.A., Gelfand M.S. Conservation of the biotin regulon and the BirA regulatory signal in Eubacteria and Archaea. Genome Res. 2002, 12:1507-1516.
62. Sandegren L., Andersson D.I. Bacterial gene amplification: implications for the evolution of antibiotic resistance. Nat. Rev. Microbiol. 2009, 7:578-588.
63. Sharma C.M., Hoffmann S., Darfeuille F., Reignier J., Findeiss S., Sittka A., Chabas S., Reiche K., Hackermuller J., Reinhardt R., Stadler P.F., Vogel J. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010, 464:250-255.
64. Soo V.W., Hanson-Manful P., Patrick W.M. Artificial gene amplification reveals an abundance of promiscuous resistance determinants in Escherichia coli. Proc. Natl. Acad. Sci. USA 2011, 108:1484-1489.
65. Sun X., Dennis J.J. A novel insertion sequence derepresses efflux pump expression and preadapts Pseudomonas putida S12 for extreme solvent stress. J. Bacteriol. 2009, 191:6773-6777.
66. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T., Vaitkevicius K., Barthelemy M., Vergassola M., Nahori M.A., Soubigou G., Regnault B., Coppee J.Y., Lecuit M., Johansson J., Cossart P. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459:950-956.
67. Tomljenovic-Berube A.M., Mulder D.T., Whiteside M.D., Brinkman F.S., Coombes B.K. Identification of the regulatory logic controlling Salmonella pathoadaptation by the SsrA-SsrB two-component system. PLoS Genet. 2010, 6:e1000875.
68. Tu K.C., Bassler B.L. Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev. 2007, 21:221-233.
69. Tu K.C., Long T., Svenningsen S.L., Wingreen N.S., Bassler B.L. Negative feedback loops involving small regulatory RNAs precisely control the Vibrio harveyi quorum-sensing response. Mol. Cell 2010, 37:567-579.
70. van Hijum S.A., Medema M.H., Kuipers O.P. Mechanisms and evolution of control logic in prokaryotic transcriptional regulation. Microbiol. Mol. Biol. Rev. 2009, 73:481-509.
71. Wilson M.D., Odom D.T. Evolution of transcriptional control in mammals. Curr. Opin. Genet. Dev. 2009, 19:579-585.
72. Wilson M.D., Barbosa-Morais N.L., Schmidt D., Conboy C.M., Vanes L., Tybulewicz V.L., Fisher E.M., Tavare S., Odom D.T. Species-specific transcription in mice carrying human chromosome 21. Science 2008, 322:434-438.
73. Winfield M.D., Groisman E.A. Phenotypic differences between Salmonella and Escherichia coli resulting from the disparate regulation of homologous genes. Proc. Natl. Acad. Sci. USA 2004, 101:17162-17167.
74. Winfield M.D., Latifi T., Groisman E.A. Transcriptional regulation of the 4-amino-4-deoxy-L-arabinose biosynthetic genes in Yersinia pestis. J. Biol. Chem. 2005, 280:14765-14772.
75. Yip E.S., Grublesky B.T., Hussa E.A., Visick K.L. A novel, conserved cluster of genes promotes symbiotic colonization and sigma-dependent biofilm formation by Vibrio fischeri. Mol. Microbiol. 2005, 57:1485-1498.
76. Zhang J. Evolution by gene duplication: an update. Trends Ecol. Evol. 2003, 16:292-298.
77. Zhang Z., Saier M.H. A novel mechanism of transposon-mediated gene activation. PLoS Genet. 2009, 5:e1000689.
78. Zhang Z., Saier M.H. A mechanism of transposon-mediated directed mutation. Mol. Microbiol. 2009, 74:29-43.